The history of tomato: From domestication to biopharming

Véronique Bergougnoux

The history of tomato: From domestication to biopharming

2014, Biotechnology Advances

Abstract

Imported from the Andean region to Europe in the 16th century, today tomato is widespread throughout the 19 world and represents the most economically important vegetable crop worldwide. Tomato is not only traded 20 in the fresh market but is also used in the processing industry in soups, as paste, concentrate, juice, and ketchup. 21 It is an incredible source of important nutrients such as lycopene, β-carotene and vitamin C, which all have 22 positive impacts on human health. Its production and consumption is increasing with population growth. In 23 this review, we report how tomato was already domesticated by the ancient Incan and Aztec civilizations, and 24 how it came to Europe, where its breeding history started. The development of genetic, molecular biology and 25 plant biotechnology have opened the doors towards the modern genetic engineering of tomato. The different 26 goals of tomato genetic engineering are presented, as well as examples of successfully engineered tomatoes in 27 terms of resistance to biotic and abiotic stresses, and fruit quality. The development of GM tomato for 28 biopharming is also described.

Figures (17)

Fig. 1. Metrics of tomato production in the world. 1A— Tomato production and the area dedicated to tomato culture worldwide for the period 1990-2011 The frame depicts the increase ir tomato consumption for the same period. 1B— Weight (in %) of the different continents in tomato production, comparison between 1990 and 2010. 1C— Production of the nine leadins producers (source: FAO Statistics; http://faostat3.fao.org/home/index.html). Today, tomato is not only sold fresh but also processed as paste, soup, juice, sauce, powder, concentrate or whole. Tomato is one of the most consumed vegetables in the world, after potatoes and before on- ions (FAOSTAT, http://faostat3.fao.org/home/index.html), and probably the most preferred garden crop. With worldwide production reaching almost 160 million tons in 2011, tomato is the seventh most important crop species after maize, rice, wheat, potatoes, soybeans and cassava. During the last 20 years, tomato production, as well as the area dedicat- ed to its culture, has doubled (Fig. 1A). Surprisingly, whereas 20 years ago, Europe and the Americas represented the most important pro- ducers, today Asia dominates the tomato market with China ranking first, followed in decreasing order by India, USA, Turkey, Egypt, Iran, Italy, Brazil, Spain and Uzbekistan (Fig. 1B-C). Interestingly the coun- tries harboring the highest yield are from northern Europe, where the climatic conditions are not favorable to the culture of tomato and where the area dedicated to tomato culture is very small (Table 1). It is noteworthy that these countries produce most of their tomatoes ae Lee eee From the botanical point of view, tomato (Solanum lycopersicum L.) is a fruit berry, and not a vegetable. This misunderstanding was a ques- tion of debates during the 19th century in USA, with the special case of Nix vs. Hedden — 149 U.S. 304 (1893). In 1887, Nix contested the de- cision of the tax collector of the port of New York to recover taxes on tomatoes imported from the West Indies in the spring of 1886, which the collector assessed as a vegetable. The court opined: “Botanically speaking, tomatoes are the fruit of a vine, just as are cucumbers, squashes, beans, and peas. But in the common language of the people, [...] all these are vegetables which are grown in kitchen gardens, and which, whether eaten cooked or raw, are, like potatoes, carrots, parsnips, turnips, beets, cauliflower, cabbage, celery, and lettuce, usually served at 9 91 92 9% 94 9E 9¢ 97 98 os 1¢ 1¢

Tomato yield in different countries and comparison with production rank and harvested area. Table 1 dinner in, with, or after the soup, fish, or meats which constitute the principal part of the repast, and not, like fruits generally, as dessert.” (http://supreme.justia.com/cases/federal/us/149/304/case.html).

Food supply quantity (kg/capita/year) in the 15 countries consuming the most tomatoes The countries with the highest production are highlighted in pale gray. Table 2

Fig. 2. General phylogenetic tree based on the analysis of GBSSI gene sequences from 65 accessions of the 9 tomato species and 14 outgroup taxa. Numbers indicate bootstrap values, an decay values are indicated between parentheses. Extracted from Peralta and Spooner (2005).

Comparison of wild tomato species (Solanum L. section Lycopersicon subsection Lycopersicon) adapted from Peralta et al. (2005) and Spooner et al. (2005). SC: self-compatible, SI: self-incompatible, At: autogamous, Al: allogamou Table 3

Fig. 3. Schematic representation of development of the flower into a fruit after pollination/fertilization (A) and of the physiological processes occurring during fruit development (B, from Tanksley, 2004).

Fig. 4. Ethylene biosynthetic pathway and ripening regulated processes. 1: adomet synthetase, 2: kinase, 3: aminotransferase, 4: ACC synthase (ACS), 5: ACC oxydase (ACO).

Fig. 5. Carotenoids biosynthetic pathway and tomato mutants. Pictures are from the Tomato Genetic Resource Centre. ABA: abscissic acid; AO, adldehyde oxidase; CrtR-b: carotene- hydroxylase; Cyc-B: chromoplast specific lycopene synthase; DMAPP: dimethylally!l diphosphate; GPP: genaryl diphosphate; GGPP: geranylgeranyl diphosphate; Ggps: GGPP- synthase; IPP: isopentenyl diphosphate; Lcy-b: lycopene [-cyclase; Lcy-e: lycopene ¢-cyclase; MEP: methylerythritolphosphate; Nxs: neoxanthin synthase; Pds: phytoene desaturase; Psy: phytoene synthase; Vde1: violaxanthin deepoxidase; VNCED: 9-cis-epoxycarotenoid dioxygenase; Zds: ¢-carotene desaturase; Zep1: zeaxanthin epoxidase. ripens slowly and has an extended shelf-life. Interestingly, the rin muta- tion in its form rin/Rin constitutes the basis for most of the tomato hy- 51: brids with slow ripening and long shelf-life (Giovannoni, 2007). Ina recent study, Martel et al. (2011) demonstrated that RIN interacts the NAC domain family (Martel et al., 2011; Vrebalov et al., 2002). If these mutations are homozygous, the process of ripening is inhibited, the fruits remain yellow or light orange and can be stored for months at room temperature. When the mutations are heterozygous, the fruit

Nutritional value of 100 g of red fresh tomato (source: USDA, http://www.usda.gov/wps/ portal/usda/usdahome).

Non-exhaustive list of agronomic traits of interest available from wild tomato species (extracted from Foolad, 2007, for more details see the references therein). Table 6

Non-exhaustive list of successful tomato engineering. References can be found in Rajan et al. (2007) and Di Matteo et al. (2011). References in bold are discussed in the text. Table 7

JBA-06761; No of Pages 20 Biotechnology Advances xxx (2013) xxx–xxx Contents lists available at ScienceDirect Biotechnology Advances journal homepage: www.elsevier.com/locate/biotechadv Research review paper 2 The history of tomato: From domestication to biopharming 3Q1 Veronique Bergougnoux 1 4 Department of Molecular Biology, Center of the Region Haná for Biotechnological Research, Palacký University, Šlechtitelů 11, 783 71 Olomouc, Czech Republic R O O F 1 5 a r t i c l e i n f o a b s t r a c t Imported from the Andean region to Europe in the 16th century, today tomato is widespread throughout the world and represents the most economically important vegetable crop worldwide. Tomato is not only traded in the fresh market but is also used in the processing industry in soups, as paste, concentrate, juice, and ketchup. It is an incredible source of important nutrients such as lycopene, β-carotene and vitamin C, which all have positive impacts on human health. Its production and consumption is increasing with population growth. In this review, we report how tomato was already domesticated by the ancient Incan and Aztec civilizations, and how it came to Europe, where its breeding history started. The development of genetic, molecular biology and plant biotechnology have opened the doors towards the modern genetic engineering of tomato. The different goals of tomato genetic engineering are presented, as well as examples of successfully engineered tomatoes in terms of resistance to biotic and abiotic stresses, and fruit quality. The development of GM tomato for biopharming is also described. © 2013 Published by Elsevier Inc. Available online xxxx P Keywords: Tomato Domestication Breeding Genetic engineering Biopharming E D 76 8 190 11 12 13 14 15 16 17 C Introduction to tomato . . . . . . . . . . . . . . . . . . . . . . 1.1. Economic importance of tomato and its botanical description . 1.2. Habitat and diversity of tomato . . . . . . . . . . . . . . . 1.3. History of domestication . . . . . . . . . . . . . . . . . . 1.4. The tomato today: a model organism for scientists . . . . . . 2. Challenges of tomato breeding and genetic bases of important traits . 2.1. Tomato yields . . . . . . . . . . . . . . . . . . . . . . . 2.2. Resistance to biotic and abiotic stresses . . . . . . . . . . . 2.3. Size and shape of fruit . . . . . . . . . . . . . . . . . . . 2.4. Ripening and color establishment . . . . . . . . . . . . . . 2.5. Nutritional value . . . . . . . . . . . . . . . . . . . . . 2.6. Limits of classical breeding: the new area of genetic engineering 3. Genetic engineering of tomato . . . . . . . . . . . . . . . . . . . 3.1. Agrobacterium-mediated transformation of tomato . . . . . . 3.2. Selection of transgenic plants . . . . . . . . . . . . . . . . 3.3. Temporal and/or organ-speciﬁc expression: choice of promoter 4. Transgenic tomatoes with enhanced agronomic traits . . . . . . . . 4.1. Resistance to biotic stresses . . . . . . . . . . . . . . . . 4.2. Resistance to abiotic stresses . . . . . . . . . . . . . . . . 4.3. Fruit quality . . . . . . . . . . . . . . . . . . . . . . . . 4.4. Biopharming . . . . . . . . . . . . . . . . . . . . . . . 5. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . 6. Uncited references . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C O R R E 1. N 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 Contents U 32 35 34 30 31 T 33 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61 1 18 19 20 21 22 23 24 25 26 27 28 29 E-mail address: veronique.bergougnoux@upol.cz. Tel.: +420 585 634 740. 0734-9750/$ – see front matter © 2013 Published by Elsevier Inc. http://dx.doi.org/10.1016/j.biotechadv.2013.11.003 Please cite this article as: Bergougnoux V, The history of tomato: From domestication to biopharming, Biotechnol Adv (2013), http://dx.doi.org/ 10.1016/j.biotechadv.2013.11.003 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 V. Bergougnoux / Biotechnology Advances xxx (2013) xxx–xxx 64 65 Today, tomato is not only sold fresh but also processed as paste, soup, juice, sauce, powder, concentrate or whole. Tomato is one of the most consumed vegetables in the world, after potatoes and before onions (FAOSTAT, http://faostat3.fao.org/home/index.html), and probably the most preferred garden crop. With worldwide production reaching almost 160 million tons in 2011, tomato is the seventh most important crop species after maize, rice, wheat, potatoes, soybeans and cassava. During the last 20 years, tomato production, as well as the area dedicated to its culture, has doubled (Fig. 1A). Surprisingly, whereas 20 years ago, Europe and the Americas represented the most important producers, today Asia dominates the tomato market with China ranking ﬁrst, followed in decreasing order by India, USA, Turkey, Egypt, Iran, Italy, Brazil, Spain and Uzbekistan (Fig. 1B–C). Interestingly the countries harboring the highest yield are from northern Europe, where the climatic conditions are not favorable to the culture of tomato and where the area dedicated to tomato culture is very small (Table 1). It is noteworthy that these countries produce most of their tomatoes D E T 79 80 C 77 78 E 75 76 R 73 74 R 71 72 O 69 70 C 67 68 U N 66 F 1.1. Economic importance of tomato and its botanical description O 63 under controlled greenhouse conditions. The recent increase in tomato production responds to the increased consumption of tomatoes during the same period (Fig. 1A), reaching an average consumption of 20.5 kg/capita/year in 2009. The three countries where tomato is consumed the most are Libya, Egypt and Greece, with consumption exceeding 100 kg/capita/year. From a general point of view, it is in the Mediterranean and Arabian countries that the consumption of tomatoes is the highest with averages between 40 and 100 kg/capita/ year (Table 2). From the botanical point of view, tomato (Solanum lycopersicum L.) is a fruit berry, and not a vegetable. This misunderstanding was a question of debates during the 19th century in USA, with the special case of Nix vs. Hedden — 149 U.S. 304 (1893). In 1887, Nix contested the decision of the tax collector of the port of New York to recover taxes on tomatoes imported from the West Indies in the spring of 1886, which the collector assessed as a vegetable. The court opined: “Botanically speaking, tomatoes are the fruit of a vine, just as are cucumbers, squashes, beans, and peas. But in the common language of the people, […] all these are vegetables which are grown in kitchen gardens, and which, whether eaten cooked or raw, are, like potatoes, carrots, parsnips, turnips, beets, cauliﬂower, cabbage, celery, and lettuce, usually served at R O 1. Introduction to tomato P 62 Fig. 1. Metrics of tomato production in the world. 1A— Tomato production and the area dedicated to tomato culture worldwide for the period 1990–2011 The frame depicts the increase in tomato consumption for the same period. 1B— Weight (in %) of the different continents in tomato production, comparison between 1990 and 2010. 1C— Production of the nine leading producers (source: FAO Statistics; http://faostat3.fao.org/home/index.html). Please cite this article as: Bergougnoux V, The history of tomato: From domestication to biopharming, Biotechnol Adv (2013), http://dx.doi.org/ 10.1016/j.biotechadv.2013.11.003 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 3 V. Bergougnoux / Biotechnology Advances xxx (2013) xxx–xxx Table 1 Tomato yield in different countries and comparison with production rank and harvested area. Yield (Hg/Ha) Rank of production Harvested area (Ha) 4,788,484 4,608,333 4,237,742 4,157,407 4,131,563 4,012,500 3,550,000 3,523,070 2,821,458 2,723,730 848,833 765,630 617,947 572,919 492,714 445,690 408,162 381,521 371,025 194,520 25 55 117 75 116 143 113 93 115 87 3 9 8 7 1 10 4 5 6 2 1702 474 31 216 32 4 40 114 48 185 148,730 49,913 71,473 103,858 985,903 58,000 269,584 212,446 183,931 865,000 t2:1 t2:2 t2:3 Table 2 Food supply quantity (kg/capita/year) in the 15 countries consuming the most tomatoes. The countries with the highest production are highlighted in pale gray. 117 118 119 120 121 122 123 124 125 C E 115 116 R 113 114 R 111 112 O 109 110 C 107 108 N 105 106 U 103 104 T 126 dinner in, with, or after the soup, ﬁsh, or meats which constitute the principal part of the repast, and not, like fruits generally, as dessert.” (http://supreme.justia.com/cases/federal/us/149/304/case.html). The tomato belongs to the Solanaceae family, containing more than 3000 species including many plants of economic importance including potatoes, eggplants, petunias, tobacco, peppers (Capsicum) and Physalis. Solanum is the largest genus in the Solanaceae family, encompassing 1250 to 1700 species. Species of the Solanum genus are present on all temperate and tropical continents and are remarkable for their morphological and ecological diversity. Solanum is probably the most economically important genus, containing crop species and many other species producing poisonous or medicinal compounds (Weese and Bohs, 2007). Since its introduction in Europe in the 16th century, it was assumed that the tomato was closely related to the genus Solanum and was identiﬁed as Solanum pomiferum. In 1753, Linnaeus classiﬁed for the ﬁrst time tomatoes in the genus Solanum under the speciﬁc name of S. lycopersicum. Nevertheless, the genus and designation of tomato were for a long time a subject of debate, as reported by several authors (Foolad, 2007; Peralta and Spooner, 2007). The use of molecular data allowed revision of the phylogenetic classiﬁcation of the Solanaceae and the genus Lycopersicon was re-introduced in the Solanum genus into the section Lycopersicon. It is interesting to note that 200 years of debate were necessary to conﬁrm the description of Linnaeus. The ingroup organization of tomato has also evolved since the ﬁrst description in 1940 done by Müller, who identiﬁed six tomato species 102 R O O F Country Netherlands Belgium Norway United Kingdom Ireland Iceland Denmark Finland Sweden Austria United States of America Spain Brazil Italy China Uzbekistan Turkey Egypt Iran India t2:4 Country t2:5 t2:6 t2:7 t2:8 t2:9 t2:10 t2:11 t2:12 t2:13 t2:14 t2:15 t2:16 t2:17 t2:18 t2:19 Libya Egypt Greece Tunisia Turkey Armenia Lebanon Uzbekistan Iran Italy Spain Cuba United Arab Emirates Portugal Turkmenistan Food supply quantity (kg/capita/year) Rank of production 150.3 115.9 105.3 94.9 90.5 87.3 75.4 74.4 71.6 60.5 58.9 58.7 57.8 57.7 50.2 54 5 18 101 13 50 45 106 6 7 133 33 3 16 68 separated into two sections: subgenus eulycopersicon, including Lycopersicon esculentum and Lycopersicon pimpinellifolium; and the subgenus eriopersicon, regrouping Lycopersicon peruvianum, Lycopersicon cheesmaniae, Lycopersicon hirsutum and Lycopersicon glandulosum. Rick (1960, 1979) proposed a tomato classiﬁcation relying on the ability of the wild species to cross with the cultivated tomato. He recognized nine wild tomato species divided into two main groups according their crossability: the Esculentum and Peruvianum complexes. All the species of the Esculentum complex (L. esculentum, L. pimpinellifolium, L. cheesmaniae, Lycopersicon pennellii, L. hirsutum, Lycopersicon chmielewskii and Lycopersicon parviﬂorum) can be hybridized with the cultivated tomato and represent potential sources of resistance to biotic and abiotic stresses as well as other desirable characters; the species from the Peruvianum complex (Lycopersicon chilense and L. peruvianum) are extremely diverse and represent real potential for crop improvement. The use of these latter species was strongly limited due to their poor hybridization capacity with the cultivated tomato and the necessity to develop special methods such as embryo rescue (Foolad, 2007). The actual description of the tomato is more complex than was thought initially and Peralta and Spooner (2001) reported the ﬁnal organization of the Solanum sec. Lycopersicon. Their phylogenetic study, based on the sequence of the granule-bound starch synthase (GBSSI) gene, allowed them to ascertain the outgroup organization within the Solanum subgenus Potatoe. This study supported Solanum juglandifolium and Solanum ochranthum as the closest outgroup of tomato (Fig. 2) and divided ﬁnally the tomato into three groups: sect. Lycopersicon “subsect. Lycopersicon”, ser. Lycopersicon, ser. Eriopersicon and ser. Neolycopersicon. The ﬁnal classiﬁcation of tomato recognizes the cultivated tomato (S. lycopersicum) and its twelve wild relatives, the two species Solanum galapense and Solanum cheesmaniae being endemic to the Galapagos Islands. The species Solanum peruvianum was divided into northern and southern species, and a more precise analysis identiﬁed four species: Solanum arcanum, Solanum huaylasense, S. peruvianum and Solanum corneliomulleri (Peralta et al., 2005, 2008). The different wild tomato species, according to their relationships into the Solanum genus, are summarized in Table 3. 127 Q61 1.2. Habitat and diversity of tomato 164 Wild tomato species are native to western South America along the coast and high Andes from central Ecuador, through Peru, to northern Chile, and in the Galapagos Islands. Consequently tomato wild species grow in a variety of habitats ranging from sea level on the Paciﬁc coast 165 P 1 2 3 4 5 6 7 8 9 10 19 24 35 40 45 46 48 55 57 92 D t1:3 t1:4 t1:5 t1:6 t1:7 t1:8 t1:9 t1:10 t1:11 t1:12 t1:13 t1:14 t1:15 t1:16 t1:17 t1:18 t1:19 t1:20 t1:21 t1:22 t1:23 E t1:1 t1:2 Please cite this article as: Bergougnoux V, The history of tomato: From domestication to biopharming, Biotechnol Adv (2013), http://dx.doi.org/ 10.1016/j.biotechadv.2013.11.003 128 Q62 129 Q63 Q64 130 Q65 Q66 131 132 133 134 135 136 Q67 Q68 Q69 137 138 139 140 141 Q70 142 143 144 145 146 147 148 149 150 Q71 151 Q72 152 153 154 155 156 Q73 Q74 157 Q75 158 159 Q76 160 Q77 Q78 161 162 163 166 167 168 4 R O O F V. Bergougnoux / Biotechnology Advances xxx (2013) xxx–xxx Fig. 2. General phylogenetic tree based on the analysis of GBSSI gene sequences from 65 accessions of the 9 tomato species and 14 outgroup taxa. Numbers indicate bootstrap values, and decay values are indicated between parentheses. Extracted from Peralta and Spooner (2005). up to 3300 m asl. in the Andean Highlands, and from arid to rainy climates (Table 3). Tomato wild species are often restricted to narrow 171 and isolated valleys where they adapted to particular climatic and soil 172 types. It is probable that the Andean geography, the diverse ecological 173 habitats and the different climates together contributed to wild tomato 174 diversity. This hypothesis is supported by a very recent study based on Q79 the two closely related wild tomato species S. lycopersicum and Solanum 175 176 pimpinellifolium (Nakazato and Housworth, 2011). This diversity is 177 expressed through morphological, physiological and sexual characteris178 tics (Peralta and Spooner, 2005; Spooner et al., 2005). 179 The mating system plays a key role in species diversiﬁcation and 180 outcrossing constitutes an important and widespread strategy for main181 taining genetic variability. Genetically controlled self-incompatibility 182 is a very common mechanism in the plant kingdom. In tomato, the 183 self-incompatibility is gametophytic and varies from allogamous self184 incompatible, to facultative allogamous, to autogamous and self185 compatible (Table 3). Self-incompatibility is strongly correlated 186 with the degree of outcrossing, allelic diversity, ﬂoral display and de187 gree of stigma exsertion in wild tomatoes (Peralta et al., 2008). Indeed, 188 an exserted stigma above the anthers will promote outcrossing by buzz 189 pollination, whereas a recessed stigma below the anthers will promote 190 self-fertilization (Chen and Tanksley, 2004). By investigating the bases 191 of self-compatibility/-incompatibility and ﬂower characteristics, Rick 192 (1982) came to the conclusion that the mating system evolved from 193 self-incompatible, as the ancestral condition, to self-compatible. Chang194 es from self-incompatibility to self-compatibility are events which are 195 expected to happen infrequently and independently. This is the case Q81196 Q80 of Solanum habrochaites and Solanum pennellii, for which both self197 compatible and self-incompatible populations have been identiﬁed 198 (Rick, 1982). The self-incompatible populations have a higher degree 199 of diversity, larger ﬂower parts, and exserted stigma, as opposed to 200 self-compatible populations characterized by reduced genetic diversity, 201 smaller ﬂower parts and little or no stigma exsertion. Thus, in tomato, 202 ﬂower stigma exsertion and gametophytic incompatibility contribute 203 to greater outcrossing and genetic diversity. D E T C E R R O C U N 204 1.3. History of domestication 205 206 Despite the centuries since tomato was introduced to Europe, the origin of its domestication is still unclear, and two hypotheses are still being contended: the Peruvian and Mexican hypotheses. How can the place of domestication of a crop be determined? In an attempt to solve this question, DeCandolle (1886) used an approach combining 207 208 209 botany, archeology and paleontology, history and philology. Botany consists of observing the natural occurrence of the crop and/or its putative relative wild species; archeology and paleontology focus on studying fossils from caves, burial sites or other preserved deposits; history looks for evidence of the crop in the early reports of people; and ﬁnally philology or linguistic evidence is based on the comparison of native names to prior languages. DeCandolle expressed for the ﬁrst time the Peruvian origin of tomato domestication. His conclusions were based on the fact that: i) no unambiguous natural records of tomato were identiﬁed out of the Americas after its European discovery, ii) “mala peruviana” and “pomi del Peru” were used to refer to the tomato, suggesting its initial domestication and transport from Peru to Europe, iii) the cultivated tomato was thought to originate from the wild cherry tomato which was known to be localized from coastal Peru through Mexico to the southwestern USA (California), iv) the distribution of the cultivated tomato and its progenitors arose from Peru by garden escapes, v) the domestication occurred before the discovery of America but not very long before that (reviewed in Peralta and Spooner, 2007). The Mexican origin of domestication was proposed by Jenkins in 1948. It was mainly justiﬁed by the fact that no evidence of pre-Colombian tomato cultivation in South America was available, compared to good evidence in Mexico. Following the philology, Jenkins also argued that the name “tomato” comes from the Mexican Nahua word “tomatl” which refers to “plants bearing globous and juicy fruit” (Bauchet and Causse, 2012). However to date, the origin of the domestication of tomato is unsolved, even though it has been reported that tomatoes from Europe and North America share similar isozymes and molecular markers with those from Mexico and Central America, suggesting that the tomato was introduced to Europe and North America from these regions (Bauchet and Causse, 2012; Peralta and Spooner, 2007). None of the hypotheses on the origin of tomato domestication is more conclusive than the other. It might be that domestication occurred independently in both regions. The most likely ancestor of cultivated tomatoes is the wild cherry tomato, usually identiﬁed as Solanum lycopersicum var. cerasiforme because of its wide representation in Central America. Nevertheless the genetic investigations made by Nesbitt and Tanksley in 2002 demonstrated that the plants known as “cerasiforme” are a mixture of wild and cultivated tomatoes, rather than the direct ancestor of the cultivated tomato. A very recent study based on the analysis of single nucleotide polymorphisms not only conﬁrms that S. lycopersicum var. cerasiforme is not the ancestor of the cultivated tomato but also reinforces the model that a pre-domestication of the tomato occurred in the P 169 170 Please cite this article as: Bergougnoux V, The history of tomato: From domestication to biopharming, Biotechnol Adv (2013), http://dx.doi.org/ 10.1016/j.biotechadv.2013.11.003 210 211 212 213 214 215 216 217 218 219 220 221 222 223 224 225 226 227 228 229 230 231 232 233 234 235 236 237 238 239 240 241 242 243 244 Q82 245 246 247 248 249 250 251 252 N C Table 3 Comparison of wild tomato species (Solanum L. section Lycopersicon subsection Lycopersicon) adapted from Peralta et al. (2005) and Spooner et al. (2005). SC: self-compatible, SI: self-incompatible, At: autogamous, Al: allogamous. O t3:3 Species (Solanum name) Lycopersicon equivalent Distribution and habitat t3:4 S. cheesmaniae L. cheesmaniae t3:5 S. galapagense L. cheesmaniae var. minor t3:6 S. lycopersicum L. esculentum t3:7 S. pimpinellifolium L. pimpinellifolium t3:8 S. chilense L. chilense t3:9 t3:10 S. chmielewskii S. habrochaites L. chmielewskii L. hirsutum t3:11 S. pennellii L. pennellii t3:12 S. neorickii L. parviﬂorum t3:13 S. peruvianum north Endemic to the Galapagos Islands, Ecuador; wide variety of habitat; sea level to 500 m Endemic to the Galapagos Islands; mostly occurring on coastal lava to within 1 m of high tide mark within range of sea spray, but occasionally inland; sea level to 50 m Known only from cultivation or escapes; world-wide in a variety of habitats, many escaped plants have smaller fruits (“cerasiforme”); sea level to 4000 m Central Ecuador to central Chile; dry coastal habitats; 0-500 m but exceptionally up to 1400 m S Peru to N Chile; in hyper-arid rocky plains and coastal deserts; sea level to 3250 m S Peru to N Bolivia; high dry Andean valleys; 1600-3200 m Central Ecuador to Central Peru, on the western slopes of the Andes; in a variety of forest types from premontane forest to dry forests; (40)-200-3300 m N Peru to N Chile; dry rocky hillsides and sandy areas; sea level to 2300 m S Ecuador to S Peru; dry inter-Andean valleys, often found trailing over rocky banks and roadsides; (920)-1950-2600 m N Peru, coastal and inland Andean valleys; lomas, dry valleys and dry rocky slopes; 100 to 2800 m N Peru; rocky slopes of the Callejon de Huaylas along the Rio Santa and in the adjacent Rio Fortaleza drainage; (940)1700-3000 m Central Peru to N Chile; coastal lomas formations and occasionally in coastal deserts, occasionally as a weed at ﬁeld edges in coastal river valleys; sea level to 600 m Central to S Peru, W slops of the Andes; landslides and rocky slopes; (40)200-3300 m t3:14 t3:15 t3:16 S. peruvianum south S. arcanum S. huaylasense L. peruvianum var. hirsutum L. peruvianum S. peruvianum L. peruvianum S. corneliomuelleri L. peruvianum var. glandulosum R R E C T E Fruit color Reproductive system Importance for breeding purposes Yellow, orange SC, exclusively At Salt tolerance; Lepidoptera and virus resistance Salt tolerance; Lepidoptera and virus resistance Yellow, orange SC, exclusively At Red SC, facultative Al Moisture-tolerance, resistance to wilt, root-rotting, and leaf-spotting fungi Red SC, At, facultative Al Green, purple stripes SC, Al Color and fruit quality; resistance to insect, nematode and disease Drought resistance Green Green SC, facultative Al SI High sugar content Cold and frost tolerance; resistance to insects due to their glandular hairs SI Drought resistance; resistance to insects D Green P Pale green SC, At Green Typically SI, Al, rare population SC, At with a trend to reduce variability in Northern races Green Green Green R O Resistance to virus, bacteria, fungi, aphid and nematode V. Bergougnoux / Biotechnology Advances xxx (2013) xxx–xxx Please cite this article as: Bergougnoux V, The history of tomato: From domestication to biopharming, Biotechnol Adv (2013), http://dx.doi.org/ 10.1016/j.biotechadv.2013.11.003 t3:1 t3:2 U O F 5 6 276 277 278 279 280 281 282 283 284 285 286 287 288 289 290 291 292 293 294 295 296 297 298 299 300 301 302 303 304 305 306 307 308 309 310 311 312 313 314 315 316 317 318 t4:4 t4:5 t4:6 t4:7 Pseudomonas syringae pv. syringae t4:8 t4:9 t4:10 Alternaria alternata f.sp. lycopersici Alternaria alternata, Stemphylium botryosum, Pleospora tarda, Stemphylium herbarum, Pleospora herbarum, Ulocladium consortiale Alternaria alternata Alternaria solani Fusarium oxysporum f.sp. radicis-lycopersici t4:11 t4:12 F Black shoulder Early blight Fusarium crown and root rot Fusarium wilt Gray mold Late blight Leaf mold Powdery mildew Pythium damping-off and fruit rot Verticillium wilt White mold O Alternaria stem canker Black mold rot Fusarium oxysporum f.sp. lycopersici Botrytis cinerea, Botryotinia fuckeliana Phytophthora infestans Fulvia fulva Oidiopsis sicula, Leveillula taurica Pythium aphanidermatum, Pythium arrhenomanes, Pythium debaryanum, Pythium myriotylum, Pythium ultimum Verticillium albo-atrum, Verticillium dahliae Sclerotinia sclerotiorum, Sclerotinia minor R O 274 275 Clavibacter michiganensis subsp. michiganensis Pseudomonas syringae pv. tomato Xanthomonas campestris pv. vesicatoria Erwinia carotovora subsp. carotovora Fungal diseases P 272 273 t4:1 t4:2 t4:3 Nematodes, parasitic Root-knot Sting Stubby-root D 270 271 Bacterial diseases Bacterial canker Bacterial speck Bacterial spot Bacterial stem rot and fruit rot Syringae leaf spot E 268 269 Table 4 Non exhaustive list of important pests and diseases of tomato with their causal agents. T 266 267 C 264 265 E 262 263 R 260 261 R 259 O 257 258 C 255 256 Andean region (Peruvian hypothesis), with the domestication being completed in Mesoamerica (Mexican hypothesis), followed by its introduction to Europe by Spaniards and then spread all over the world (Blanca et al., 2012). The history of tomato's use (and probable consequent domestication) was reported by George McCue (1952), who did a remarkable bibliographical investigation. It was probably the Spanish conquistador Cortes who ﬁrst introduced the small yellow tomato to Spain after the capture in 1521 of Tenochtitlan, the Aztec city known today as Mexico City. From Spain, the tomato reached Italy through Naples, which was Spanish property at that time. The ﬁrst description of the tomato in Europe was found in a herbarium written in 1544 by Petrus Matthiolius. Due to its botanical closeness with the mandrake, Matthiolius described the tomato thusly: “another species [of Mandrake] has been brought to Italy in our time, ﬂattened like the melerose and segmented, green at ﬁrst and when ripe of a golden color, which is eaten in the same manner [as the eggplant – fried in oil with salt and pepper, like mushrooms]”. Tomato was probably used for human consumption very early after its introduction to Europe as cookbooks referred to its use in gazpacho by the beginning of the 17th century. Nevertheless, due to its resemblance with toxic Solanum, such as mandrake and belladonna, the tomato was long used only for ornamental purposes. Thus, in Italy, the fruit was used solely as decoration and was incorporated into the local cuisine only late in the 17th or early 18th century. In 1760, Blois reported that tomato was used in France for its ornamental properties and 18 years later, he mentioned that the catalog of seeds of the “Maison grainiere Andrieux Vilmorin”, which still exists to this day, offered seeds of tomato as a vegetable. Following a south/north axis, tomato consumption expanded to the north. In England, tomato consumption was very common by the mid-18th century. From England, tomatoes were “exported” to the Middle East/Asia by John Baker, British consul in Aleppo. Tomatoes migrated then to North America due to English colonization. The real domestication of the tomato as an edible vegetable started during the 19th century. Thus, in 1820, Sabine referenced that four red tomatoes and two yellow were cultivated in Europe; he even gave advice on how to cultivate them in the speciﬁc conditions of England. In America, Alexander W. Livington promoted the tomato and was the ﬁrst to be able to improve the wild tomato, developing and stabilizing the plants. This contribution to tomato development in the USA was so important that in 1937 it was admitted that the majority of the varieties resulted from the ability of Livington to “evaluate and perpetuate superior material in the tomato”. The numerous cultivars available since the end of the 19th century were produced by open pollination under the auspices of farms or small collectives. Development of new cultivars happened by spontaneous mutation, natural outcrossing or recombination of pre-existing genetic variation (Bauchet and Causse, 2012). Because tomatoes are mostly autogamous (Table 4), crosses between two different individuals were quite rare and the plants developing from the seeds had a parental phenotype. This allowed obtaining and maintaining ﬁxed populations called “heirlooms” which were unique in their size, color and shape. The best example of tomato breeding is probably the one of Alexander Livingston, who wanted to obtain tomato fruits smooth in shape, uniform in size and with better ﬂavor. For this purpose, he selected in his ﬁeld tomatoes with different traits. He saved the seeds, grew them in ﬁelds, selected repeatedly over 5 years, until he obtained a ﬂeshier and larger fruit (1893, reprint 1998). In 1870, he introduced on the market the cultivar Paragon which is still grown today in the USA. With expansion of tomato's use, the 20th century was marked by the development of private seed industries which developed the principle of the F1 hybrid. Indeed, hybrids combine the agronomical traits of the two parents, but because these characters segregate in the progeny, farmers are not able to maintain these hybrids by seed collecting and further ﬁeld exploitation, forcing them to buy new seeds each growing season (Bai and Lindhout, 2007). From an evolutionary point of view, domestication and breeding programs induced drastic physiological U N 253 254 V. Bergougnoux / Biotechnology Advances xxx (2013) xxx–xxx Meloidogyne spp. Belonolaimus longicaudatus Paratrichodorus spp., Trichodorus spp. Viral, viroid and mycoplasmalike organisms [MLO] diseases Common mosaic of tomato Curly top Potato virus Y Tomato bushy stunt Tomato mosaic Tomato mottle Tomato spotted wilt Tomato yellow leaf curl Tomato yellow top Tomato bunchy top Tomato planto macho Aster yellows Tomato big bud t4:13 t4:14 t4:15 t4:16 t4:17 t4:18 t4:19 t4:20 t4:21 t4:22 t4:23 t4:24 t4:25 t4:26 t4:27 t4:28 t4:29 t4:30 Tobacco mosaic virus (TMV) t4:31 Curly top virus Potato virus Y Tomato bushy stunt virus Tomato mosaic virus (ToMV) Tomato mottle gemini virus Tomato spotted wilt virus Tomato yellow leaf curl virus Tomato yellow top virus Tomato bunchy top viroid Tomato planto macho viroid MLO MLO t4:32 t4:33 t4:34 t4:35 t4:36 t4:37 t4:38 t4:39 t4:40 t4:41 t4:42 t4:43 and morphological changes, but this artiﬁcial selection reduced the 319 genetic diversity of cultivated tomato. 320 1.4. The tomato today: a model organism for scientists 321 The popularity of the tomato for scientists has increased over the years, until it has become a model organism for research programs, both for applied and theoretical purposes. This is probably due to 1) the possibility of growing tomato in different conditions, allowing an understanding of the adaptability of tomato to different abiotic stresses (cold, drought, etc.), 2) its relative short life cycle, 3) its photoperiod insensitivity, i.e. the ability to ﬂower, and subsequently produce seeds in any condition of day length, 4) its high self-fertility and homozygosity, characteristics leading to the breeding of heirlooms by the end of 19th century, 5) the ease of controlled pollination and hybridization, 6) the simplicity of its genetics with a relatively small genome (estimated to be approximately 900 Mb for the inbred tomato cultivar “Heinz 1706”, which was used for the recent sequencing of the tomato genome; The Tomato Genome Consortium, 2012) and lack of gene duplication, and 7) its ability to be propagated asexually by grafting, or to regenerate whole plants from different parts of the plant. 322 Please cite this article as: Bergougnoux V, The history of tomato: From domestication to biopharming, Biotechnol Adv (2013), http://dx.doi.org/ 10.1016/j.biotechadv.2013.11.003 323 324 325 326 327 328 329 330 331 332 333 334 335 336 337 V. Bergougnoux / Biotechnology Advances xxx (2013) xxx–xxx 375 2.1. Tomato yields 376 377 385 386 Despite its potentially improved agronomical traits, a cultivar which does not have higher or at least equal yield than the already available cultivars will not be considered in breeding programs. Yield takes into account both fruit number and fruit weight. Over time, the improvement of cultural practices (notably the use of fertilizers) has contributed to the same extent as tomato breeding to increase yield. It is obvious that tomato yield is not an isolated trait, as it is strongly correlated with factors inﬂuencing the overall growth of the plant. Temperature is one of these factors inﬂuencing plant growth and indirectly yield. By breeding tomatoes for resistance to high temperatures, Scott was able to increase yield under hot and humid condition (Scott et al., 1997). 387 2.2. Resistance to biotic and abiotic stresses 388 One of the most prominent issues in tomato breeding is resistance to biotic stresses represented by destructive pests and diseases which can cause signiﬁcant economic losses (Bai and Lindhout, 2007). Tomato is the target of more than 200 pests and diseases. A non-exhaustive list is given in Table 4. These pests and diseases are controlled via chemical treatments, which produce several negative effects: development of resistance to the chemicals and the subsequent necessity to develop new chemicals, and harm to the environment, the farmer and the consumer. Moreover, their use increases the costs of crop production and is subjected to chemical-use laws. In order to limit the use of chemicals in 366 367 368 369 370 371 372 373 378 379 380 381 382 383 384 389 390 391 392 393 394 395 396 397 C 364 365 E 363 R 361 362 R 359 360 O 357 358 C 355 356 N 353 354 U 351 352 398 399 400 401 402 2.3. Size and shape of fruit 403 In order to understand the modiﬁcation of tomato fruit that occurred during domestication, it is necessary to review what a tomato fruit is. The ﬂeshy-fruit corresponds to the ovary of the plant, and is composed of an epidermis, a thick pericarp and the placental tissues surrounding the seeds (Fig. 3A). The pericarp is the outer wall of the gynoecium, which is composed of at least two carpels, determining the number of locules of the fruit. There are essentially four stages in the development of the fruit: 1) 2- to 3-weeks of ﬂower development, 2) a period of intensive mitotic division activity which is initiated by fertilization and lasts for approximately 2 weeks, 3) a period of cell expansion (up to 20-fold), characterized by intense endoreduplication and the establishment of highly polyploid cells, and 4) a ripening or maturation phase which arises after growth stops and is characterized by chemical, biochemical and structural changes (Fig. 3B; Tanksley, 2004). The most prominent changes observed during domestication and breeding of tomato are the intrinsic qualities of the fruit such as size, shape, color, fruit ﬁrmness and shelf-life. If one considers wild tomato species, the fruits are very small, intended to propagate the species and not to feed humans. But the modern cultivated tomatoes offer a large variation in fruit size, ranging from the cherry tomato (less than 20 g) to the beef tomato (up to 500 g). The potential size of the fruit depends on the cell number which is established at the pre-anthesis stage but the ﬁnal fruit size depends on the rate and duration of cell enlargement. Endoreduplication plays a major role in the cell enlargement observed during fruit development (Chevalier et al., 2011). Six QTLs seem to be responsible for the enlargement of the fruit during domestication. One of them is fruit weight 2.2 which can increase the size of the fruit by 30%. Its further description indicated that it encodes a negative repressor of cell division, and large fruits are characterized by a higher mitotic activity during the cell division phase of fruit development (Cong et al., 2002). Two loci, fasciated and locule-number, are responsible for fruit size changes via the modiﬁcation of the number of carpels in the ﬂower. The fasciated locus has a stronger effect on fruit morphology than the locule-number locus. Plants bearing the fasciated mutation can develop more than 15 locules. Nevertheless, it is noteworthy that plants developing fruits whose weight exceeds 500 g are the result of the cumulative effect of both mutations (Lippman and Tanksley, 2001). The attempt to identify the gene responsible for this phenotype revealed that the fasciated gene regulates ﬂoral meristem size and is expressed very early during ﬂoral organogenesis. Nevertheless, none of the tomato homologs of Arabidopsis genes known to regulate this process were identiﬁed as responsible for the fasciated phenotype in tomato (Barrero et al., 2006). Large choices of fruit shape are also available: round, oblate, pear-, torpedo- or bell-shaped. Today it is considered that fewer than ten QTLs are responsible for the majority of the size and shape modiﬁcations associated with the history of cultivated tomato (Tanksley, 2004). Only few of them are described here. At the beginning of the 20th century, segregation of a locus conditioning the pear-shape of tomato fruit was described in the same time as oblate- to oval-shape fruits; 75 more years were necessary before researchers demonstrated that these two phenotypes are mediated through the same gene, ovate (Ku et al., 1999). This gene is expressed during early ﬂower development and the two ﬁrst weeks following anthesis. Ovate results in a more or less pronounced asymmetric elongation, giving rise to a more or less pronounced pear shape. Interestingly, the mutation leads to different morphology depending on the genetic background in which it is expressed, suggesting that ovate interacts with an unknown locus (Tanksley, 2004; Van der Knaap and Tanksley, 2001). The ovate gene encodes a nuclear 404 405 R O O F 374 Domestication is characterized by the modiﬁcation of a wide range of morphological and physiological traits of the crop compared to its wild ancestor. This process is called the “domestication syndrome” (Hammer 1984 in Doebley et al, 2006). The domestication syndrome varies from crop to crop but generally focuses on growth habit which becomes more compact, increased earliness of the crop, reduction/loss of seed dispersal and dormancy, gigantism and increased morphological diversity in the consumed part of the crop. In tomato, the breeding objectives are to produce and distribute new tomato cultivars with improved agronomical traits, depending on which market the cultivar is dedicated to: the fresh or the processed market. Processing tomatoes are mainly cultivated in ﬁelds, whereas fresh tomatoes are grown either in ﬁelds or in greenhouses with or without temperature control. Breeding objectives have evolved over time with the cultivars released and modiﬁcations of growing systems. Despite the fact that three main objectives are recurrent (adaptability to the environment, resistance to pests and diseases and fruit yield and quality), the breeding history has passed through four phases: breeding for yield in the 1970, for shelf-life in the 1980, for taste in the 1990 and since then for nutritional value (Bai and Lindhout, 2007; Bauchet and Causse, 2012; Causse et al., 2007; Foolad, 2007). The molecular basis of the domestication syndrome has been studied for growth habit (self-pruning, plant height and earliness) and fruit traits (set, size, shape, color, morphology). This has led to the identiﬁcation of qualitative genes and quantitative trait loci (QTLs). 345 346 P 350 344 D 2. Challenges of tomato breeding and genetic bases of important traits 342 343 E 348 349 340 341 agricultural practices, breeders turned to the wild species. Indeed the ﬁrst introgression of interesting agronomical traits from wild species to the cultivated tomato was reported by Walter (1967). He reported the development of a cultivated tomato resistant to Cladosporium fulvum, a fungus responsible for leaf mold, by crosses with S. pimpinellifolium. T 347 Other plants are already model organisms for scientists, such as Arabidopsis, maize, rice, or poplar. But ﬁrst, the tomato is phylogenetically distant from these plants, and second, it possesses speciﬁc morphological traits which are not shared with other model plants. For example, it has an indeterminate growth habit due to reiterative switches from vegetative to reproductive phases. A large set of mutants, spontaneous or induced by chemicals or irradiation, is available, and represents an important pool of resources for breeders as well as for scientists to isolate and understand the function of genes which regulate development and growth of tomato (Lozano et al., 2009). 338 339 7 Please cite this article as: Bergougnoux V, The history of tomato: From domestication to biopharming, Biotechnol Adv (2013), http://dx.doi.org/ 10.1016/j.biotechadv.2013.11.003 406 407 408 409 410 411 412 413 414 415 416 417 418 419 420 421 422 423 424 425 426 427 428 429 430 431 432 433 434 435 436 437 438 439 440 441 442 443 444 445 446 447 448 449 450 451 452 453 454 455 456 457 458 459 460 461 8 C T E D P R O O F V. Bergougnoux / Biotechnology Advances xxx (2013) xxx–xxx R E Fig. 3. Schematic representation of development of the ﬂower into a fruit after pollination/fertilization (A) and of the physiological processes occurring during fruit development (B, from Tanksley, 2004). 462 Q83 protein (Van Liu et al., 2002). Two other loci are important in the control 474 2.4. Ripening and color establishment 471 472 O 469 470 C 467 468 U N 465 466 R 473 of fruit shape: sun and fs8.1. The locus fs8.1 is responsible for the “square” tomato which is the result of adaptation of the tomato for mechanical harvest (Grandillo et al., 1996). Like ovate, fs8.1 is expressed during ovary development. As with the ovate locus, the sun mutation induces an increase in the length of fruit; but in the case of the sun mutant, the elongation occurs in both longitudinal directions, conferring a bilateral symmetry (Van der Knaap and Tanksley, 2001). Moreover, whereas ovate is expressed early during ﬂower development, sun is expressed only during the phase of cell division. All together demonstrate that, although the two mutations confer similar phenotypes, they surely have different genetic base (Tanksley, 2004). 463 464 Ripening, or fruit maturation, is the physiological process giving rise to red, fully developed mature fruit. During ripening, important biochemical reactions occur. Some are beneﬁcial to the fruit, such as acqui478 sition of color, accumulation of sugars and volatile compounds. Others 479 are detrimental to long storage, such as loosening of the cell wall, 480 which leads to loss of fruit ﬁrmness and reduction of shelf-life. In 481 the climacteric fruit of tomato, the onset of ripening is preceded by 482 the increase of respiration and the biosynthesis of ethylene (Lelievre 483 et al., 1997). Ethylene results from the methionine metabolism 484 Q84 (Yang, 1985). The S-adenosylmethionine is converted via ACC synthase 485 (ACS) to 1-amino-cyclopropane-1-carboxylic acid (ACC), which is sub486 sequently converted to ethylene via ACC oxidase (ACO). In addition to 475 476 477 ACC, ACS produces methylthioadenosine, which is used to synthesize new methionine via a modiﬁed cycle, called Yang cycle (Fig. 4). This alternative methionine pathway ensures that high rates of ethylene can be maintained even when the pool of methionine is limited (Alexander and Grierson, 2002; Bapat et al., 2010). Ethylene can be produced by two distinct systems. The system 1 is responsible for the low production of ethylene in all tissues, is autoinhibited by ethylene and functions during normal vegetative development. The system 2, characterized as autocatalytic, is responsible for an auto-stimulated massive ethylene production, requires the induction of new ACS and ACO isoforms, and is speciﬁc of climacteric fruits and petal senescence (Bapat et al., 2010; Lin et al., 2009). The control of ripening can be done at several points: ethylene synthesis, ethylene perception, ethylene signaling pathway. Several tomato germplasms with altered ripening were identiﬁed and a non-exhaustive list can be found in Moore et al. (2002). Among them, one can cite: ripening-inhibitor (rin), never-ripe (Nr), non-ripening (nor), high-pigment 2 (hp-2) or colorless non-ripening (Cnr). The Nr mutant is an ethylene receptor mutant which results in non-ripening, ethylene insensitive fruit (Wilkinson et al., 1995). The analysis of the tomato germplasms revealed that climacteric ripening represents a combination of ethylene mediated and non-ethylene mediated regulation. Indeed the initial evidence of non-ethylene mediated regulation came from the analysis of the two mutants, rin and nor, that do not produce autocatalytic ethylene, do not ripen, and more importantly do not ripen in response to exogenous ethylene. The molecular characterization identiﬁed rin as encoding a transcription factor belonging the MADS-box family whereas nor encodes a transcription factor of Please cite this article as: Bergougnoux V, The history of tomato: From domestication to biopharming, Biotechnol Adv (2013), http://dx.doi.org/ 10.1016/j.biotechadv.2013.11.003 487 488 489 490 491 492 493 494 495 496 497 498 499 500 501 502 503 504 505 506 507 508 509 510 511 512 513 9 R O O F V. Bergougnoux / Biotechnology Advances xxx (2013) xxx–xxx Fig. 4. Ethylene biosynthetic pathway and ripening regulated processes. 1: adomet synthetase, 2: kinase, 3: aminotransferase, 4: ACC synthase (ACS), 5: ACC oxydase (ACO). O R R E C T E D P ripens slowly and has an extended shelf-life. Interestingly, the rin mutation in its form rin/Rin constitutes the basis for most of the tomato hybrids with slow ripening and long shelf-life (Giovannoni, 2007). In a recent study, Martel et al. (2011) demonstrated that RIN interacts C 517 the NAC domain family (Martel et al., 2011; Vrebalov et al., 2002). If these mutations are homozygous, the process of ripening is inhibited, the fruits remain yellow or light orange and can be stored for months at room temperature. When the mutations are heterozygous, the fruit N 515 516 U 514 Fig. 5. Carotenoids biosynthetic pathway and tomato mutants. Pictures are from the Tomato Genetic Resource Centre. ABA: abscissic acid; AO, adldehyde oxidase; CrtR-b: carotenehydroxylase; Cyc-B: chromoplast speciﬁc lycopene synthase; DMAPP: dimethylallyl diphosphate; GPP: genaryl diphosphate; GGPP: geranylgeranyl diphosphate; Ggps: GGPPsynthase; IPP: isopentenyl diphosphate; Lcy-b: lycopene β-cyclase; Lcy-e: lycopene ε-cyclase; MEP: methylerythritolphosphate; Nxs: neoxanthin synthase; Pds: phytoene desaturase; Psy: phytoene synthase; Vde1: violaxanthin deepoxidase; VNCED: 9-cis-epoxycarotenoid dioxygenase; Zds: ζ-carotene desaturase; Zep1: zeaxanthin epoxidase. Please cite this article as: Bergougnoux V, The history of tomato: From domestication to biopharming, Biotechnol Adv (2013), http://dx.doi.org/ 10.1016/j.biotechadv.2013.11.003 518 519 520 521 10 545 546 547 548 549 550 551 552 553 554 555 556 557 558 t5:1 t5:2 t5:3 Table 5 Nutritional value of 100 g of red fresh tomato (source: USDA, http://www.usda.gov/wps/ portal/usda/usdahome). t5:4 Proximates t5:5 t5:6 t5:7 t5:8 t5:9 t5:10 t5:11 t5:12 Water Energy Protein Total lipid Fibers Sugars Minerals Calcium Magnesium Phosphorus Potassium Sodium Fluoride t5:13 t5:14 t5:15 t5:16 t5:17 t5:18 t5:19 t5:20 Vitamins t5:21 t5:22 t5:23 t5:24 t5:25 t5:26 t5:27 t5:28 Vitamin C Choline Vitamin A α-Carotene β-Carotene Lycopene Lutein + zeaxanthin Vitamin K g kcal g g g g mg mg mg mg mg μg mg mg μg μg μg μg μg μg 94.52 18 0.88 0.2 1.2 2.63 10 11 24 237 5 2.3 13.7 6.7 42 449 101 2573 123 7.9 If one takes into consideration only proteins/lipids/sugars content to describe the nutritional value, it appears clearly that tomato does not have a high nutritional value. Nevertheless, tomatoes represent an important source of nutrients which are important for human health such as antioxidants, represented by the content in lycopene, vitamin A (β-carotene) and ascorbic acid (vitamin C) (Table 5). Thus, tomatoes represent the main source of lycopene, which has antioxidant properties and is considered to protect against cancer or cardiovascular diseases (Rao and Agarwal, 2000). The cross between S. lycopersicum cv. Floradade and the wild relative S. galapense (L. cheesmanii f. minor C.H. Mull), bearing the Beta (B) gene, gave rise to three lines with enhanced fruit βcarotene content, and consequently higher nutritional value (Stommel, 2001). Tomatoes are also an important and remarkable source of ascorbic acid. The primary route of ascorbic acid synthesis is the L-galactose Wheeler–Smirnoff pathway in which ascorbic acid is synthesized from mannose-6-phosphate via GDP-mannose and GDP-L-galactose. More pathways have been described notably the alternatice pathway with an L -galactonic acid intermediate, deriving from cell wall polymers (Di Matteo et al., 2010; Ioannidi et al., 2009; Stevens et al., 2007). Compared to the modern cultivated tomato, wild tomato varieties are rich in ascorbic acid and can contain up to 5 times more ascorbic acid than the cultivated counterpart (Stevens, 1986). Stevens et al. (2007) investigated the QTLs and candidate genes affecting fruit ascorbic acid. The recent work of Di Matteo et al. (2010) demonstrated that the accumulation of ascorbic acid is achieved by increasing pectin degradation and may be triggered by ethylene. Some cultivars with enhanced nutritional value were thus successfully developed, but reduction of the yield in these new cultivars hindered their commercial success (Causse et al., 2007). Soluble and total solids are important traits for processing tomatoes and contribute to the deﬁnition of the concentrated tomato product. Soluble solids represent sugars and organic acids whose ratio, together with the composition in volatile aroma, characterizes the ﬂavor of the fruit. The organic acids, alone, determine the pH of the ﬁnal product. A pH above 4.5 will allow the development of microorganisms, spoiling the ﬁnal product. Increased temperatures and extended processing time are the only ways to get rid of this problem, but they also increase the costs linked to processing. Insoluble solids, represented by components of the cell wall and proteins, deﬁne the ﬁrmness of the fruit but also the viscosity of the ﬁnal products, such as tomato juice, ketchup, soups and paste. Two other criteria are of high importance for the breeding of new cultivars for processing tomatoes: growth habit and ease of harvest. The spontaneous self-pruning (sp) mutation appeared in 1914, allowing the development of cultivars with bushy growth habit. In addition, sp induces the concentration of ﬂowers and consequently of fruits, and contributes to fruit ﬁrmness and resistance to over-ripening. All these characteristics made cultivars bearing this mutation material of choice for mechanical harvest. The “jointless” mutations (j and j2) are characterized by no abscission zone in fruit pedicel, enabling harvest without calyx and pedicel, i.e. the fruit free from any “green” parts. 564 565 O F 563 R O 543 544 2.5. Nutritional value P 541 542 559 560 D 539 540 carotenoid isomerase. The Del mutant accumulates high levels of δcarotene and encodes a lycopene β-cyclase, like the mutation B, which is characterized by the accumulation of γ-carotene (Lewinshon et al., 2005). E 537 538 T 535 536 C 533 534 E 531 532 R 529 530 R 528 O 526 527 C 524 525 with the promoter of genes involved in the major processes observed during ripening: ethylene biosynthesis, perception and signaling, cell wall metabolism, and carotenoid. Color change is the most obvious trait of tomato ripening. The color of fruit depends on its content of carotenoid pigments, mainly lycopene and to a lesser extent β-carotene. The ﬁrst step in carotenoid synthesis is the condensation of two molecules of GGPP (geranylgeranyl diphosphate, synthesized from isopentenyl diphosphate/IPP and dimethylallyl diphosphate/DMAPP) to produce phytoene by phytoene synthase (PSY). Phytoene is converted into lycopene via the production of the intermediate ζ-carotene; this reaction involves two enzymes: phytoene desaturase (PDS) and ζ-carotene desaturase (ZDS). The cyclization of lycopene is an important branching point in the pathway as it can give rise to β-carotene and xanthophylls on one side, or to δ-carotene/αcarotene and lutein on the other side. β-carotene is synthesized by a two-step reaction mediated by lycopene β-cyclase (LCY-B/CRTL-B) with the production of γ-carotene as intermediate. Lycopene ε-cyclase (LCY-E/CRTL-E) allows the synthesis of δ-carotene from lycopene. The production of other compounds results from hydroxylation of the cyclic carotenes by two carotenoid hydroxylases (CHYs), one speciﬁc for βrings (BCH type) and the other one catalyzing hydroxylation of both β- and ε-rings (CYP97 type) (Ruiz-Sola and Rodríguez-Concepción, 2012). The next steps are epoxydation by means of ZEP1 (Fig. 5; Hirschberg, 2001). In tomato, several mutants affected in color are available: r (yellow ﬂesh, yellow color of the ripe fruit ﬂesh), sh (sherry, yellow fruit fresh with reddish tinge), hp-1 (high pigment1, higher content in chlorophyll, carotenoids and ascorbic acid), tg (tangerine, fruit ﬂesh and stamens are orange colored), B (beta-carotene, high β-carotene and lycopene content in ripe fruit), at (apricot, yellow-pinkish color of the fruit ﬂesh), og (old gold, increased lycopene content), DEL (delta, reddish-orange mature fruit color). These mutants contributed to the elucidation of the carotenoid synthesis pathway (Causse et al., 2007) and their molecular characterization contributed to the identiﬁcation of the genes responsible for the mutations/phenotypes. The mutant r encodes the phytoene synthase, PSY1, the ﬁrst speciﬁc step of the carotenoid biosynthesis pathway (Hirschberg, 2001). The orange color of the mutant tg is due to the accumulation of prolycopene and encodes a U N 522 523 V. Bergougnoux / Biotechnology Advances xxx (2013) xxx–xxx Q85 561 562 566 567 568 569 570 571 572 573 574 575 576 577 578 579 580 581 582 583 584 585 586 587 Q86 588 589 590 591 Q87 592 593 594 595 596 597 598 599 600 601 602 603 604 605 606 607 608 609 610 611 612 613 614 2.6. Limits of classical breeding: the new area of genetic engineering 615 In order to obtain new cultivars with improved agronomical traits, three objectives have to be taken into account: environmental conditions, mode of culture and mode of harvest. Efﬁcient breeding relies on the availability of genetic diversity and the heritability of the traits of interest. Very often, many traits must be simultaneously improved 616 617 Please cite this article as: Bergougnoux V, The history of tomato: From domestication to biopharming, Biotechnol Adv (2013), http://dx.doi.org/ 10.1016/j.biotechadv.2013.11.003 618 619 620 11 V. Bergougnoux / Biotechnology Advances xxx (2013) xxx–xxx 646 647 648 649 650 651 652 653 654 655 656 657 658 659 660 661 662 663 664 665 666 667 668 669 670 671 672 673 674 675 676 677 678 679 680 681 682 683 684 685 686 L. pimpinellifolium, L. hirsutum, L. pennellii, L. peruvianum L. cheesmaniae, L. esculentum, L. pimpinellifolium, L. chilense, L. hirsutum, L. pennellii, L. parviﬂorum, L. peruvianum L. esculentum, L. pimpinellifolium, L. chilense, L. hirsutum, L. peruvianum L. pimpinellifolium, L. peruvianum Abiotic stress Cold (low temperature) L. pimpinellifolium, L. hirsutum Drought L. pimpinellifolium, L. pennellii Salt L. pimpinellifolium, L. pennellii R O O F 644 645 Resistance to insects Fruit characteristics Antioxidant capacity Ascorbic acid Citric acid Color Jointless L. pennellii L. pennellii L. pennelli L. pimpinellifolium, L. peruvianum, L. hirsutum, L. parviﬂorum, L. chmielewski, L. pennellii L. cheesmanii, L. hirsutum, L. pennellii, L. parviﬂorum L. pimpinellifolium, L. parviﬂorum, L. pennellii L. pennellii L. parviﬂorum L. pennellii, L. pimpinellifolium L. pimpinellifolium L. pimpinellifolium, L. peruvianum, L. hirsutum, L. parviﬂorum, L. pennellii L. pimpinellifolium, L. peruvianum, L. hirsutum, L. parviﬂorum, L. chmielewskii, L. pennellii L. pennellii, L. hirsutum L. pimpinellifolium L. pimpinellifolium L. pimpinellifolium, L. peruvianum, L. hirsutum, L. parviﬂorum L. pennellii, L. pimpinellifolium, L. peruvianum, L. cheesmanii L. chmielewskii, L. cheesmanii, L. pennelli, L. pimpinellifolium, L. hirsutum L. pimpinellifolium, L. peruvianum, L. hirsutum, L. parviﬂorum, L. pennellii L. pennellii, L. chmielewskii, L. cheesmanii, L. pimpinellifolium, L. peruvianum, L. hirsutum L. chmielewskii, L. pennelli, L. pimpinellifolium, L. peruvianum, L. hirsutum, L. parviﬂorum L. cheesmanii Plant characteristics Branch number Male sterility Growth habit Height Self-pruning L. cheesmanii L. pimpinellifolium L. peruvianum, L. pimpinellifolium L. pennelli, L. pimpinellifolium, L. hirsutum, L. cheesmanii L. chmielewskii, L. pimpinellifolium β-carotene Lycopene Orange Yellow Cracking Diameter Shape P 642 643 Resistance to virus Firmness D 640 641 Germplasm source (Lycopersicum name) Biotic stress Resistance to bacteria Resistance to fungi Sugars Length Locule number Maturity Ripening Soluble solids E 638 639 Phenotype T 636 637 C 634 635 E 632 633 R 630 631 R 628 629 O 627 Table 6 t6:1 Non-exhaustive list of agronomic traits of interest available from wild tomato species t6:2 (extracted from Foolad, 2007, for more details see the references therein). t6:3 Viscosity Weight Yield t6:4 t6:5 t6:6 t6:7 t6:8 t6:9 t6:10 t6:11 t6:12 t6:13 t6:14 t6:15 t6:16 t6:17 t6:18 t6:19 t6:20 t6:21 t6:22 t6:23 t6:24 t6:25 t6:26 t6:27 t6:28 t6:29 t6:30 t6:31 t6:32 t6:33 t6:34 t6:35 t6:36 t6:37 t6:38 t6:39 t6:40 t6:41 t6:42 t6:43 t6:44 t6:45 C 625 626 N 623 624 and introduced into the new cultivar and most of them are controlled by several genes and/or inﬂuenced by the environment. Finally, and importantly, the organoleptic signature, considered often as a “side” criterion for selection, is evaluated by sensorial analyses which cannot be developed on the scale of mass screening (Causse et al., 2007). Traditional breeding usually starts from a cross between elite lines of adapted cultivars, or between an elite line and either wild species or close outgroup related species (S. juglandifolium and S. ochranthum). It must be noted that the production of a new cultivar from a cross between two cultivars takes 5 to 7 years, and the incorporation of new genes from wild relatives takes about 20 years, the complexity of the breeding program increasing with the complexity between parents (Causse et al., 2007). The choice of parental lines is thus crucial and demands good knowledge of the available germplasm. In the case of tomato, more than 83,000 accessions are stored in seed banks throughout the world, placing tomato as the number one collected and conserved vegetable species (Bauchet and Causse, 2012). The main collections are: the Tomato Genetic Resource Center in California (USA — TGRC, http://tgrc. ucdavis.edu/), the USDA collection (USA — www.ars.usda.gov), the World Vegetable Center in Taiwan (www.avrdc.org) and other collections in Europe. In the frame of the European Solanaceae project (EU-SOL, www.eu-sol.wur.nl), approximately 7000 domesticated tomato accessions, alongside representative wild species, were enumerated. These collections represent a precious source of information for subsequent breeding programs. All wild species can be crossed with the cultivated tomato (S. lycopersicum) with more or less high efﬁciency if cultivated tomato is used as the female (Bedinger et al., 2011). When two species are non-crossable, in vitro techniques are required, such as cell fusion and regeneration from tissue or single cells, or embryo-rescue (Bai and Lindhout, 2007; Rick, 1974); this is particularly necessary in the case of crosses with S. peruvianum. Table 6 gives a nonexhaustive list of traits which have a potential for breeding and their germplasm origin. A few examples of the improvement of cultivated tomato by introgression of “wild” characters can be mentioned here: the use of L. hirsutum for improving cold tolerance, of L. chilense for drought tolerance, of L. cheesmanii for soluble solids and salt tolerance (Hobson and Grierson, 1993), or of L. pennellii for sugar yield (Fridman et al., 2000; Ikeda et al., 2013) or yield and ﬁtness (Semel et al., 2006). Recently, in an attempt to increase the endogenous content of ﬂavonoids, compounds with a positive impact on human health, S. pennellii var. puberulum was crossed with cultivated tomato (Willits et al., 2005). The plants accumulated high levels of quercetin in the fruit. Some accessions accumulated lycopene or ascorbic acid at levels twice those of traditional cultivars. Thus carotene content can be signiﬁcantly increased in cultivated tomato by using S. hirsutum in crosses. Analogously, a strategy based on S. pimpinellifolium, S. cheesmanii and S. chmielewskii has increased the sugar content (Stevens, 1986). The method of Gas chromatography–mass spectrometry was used to characterize the metabolic proﬁle of leaves and fruits of wild tomato species in comparison to cultivated tomato. The method allowed identifying more than 90 metabolites constituting the metabolic signature of each species. This is of importance as it can constitute a way of selecting parental lines used in crosses (Schauer et al., 2005). By 2050, the world population is estimated to reach 9.07 billion, with 62% of people living in Africa, Southern Eastern Asia. These same regions are where a huge proportion of the population suffers from hunger (FAO, data collected for the period 2010–2012). Traditional agriculture and breeding cannot sustain the increasing food demand for several reasons: 1) decreasing arable land giving way to living space, 2) increasing problem of drought and salt stresses due to environmental and climate changes, and 3) slow and laborious “empirical” selection (Ahmad et al., 2012). The development of molecular biology offers breeders a new prospect for genetic improvement based on molecular markers and genetic engineering. Molecular markers used in markerassisted selection (MAS) are not reviewed in this work as they have been extensively reported in various recent reviews (Bauchet and U 621 622 Causse, 2012; Causse et al., 2007). Attempts to understand the plant genome, i.e. how the plant functions and how a gene can make a plant, led in 2003 to the development of the international “Solanaceae Genomics Network” (SOL) project. This consortium encompasses several databases resulting from gene sequencing, gene expression proﬁling, metabolites proﬁling, genome sequencing and annotation. The fullysequenced tomato genome was released in 2012, and its annotation is still underway (The Tomato Genome Consortium, 2012). All this information allows a better understanding of the plant growth and development; today a speciﬁc character can be easily introduced in a cultivar of interest by means of plant transformation and regeneration in a shorter time than traditional breeding. Moreover, genetic engineering surmounts the barriers intra-/inter-crossability. Indeed, a gene from a non-related species can be introduced into the crop of interest which would not have been possible by classical breeding, due to interspeciﬁc incompatibility. Please cite this article as: Bergougnoux V, The history of tomato: From domestication to biopharming, Biotechnol Adv (2013), http://dx.doi.org/ 10.1016/j.biotechadv.2013.11.003 687 688 689 690 691 692 693 694 695 696 697 698 699 700 701 702 12 V. Bergougnoux / Biotechnology Advances xxx (2013) xxx–xxx 717 Genetic engineering, i.e. the introduction of a gene or its silencing, provides the tools for fast and speciﬁc improvement of tomato agronomical traits. Except for the report on chloroplast transformation using particle bombardment (Ruf et al., 2001), the most widely used method for transferring genes into tomato is Agrobacterium-mediated transformation. The FLAVR-SAVR™ tomato variety was the ﬁrst genetically engineered crop to be commercialized (Kramer and Redenbaugh, 1994). Despite the fact that this new tomato also contained a bacterial gene encoding resistance for kanamycin (used for selection), the new cultivar was introduced on the fresh tomato market on May 21, 1994. The FLAVR-SAVR™ tomato found an important albeit brief success, due to the costs linked to engineering and the newly growing negative consumer concerns about GMO (genetically modiﬁed organisms; Bruening and Lyons, 2000). 718 3.1. Agrobacterium-mediated transformation of tomato 706 707 708 709 710 711 712 713 714 715 716 719 F 704 705 simpler. In order to study the regulation of ﬂower initiation and development in tomato, Yasmeen et al. (2009) initiated the ﬂoral dip transformation of tomato. They observed that ﬂowers which did not experience pollination gave a higher percentage of transformation, similar to what was observed for Arabidopsis. It is supposed that after anthesis the locule becomes sealed, enabling the proper penetration of the bacteria to the ovule (Desfeux et al., 2000). Inﬁltration of tissues for transient gene expression and localization was developed for several species. The Agrobacterium-mediated transient expression by leaf inﬁltration is today the favorite tool in many gene functional analyses. While tobacco leaf is the material of choice, the efﬁciency of the method has been described not only for other species, such as alfafa, lettuce, tomato, and Arabidopsis (Wroblewski et al., 2005), but also for rose petals (Scalliet et al., 2006). In order to shorten the time in functional studies in fruit development, Agrobacterium-mediated transformation by inﬁltration of tissues was applied to tomato fruit (Orzaez et al., 2006). In practice, the Agrobacterium cultures were injected into the mature green fruits through the fruit stylar apex, which resulted in complete fruit inﬁltration. This new method, called “fruit agroinjection”, was found to be a powerful tool for fast transgene expression in fruits and to facilitate functional studies in that organ. A few years later, Hasan et al. (2008) reported fruit agroinjection as a tool to stably transform tomato. The efﬁciency of transformation was higher when the fruit was kept on the plant compared to detached fruit, and mature fruits at the early stage of ripening gave more transformants than immature, green fruits (Yasmeen et al., 2009). O 3. Genetic engineering of tomato R O 703 For 30 years now, Agrobacterium has been used for research pur- 720 poses, and it has also been used to produce genetically engineered 721 Q88 crops for commercial purposes. The Gram negative soil bacterium Agrobacterium tumefaciens is a phytopathogen responsible for crown gall disease in a wide range of plants (Alimohammadi and Bagherieh724 Najjar, 2009). The molecular basis of plant cell reprogramming by the 725 bacterium and the principles of Agrobacterium-mediated transforma726 tion have been already extensively reviewed (Binns and Thomashaw, 727 1988; Shantha et al., 2012). The traditional protocol for Agrobacterium728 mediated transformation is based on the co-culture of explant, with a 729 bacterial culture containing the cloning vector and the property of a 730 plant cell to regenerate a full plantlet. Frary and Van Eck (2005) describe Q89 a standard protocol, based on the initial work of McCormick et al. 731 732 (1986a, 1986b) and Fillatti et al. (1987). In brief, after an overnight 733 preculture step, the cotyledon explants are cocultivated with 734 Agrobacterium for two days. Afterward the explants are transferred 735 to a selective regeneration medium containing zeatin. The rooting 736 is ensured on a separate selective medium. 737 The ﬁrst tomato transformation by Agrobacterium was done in 1986 738 (McCormick et al., 1986) in order to avoid the need to develop a system 739 of plant regeneration from protoplasts. The leaf disk system was 740 adapted for tomato transformation. This ﬁrst Agrobacterium-mediated 741 transformation of tomato opened the door to the functional characteri742 zation of tomato genes and/or promoters as well as the expression of 743 heterologous genes. The explants used were as diverse as cotyledons, 744 hypocotyls, stems and leaves of the tomato (Bird et al., 1988; Davis 745 and Miller, 1991; McCormick et al., 1986; Ohki et al., 1978). The differ746 ent conditions relative to efﬁcient transformation have been studied 747 and reported (Park et al., 2003). 748 The generation of transgenic plants is routinely developed in most 749 plant molecular biology research laboratories; nevertheless the classical 750 method of shoot regeneration from leaf disk/cotyledons tissues co751 cultivated with disarmed Agrobacterium is a long and expensive process 752 which can result in undesirable modiﬁcations, such as somaclonal varia753 tion, i.e. modiﬁcation of the genotype independent from the character in754 troduced. In order to avoid the use of tissue culture, methods called “in 755 planta” transformation were developed (Yasmeen et al., 2009). The ﬁrst 756 “in planta” method developed was the Agrobacterium-mediated ﬂoral 757 dip transformation in Arabidopsis. For this purpose, the plant was grown 758 until ﬂowering, uprooted, fully immersed in a solution of Agrobacterium 759 with application of vacuum in order to facilitate the penetration of bacte760 ria into the plant tissue, and then planted back into soil. The plants were 761 then cultivated until the production of seeds. The transgenic progenies 762 were identiﬁed by cultivation of the seeds on a medium supplemented 763 with the appropriate selective agent (Bechtold et al., 1993). In an 764 upgraded version of this protocol, Clough and Bent (1998) suppressed 765 the phase of uprooting/vacuum/replanting, making this method even P 722 723 D 3.2. Selection of transgenic plants E T C E R R O C U N Because during the process of Agrobacterium-mediated transformation not all cells of the explant are efﬁciently transformed, the use of selection is required to avoid long, costly and laborious screening of the transgenic progeny. Thus a gene encoding an enzyme conferring resistance to antibiotics or herbicides is introduced concurrently with the gene of interest. The presence of such genes within the environment or in the food supply might provoke unpredictable damage to the ecosystem and to human health. The possibility of transmission of the marker gene through pollen is the major environmental concern (Tuteja et al., 2012). In the last decade, methodologies have been developed to eliminate marker genes from the process of genetic engineering. Several possibilities were considered. The ﬁrst one consisted of avoiding the use of the marker gene in transgenic plants. This was applied in several crops, but the efﬁciency of transformation rarely reached 5% (Bai et al., 2009; De Vetten et al., 2003; Jia et al., 2006). A second method is co-transformation, which is a simple and highly effective method. In this case, the gene of interest and the marker gene are present on two different vectors. The ﬁrst generation of the progeny will bear the two genes in its genome. Because they are not introduced in the genome at the same loci, they will segregate during sexual reproduction. The marker gene will be eliminated from the genome by further selecting transgenic lines bearing only the gene of interest (Komari et al, 1996). Transposon-based marker excision is a third strategy which has also been used to remove marker genes from the gene of interest. This strategy is based on the maize Ac/Ds transposable element (Upadhyaya et al., 2010). Finally, marker gene removal can be achieved by a strategy based on the recombination which takes place between two homologous DNA molecules. Three systems were developed based on recombination to eliminate the marker gene: the Cre/lox site speciﬁc recombination system (Dale and Ow, 1991), the FLP/FRT recombination system from Saccharomyces cerevisiae (Lyznik et al., 1996) and the R/RS recombination system from Zygosaccharomyces rouxii (Sugita et al., 2000). Because all these strategies have been described and reported in detail by several reviewers, they are not explained here (Darbani et al., 2007; Puchta, 2003; Upadhyaya et al., 2010). In tomato, the ﬁrst report of generation of marker-free transgenic plants came from Goldsbrough et al. (1993). By using the maize Ac/Ds transposable element, they were able to obtain NPTII- or GUS-free Please cite this article as: Bergougnoux V, The history of tomato: From domestication to biopharming, Biotechnol Adv (2013), http://dx.doi.org/ 10.1016/j.biotechadv.2013.11.003 766 767 768 769 770 771 772 773 774 775 776 777 778 779 780 781 782 783 784 785 786 787 788 789 790 791 792 793 794 795 796 797 798 799 800 801 802 803 804 805 806 807 808 809 810 811 812 813 814 815 816 817 818 819 820 821 822 823 824 825 826 827 828 Q90 829 V. Bergougnoux / Biotechnology Advances xxx (2013) xxx–xxx 856 857 858 859 860 861 862 863 864 865 866 867 868 869 870 871 872 873 874 875 876 877 878 879 880 881 882 883 884 885 886 887 888 889 890 891 892 893 C 854 855 E 852 853 R 850 851 R 848 849 O 846 847 C 844 845 N 842 843 U 840 841 894 895 896 897 898 899 900 901 902 903 904 905 4. Transgenic tomatoes with enhanced agronomic traits 906 The development and spread of genetically engineered crops encounters negative opinions of consumers and institutions, mainly in Europe. Thus, the World Health Organization (WHO) has reported three main concerns to the use of genetically engineered crops: generation of allergenic foods, incorporation of modiﬁed food genes into the human body and the transfer of this information to other wild species. Despite these barriers, the development of transgenic crops is expanding all over the world; indeed the surface dedicated to the cultivation of genetically engineered crops has greatly expanded, with 125 million ha in 2008 vs. 1.7 million ha 12 years ago (Ahmad et al., 2012). The leading countries are without contest the USA with 69.5 million ha dedicated to genetically engineered crops (maize, soybeans, cotton, canola, sugarbeets, alfalfa, papayas and squash), followed by Brazil, Argentina, India and Canada (10–40 million ha). Today, China is probably the only country growing transgenic tomatoes (source: www.isaaa.org, 2012). Indeed, culture of transgenic tomatoes in the USA, which represented 200,000 ha in 1998, has been suspended since 2002. The objectives of tomato improvement by genetic engineering focus on: fruit quality, resistance to pests and diseases, overcoming adverse environments (cold, drought, salinity) and production of therapeutics. In the scientiﬁc literature since 2000, more than 60 records report on genetic engineering of tomato. Because it is not possible to describe all of them in the present review, Table 7 gives a non-exhaustive list of successful genetic engineering of tomato; some of them are discussed in more detail below. 907 929 930 4.1. Resistance to biotic stresses 931 Economic losses due to pests and diseases are signiﬁcant all around the world. Up to now, pesticides are widely used to control the development of pests and diseases, but several problems have appeared due to this cultural practice: development of resistance to the chemicals, appearance of new diseases, health disorders of farmers, and detrimental effects on the environment. Genetic engineering offers a great opportunity to limit the use of such chemicals. To respond to pathogen attack, plants have evolved a variety of active and passive defense mechanisms: hypersensitive programmed cell death, expression of defense-related genes, reinforcement of cell walls, biosynthesis of phytoallexins or phenolic compounds, production of reactive oxygen species (ROS), and initiation of systemic acquired resistance (Li and Steffens, 2002). These responses are induced upon attack by bacteria, fungi, virus or insects. Moreover, three hormones, salicylic acid (SA), ad jasmonic acid (JA) and ethylene, were described to play key roles in the establishment of susceptibility/resistance. It is commonly accepted that SA and JA/ethylene have an antagonistic role, with SA being involved in resistance to biotrophic pathogens and JA/ethylene being involved in resistance to necrotrophic pathogens (Kunkel and Brooks, 2002). Studies of the molecular basis of resistance have allowed researchers to identify genes whose manipulation by overexpression could lead to improved resistance to pathogens. On the other hand, the analysis of plants with a high susceptibility to pathogens has led to the 932 933 R O O F The Cauliﬂower mosaic virus 35S (CaMV35S) promoter was, and still is, routinely used to trigger gene expression in both dicots and monocots. Despite the fact that it is assumed to be a constitutive promoter (Odell et al., 1985), some studies report that it is not expressed in all cell and tissue types (reviewed in Sunilkumar et al., 2002). A study using GFP fusion as the reporter of promoter activity in cotton demonstrated that genes driven by CaMV35S promoter are expressed in all cells and tissues albeit at different levels (Sunilkumar et al., 2002). The discrepancy between the study of Sunilkumar et al. (2002) and older studies is probably due to the GFP reporter assay used which is more sensitive than classical histological methods using GUS staining. Due to its viral origin, there are some limitations in its use for genetic engineering of crops. First, despite the lack of scientiﬁc support, some fear its risk to human health; second, the plant can recognize the sequence of foreign origin and inactivate it (Potenza et al., 2004). Thus other promoters, of plant origin, were developed to drive constitutive expression. These promoters are derived from actin and ubiquitin genes and induce strong expression of the gene of interest. One can cite here the promoter of the Arabidopsis Act2 gene, rice actin 1, maize ubiquitin 1 or Ubi.U4 from Nicotiana sylvestris (reviewed in Potenza et al., 2004). Constitutive expression can be problematic. Indeed, the gene of interest will be expressed in all tissues, independently from growth and development, leading to often undesirable pleiotropic effects which do not reﬂect the in planta function of the gene. Thus, new promoters driving the expression of the gene of interest in a speciﬁc manner were developed. Fruit and ﬂowers are the main targets for genetic engineering of fruit crops but they are the last to develop, rending their manipulation difﬁcult. Several “toolkits” have been obtained in order to speciﬁcally address gene expression in fruit (Fernandez et al., 2009). Ethylene is part of the process leading to fruit ripening. The E8 gene of tomato encodes a polypeptide belonging to the family of dioxigenases and participates in the regulation of ethylene production during ripening. The promoter analysis of E8 led to the identiﬁcation of different regions responsible for both fruit-speciﬁc expression and ethylene-regulated expression (Deikman et al., 1992). This promoter has been successfully used in tomato genetic engineering (Sun et al., 2012). Another promoter used to speciﬁcally drive the expression of a gene of interest in the fruit during ripening is the promoter of the polygalacturonase (PG) gene, encoding the major cell-wall degrading enzyme (Lau et al., 2009). When considering genetic engineering for stress tolerance, it is important to develop tools which will respond to a speciﬁc stimulus. Indeed, the mechanisms of resistance represent a certain energetic cost for the plant that remobilizes its metabolism to face the stress. Modern genetic engineering has a duty to develop plants whose mechanisms of resistance will be stimulated only if and when the plant will be exposed to stress. By studying the molecular basis of plant stress responses, researchers have been able to identify genes speciﬁcally regulated by stress and use their promoters as tools for bioengineering. As it will be detailed later, plants respond to stress by producing and accumulating molecules of low molecular weight, such as glycinebetaine. In higher plants, glycinebetaine is synthesized in the chloroplast from betaine in a two-step reaction. The ﬁrst reaction is catalyzed by a ferredoxindependent choline mono-oxygenase (CMO) and produces betaine aldehyde as an intermediate. Betaine aldehyde is further transformed into betaine by the NAD+-dependent betaine aldehyde dehydrogenase (BADH) (Su et al., 2006). BADH gene expression is stimulated by several P 838 839 D 3.3. Temporal and/or organ-speciﬁc expression: choice of promoter 834 835 E 837 832 833 stresses, such as salt, drought, cold and ABA treatment. Analysis of the promoter sequence of BADH led to the identiﬁcation of a region (P5: − 300 to + 62 bp) which triggers salt-induced gene expression. In order to validate that the P5 region of the BADH gene could be used as a new promoter to drive gene expression speciﬁcally in response to saline stress, Wang et al. (2013) transformed tomato plants with the BADH gene, as reporter gene, under the control of the P5 promoter to drive salt-inducible expression. The authors could observe that BADH expression and accumulation of betaine was correlated with the concentration of salt applied. Consequently, the salt-inducible P5 promoter appears to be an essential tool for further genetic engineering in regard to salt stress tolerance. T 836 plants from transgenic plants which originally contained one of these genes in their genome. To our knowledge, Zhang and coworkers obtained the ﬁrst genetically engineered marker-free tomato with improved tolerance to drought, cold and oxidative stresses. These authors obtained transgenic tomatoes by overexpression of the Arabidopsis Ipk2 gene, in which the marker of selection was removed by the Cre/loxP DNA recombination system (Zhang et al., 2009). 830 831 13 Please cite this article as: Bergougnoux V, The history of tomato: From domestication to biopharming, Biotechnol Adv (2013), http://dx.doi.org/ 10.1016/j.biotechadv.2013.11.003 908 909 910 911 912 913 914 915 916 917 918 919 920 921 922 923 924 925 926 927 928 934 935 936 937 938 939 940 941 942 943 944 945 946 947 948 949 950 951 952 953 954 14 Size Flavor fw2.2 Thaumatin, gdhA, GES, LIS, LeCCD1, LeACCDC1A, LeACCDC2 Soluble solids content Carotenoid content Lin5, PME Dxs, CrtB, CrtI, CrtY, PSY-1, CRY-2, CYC-B, LCY-B, LCY-B, CHY-B, DET-1, COP1LIKE, CUL4, FIBRILLIN, Spermidine synthase, PG Flavonoid content CHI, CHS, CHI, F3H, FLS, MYB12, STS, CHR, FNS-II, Del, Ros1 Ascorbic acid content GaLDH, GME, GCHA and/or ADCS Ficcadenti et al. (1999), Goetz et al. (2007), Wang et al. (2005) Behboodian et al. (2012), Brummell et al. (1999), Langley et al. (1994), Lu et al. (2001); Pinhero et al. (2003), Smith et al. (1990), Tieman and Handa (1994), Watson et al. (1994), Xiong et al. (2005) Frary et al. (2000) Bartoszewski et al., 2003; Davidovich-Rikanati et al. (2007), Kisaka and Kida (2003), Lewinsohn et al. (2001); Simkin et al. (2004), Tieman et al. (2006) Tieman et al. (1992), Zanor et al. (2009) Davuluri et al. (2005), Dharmapuri et al. (2002), Enﬁssi et al. (2005), Fraser et al. (2002), Fray et al. (1995), Giliberto et al. (2005), Liu et al. (2004), Neily et al. (2011), Römer et al. (2000), Ronen et al. (2000), Rosati et al. (2000), Smikin et al. (2007), Wang et al. (2008), Watson et al. (1994), Wurbs et al. (2007) Adato et al. (2009), Butelli et al. (2008), Colliver et al. (2002), Muir et al. (2001), Schijlen et al. (2006) de la Garza et al. (2004, 2007), Garcia et al. (2009), Gilbert et al. (2011), Zhang et al. (2011) Mehta et al. (2002), Romer et al. (2000) Álvarez-Viveros et al. (2013), Artillaga et al. (1998), Cheng et al., 2009, Cortina et al. (2005), Fillatti et al. (1987), Ghanem et al. (2011), Gisbert et al. (2000), Grichko and Glick (2001), Hsieh et al. (2002a,b), Jia et al. (2002), Moghaieb et al. (2011), Park et al. (2005), Patade et al. (2013), Rus et al. (2001); Wang et al. 2005, Wang et al. (2006), Zhang and Blumwald (2001) Abdeen et al. (2005), Alberto et al. (2005), Coego et al. (2005), Kumar and Kumar (2004), Li and Steffens (2002), Lin et al. (2004), Lincoln et al. (2002), Ma et al. (2011), Mandaokar et al. (2000), Nervo et al. (2003), Raj et al. (2005), Thomzik et al. (1997), Lincoln et al. (2002) Chen et al. (2009), Hirai et al. (2010), Pogrebnyak et al. (2005), Shchelkunov et al. (2004), Tyagi et al. (2002), Youm et al. (2008) Crt1, Samdc aroA, HAL2, HAL1, BADH, AtNHX1, ectoine, GlyI and GlyII, ACC deaminase, TPS1, APX, Osmotin, CBF1, SAMDC, cAXP Biotic stresses Vst1 and Vst2, Cry1Ac, Cry1Ab, Ep5c, Nucleoprotein gene, CP, p35, PI-II and PCI, Ep5C, PPO Pharmaceutics and other compounds TB1-HBS, CtrB, Spike, miraculin R O Nutritional value Abiotic stresses O F Reference Arf8, IAA9, iaaM PG (antisense), Rab11GTPase, TBG4, PME, ACCO, EXP1A, PLD (antisense), β-galactosidase C T t7:14 Q50 Q51 Q53 Q52 6Q56-Q54 Q55 Q54 Q57 t7:15 Q58 Q60 Q59 Inserted target Parthenocarpy Firmness P Q41 Q42t7:12 Q43 t7:13 Q44 Q45 Q46 Q47 Q49 Q48 Trait Fruit quality D t7:3 t7:4Q3 Q5 Q4 Q6 t7:5 Q9 Q8 Q7 Q11 Q10 Q12 Q13 t7:6 Q14 Q15 t7:7 Q17 Q16 Q19 Q18 Q21t7:8 Q20 t7:9 Q22 Q23 6Q26-Q24 Q25 Q24 Q28 Q27 9Q31-Q29 Q32 Q33t7:10 Q35 Q34 Q35-Q33 6Q37-Q36 Q38t7:11 Q40 Q39 Q40-Q38 Table 7 Non-exhaustive list of successful tomato engineering. References can be found in Rajan et al. (2007) and Di Matteo et al. (2011). References in bold are discussed in the text. E t7:1 Q2 t7:2 V. Bergougnoux / Biotechnology Advances xxx (2013) xxx–xxx identiﬁcation of genes which are involved in this process, and potential targets of genetic engineering by gene silencing. One of the most rapid responses is the production of superoxide (O2) 958 and hydrogen peroxide (H2O2), characterizing the oxidative burst 959 shortly after pathogen recognition. Because H2O2 is highly toxic for 960 the cell, plants have developed mechanisms of detoxiﬁcation mediated 961 by peroxidases. The Ep5c gene, encoding a secreted peroxidase, was 962 found to accumulate to signiﬁcant levels in tomato plants susceptible Q91 to Pseudomonas syringae pv. tomato, leading to the hypothesis that it is 963 964 required for disease susceptibility toward this pathogen. Whereas the 965 inhibition of Ep5C protein accumulation by RNA antisense strategy led 966 to obtaining transgenic plants resistant to P. syringae pv. tomato, the 967 mechanisms downstream of Ep5C are still unclear (Coego et al., 2005). 968 The production of quinones which results from the oxidation of phenols 969 by the action of polyphenol oxidases (PPO) is also part of the processes 970 leading to pathogens resistance. Indeed, the active quinones have a di971 rect antibiotic and cytotoxic effect on pathogens. Transgenic tomato 972 plants constitutively overexpressing the potato PPO gene were charac973 terized by increased PPO activity, leading to a higher rate of phenolic 974 compound oxidation. These plants were found to be more resistant to 975 P. syringae pv. tomato. Indeed in these transgenic plants, bacterial 976 growth was strongly inhibited (100-fold reduction of bacterial popula977 tion in infected leaves compared to the non-transgenic plants) and the 978 number of lesions was also signiﬁcantly reduced (Li and Steffens, 2002). 979 The mitochondrial alternative oxidases (AOXs) are components of 980 the alternative respiratory pathway of plants. They can be induced by 981 wounding, ethylene, ROS or salicylic acid. The LeAOX gene, encoding a 982 tomato AOX, was isolated and overexpressed by Agrobacterium983 mediated transformation in tomato. Multiplication of Tomato spotted 984 wilt virus (TSWV) was signiﬁcantly limited in the transgenic tomato E 955 U N C O R R 956 957 compared to what was observed in non-transformed plants (Ma et al., 2011). In an incompatible plant-pathogen interaction, the attack by a pathogen not only induces the resistance mechanism at the point of infection, but also induces a systemic acquired resistance (SAR) response in the tissues which are not infected. The NPR1 gene, encoding a nuclear protein, is a key regulator of the SA and JA/(ethylene) signals leading to acquired resistance. One step in genetic engineering for disease resistance would be to stimulate SAR. The Arabidopsis NPR1 gene was introduced into a tomato cultivar possessing resistance to heat-stress and to tomato mosaic virus (TMV). Characterization of the resulting transgenic tomato plants revealed that in addition to the innate resistance to TMV, they were resistant to two diseases conferred by fungi (fusarium wilt and gray leaf spot) and to two bacterial diseases (bacterial wilt and bacterial spot) (Lin et al., 2004). The last example presented in the frame of this review is focused on resistance to insects. In response to insect attack, plants accumulate an array of defense proteins, including proteinase inhibitors and secondary metabolites with harmful activity to the insects. Plant proteinase inhibitors accumulate in plants in response to insect wounding and are part of the JA-mediated resistance response. The plant proteinase inhibitors inhibit the activity of insect proteases which are secreted in the digestive tract of larvae in order to assimilate amino acids. The type of proteases is speciﬁc to the type of insect. Thus, whereas serine proteinases are mainly represented in lepidopteran larvae, cysteine and aspartic proteinases are speciﬁcally found in coleopteran species. Thanks to this speciﬁcity, engineering programs can be initiated to focus on different groups of tomato pests. In tomato, the leaf-speciﬁc expression of two potato protease inhibitors, belonging to different classes (serineproteinase inhibitor and carboxypeptidase inhibitor), conferred Please cite this article as: Bergougnoux V, The history of tomato: From domestication to biopharming, Biotechnol Adv (2013), http://dx.doi.org/ 10.1016/j.biotechadv.2013.11.003 985 986 987 988 989 990 991 992 993 994 995 996 997 998 999 1000 1001 1002 1003 1004 1005 1006 1007 1008 1009 1010 1011 1012 1013 1014 V. Bergougnoux / Biotechnology Advances xxx (2013) xxx–xxx signiﬁcantly stronger resistance to damages caused by Heliothis obsoleta and Liriomyza trifolii larvae (Abdeen et al., 2005). In any genetic engi1017 neering strategy, it is recommended that genes involved in different 1018 mechanisms of resistance are used to avoid the risk of pathogen1019 acquired resistance. 1039 1040 1041 Q93 1042 1043 1044 1045 1046 1047 1048 1049 1050 1051 1052 1053 1054 1055 1056 1057 1058 1059 1060 1061 1062 1063 1064 1065 1066 1067 1068 1069 1070 1071 1072 1073 1074 1075 1076 1077 1078 C 1037 1038 E 1035 1036 R 1033 1034 R 1031 1032 O 1029 Q92 1030 C 1027 1028 N 1025 1026 U 1023 1024 P Drought, salt, cold and heat stresses share common molecular mechanisms: detoxiﬁcation of ROS, osmoprotection, protection of enzymatic systems, and water and ion ﬂuxes (Zhu, 2002). In northern countries, tomatoes are grown in greenhouse conditions where temperature has to be controlled, increasing the expense of culture. The development of cultivars more tolerant to cold temperature or chilling is an opportunity to decrease this expense. The study of species from temperate regions, more tolerant to cold, led to the identiﬁcation of several genes regulated by cold and grouped under the name of COR genes (Tomashov, 1998). All the COR genes have two speciﬁc sequences in the promoter: the C-repeat (CRT) and dehydration responsive element (DRE)-related motifs which interact with the CRT/DRE binding factor 1 (CBF1; Stockinger et al., 1997). When the Arabidopsis CBF1 gene was introduced into tomato, the transgenic plants harbored higher chilling tolerance. This response was associated with a decrease of ROS and pronounced tolerance to oxidative damages (Hsieh et al., 2002a). Cold stress also induces osmotic disorders. Thus tolerance to cold induces the transcription of genes encoding enzymes responsible for the synthesis of osmoprotectants and the antioxidant defense (Goyary, 2009). Osmotin and osmotin-like proteins were found to accumulate in plants under a wide range of biotic and abiotic stresses. Patade et al. (2013) reported that transgenic tomato plants accumulating osmotin and proline during cold treatment had better protection of cell structures and higher ROS detoxiﬁcation. As opposed to cold or freezing conditions, the production of plants tolerant to high temperature is of primary interest in regards to global warming and climate changes. The response of plants to high temperatures is characterized by metabolic changes which aim to protect the essential structures and functions of cells. The accumulation of polyamines, such as betaine, putrescine, spermidine or spermine, is one of these mechanisms. Indeed, betaine was found to protect enzymes, such as photosystem II of the photosynthetic machinery, against heat-induced inactivation (Allakhverdiev et al., 1996). S-adenosyl-Lmethionine decarboxylase (SAMDC) is one of the key regulators of polyamines synthesis. Tomatoes expressing the SAMDC gene of S. cerevisiae accumulated substantially higher amounts of spermine and spermidine and were found to be more tolerant to high temperature. Moreover, the antioxidant enzymatic activity and protection of lipid membranes against peroxidation was signiﬁcantly enhanced in the transgenic plants, showing that the accumulation of polyamines is a good strategy for protection against high temperatures (Cheng et al., 2009). As already mentioned, heat stress, and all abiotic stresses in general, generates the production of ROS, possessing highly oxidant properties. In order to protect themselves against ROS-induced damage, plants evolved antioxidant enzymes, such as superoxide dismutase (SOD) and ascorbate peroxidase (APX). Overexpression of cytosolic APX in tomato allowed the plant not only to protect itself from damage caused by high temperatures, but also to protect itself against damage caused by exposure to UV-B (Wang et al., 2006). Today, more than one-ﬁfth of the world's arable land suffers from salt stress. Salt stress is a major problem in agriculture worldwide, affecting crop growth, development, production, quality and yield. Increased salinization of arable land is expected to have devastating global effects, resulting in loss of 30% of arable land within the next 25 years, and up to 50% by the year 2050 (Wang et al., 2003). Saline stress is detrimental to plants because it brings water stress and inhibits key biochemical reactions due to the excess of sodium (Li et al., 2011; Moghaieb et al., 2011). To withstand saline stress, plants have developed several strategies: sequestration of solutes, limitation of lipid D 1021 1022 E 4.2. Resistance to abiotic stresses T 1020 peroxidation and/or production of osmoprotectants. The large, acidic vacuole of plants serves for sequestration of such deleterious solutes. A huge variety of ion transporters are localized on the vacuolar membrane, allowing the allocation of different ions and molecules into the vacuole (Martinoia et al., 2000). In tomato, expression of the Arabidopsis vacuolar Na+/H+ antiport (AtNHX1), which drives the export of salts from cytoplasm into the vacuole, resulted in the production of transgenic tomato plants able to grow in the presence of 200 mM NaCl. Interestingly, whereas leaves accumulated huge amount of salt, no changes in salt concentration were observed in fruit (Zhang and Blumwald, 2001). Another consequence of salt stress is lipid peroxidation with the production of methylglyoxal, a highly mutagenic and cytotoxic compound. The detoxiﬁcation of methyglyoxal is triggered by speciﬁc enzymes, glyoxalase I and II. Recently, the GlyI gene from Brassica juncea and the GlyII gene from Pennisetum glaucum were simultaneously introduced into tomato. In the transgenic tomatoes expressing both genes, lipid peroxidation and peroxide production were signiﬁcantly reduced. Moreover degradation of chlorophyll due to saline stress was limited in transgenic tomato plants. Altogether, this led to the conclusion that engineering the glyoxalase detoxiﬁcation system is a way to enhance tolerance to high salt concentration in tomato (Álvarez-Viveros et al., 2013). Moghaied and coworkers (2011) demonstrated that improving the osmoprotective system is also a good strategy to induce salt stress tolerance in tomato. Ectoine, a common solute of halophilic bacteria, is a good example of an osmoprotectant. Ectoine is synthesized from L-aspartate β-semialdehyde in a three-step reaction catalyzed by enzymes encoded by the ectB, ectA and ectC genes. When the three genes were introduced into tomato by Agrobacterium-mediated transformation, the resulting transgenic plants accumulated high amounts of ectoine in a dose-dependent response, i.e. the higher the concentration of salt applied, the more the ectoine accumulated. Water uptake and transport to leaves was higher in transgenic lines, suggesting that ectoine contributes to establish a proper water status upon stress. As already mentioned, salt stress negatively inﬂuences the overall growth of the plant, inhibiting leaf growth and inducing premature senescence. Plant growth and development require proper hormonal status. In salt-stressed plants, the general hormonal status is modiﬁed, and more speciﬁcally the endogenous cytokinin (CK) content is decreased. Overcoming the salt-induced reduction of CK could be means of engineering tolerance to saline stress. This can be achieved by increasing CK synthesis via overexpression of genes encoding enzymes for CK biosynthesis. The constitutive expression of the IPT gene, encoding the enzyme responsible for the ﬁrst step in CK biosynthesis, led to more than 150-fold increase of the CK content in tobacco and cucumber but had a deleterious effect inhibiting root growth and inducing water deﬁcit syndromes (Smigocki and Owens, 1989). The role of CK in salt stress tolerance in tomato was assessed by two nice experiments (Ghanem et al., 2011). In the ﬁrst experiment, overexpression of the IPT gene was driven by a heat shock inducible promoter. Transient root induction of the IPT gene resulted in a slight decrease in root biomass but when the saline stress was applied, the higher endogenous CK content delayed stomatal closure and leaf senescence, and induced a 2-fold increase in shoot growth. In the second experiment, the same authors grafted non-transgenic tomato plants onto the root systems of transgenic tomato plants (WT/35S::IPT) constitutively expressing the IPT gene. When the WT/35S::IPT plants were cultivated with moderate salt stress, the number and size of the fruit produced were signiﬁcantly enhanced compared to the non-transgenic, non-grafted tomato plants. These last results, taken together, show how a precise regulation of the hormonal status can be genetically engineered in order to produce tomato with enhanced tolerance to salt stress. Drought or water deﬁcit is an important environmental factor greatly affecting agriculture, making the management of water an important task in agriculture. Genetic engineering for drought tolerance/resistance is based on the knowledge gained from plants developing in arid and semi-arid regions. Plants growing in water-limited conditions have R O O F 1015 1016 15 Please cite this article as: Bergougnoux V, The history of tomato: From domestication to biopharming, Biotechnol Adv (2013), http://dx.doi.org/ 10.1016/j.biotechadv.2013.11.003 1079 1080 1081 1082 1083 1084 1085 1086 1087 1088 1089 1090 1091 1092 1093 1094 1095 1096 1097 1098 1099 1100 Q94 1101 1102 1103 1104 1105 1106 1107 1108 1109 1110 1111 1112 1113 1114 1115 1116 1117 1118 1119 1120 1121 1122 1123 1124 1125 1126 1127 1128 1129 1130 1131 1132 1133 1134 1135 1136 1137 1138 1139 1140 1141 1142 1143 1144 16 V. Bergougnoux / Biotechnology Advances xxx (2013) xxx–xxx 1173 1174 1175 1176 1177 1178 1179 1180 1181 1182 1183 1184 1185 1186 1187 1188 1189 1190 1191 1192 1193 1194 1195 1196 1197 1198 1199 1200 1201 1202 1203 1204 1205 1206 1207 1208 C 1171 1172 E 1169 1170 R 1167 1168 R F O 1162 1163 O 1160 1161 C 1158 1159 U N 1156 1157 R O Tomato cultivars developed by traditional methods soften during ripening, and require harvesting and transporting while fruits are still green. Since 1962, it has been clearly deﬁned that ethylene is the hormone driving ripening, as a rise in ethylene occurs before the onset of ripening (Burg and Burg, 1962) and ethylene production is maintained throughout ripening. The injection of ethylene allows the fruit to turn red. The disadvantage of this practice is that the processes which lead to development of natural ﬂavor are not induced, resulting in a tasteless fresh tomato (Paduchuri et al., 2010). Inhibition of fruit ripening, and consequently the extension of shelf-life and storage, by genetic engineering can be obtained by reducing or inhibiting ethylene production. This is reached by the down-regulation or silencing of genes encoding proteins involved in the ethylene biosynthesis pathway, such as aminocyclopropane-1-carboxilic acid (ACC) synthase or AAC oxidase (Hamilton et al., 1990; Oeller et al., 1991). Another possibility is to stimulate degradation of ethylene precursors by overexpressing genes encoding proteins responsible for this reaction, such as ACC deaminase or S-adenosyl methionine hydrolase (Good et al., 1994; Klee et al., 1991). In tomato, the method of hpRNA-mediated silencing was used to inhibit expression of the ACO1 gene, encoding for an ACC oxidase. The lower ethylene content in transgenic tomato plants was associated with a decrease in pectin methylesterase and polygalacturonase (PG) activities, and consequently a reduced loss of ﬁrmness during ripening. Nevertheless, the transgenic fruits developed their color later than the non-transformed fruits (Behboodian et al., 2012). This result conﬁrmed what has been known for a long time: alteration of the ethylene pathway affects color development. This is a negative aspect of the selection and points out the fact that alteration of the ethylene pathway is probably not the best target of genetic engineering for delayed ripening and/ or ﬁrmness. As already mentioned, PG is one of the targets of ethylene. This enzyme is responsible for the cell wall degradation which occurs during ripening and leads to fruit softening. In tomato, its expression was inhibited by the RNA antisense strategy. The resulting transgenic tomato plants harbored only 1% of residual PG activity and were characterized by ﬁrmer fruits. Ethylene production and lycopene accumulation were not modiﬁed in these transgenic fruits (Smith et al., 1990). The color of tomato fruit is due to the presence of β-carotene and lycopene, which both have been found to have a beneﬁcial effect on human health. Several attempts to produce a tomato with higher carotenoid content have been made. The PSY-1 enzyme catalyzes the ﬁrst committed step of the carotenoid biosynthesis pathway by producing phytoene from GGPP. In order to increase the carotenoid content of fruit, the Psy-1 gene was constitutively expressed in tomato. When the 1154 1155 P 1166 1151 1152 1153 D 4.3. Fruit quality 1149 1150 carotenoid content was signiﬁcantly increased in the fruit of transgenic plants, some undesirable effects were observed, notably dwarﬁsm of the transgenic plant, probably due to the lack of gibberellins. Indeed, both gibberellins and carotenoids are synthesized from GGPP and the probable consequence of accumulation of PSY-1 in the transgenic tomato was stimulation of carotenoid synthesis in detriment to gibberellins biosynthesis (Fray et al., 1995). The use of the PG promoter drove the expression of Psy-1 speciﬁcally in the fruit. While high accumulation of carotenoid could be measured in the fruit, the overall size of the plant was not affected (Fraser et al., 2002), highlighting again the advantages of using organ-speciﬁc promoters. The spontaneous tomato high-pigment mutant is characterized by a high accumulation of carotenoids and the accumulation of other molecules such as ﬂavonoids, vitamins C and E, thus enhancing the nutritional quality of the fruit (Azari et al., 2010). Surprisingly the corresponding gene does not encode an enzyme involved in the carotenoid biosynthesis pathway. Molecular characterization of the mutants revealed that the mutation affects the tomato homolog of Arabidopsis DEETIOLATED (DET1), a negative regulator of photomorphogenesis (Mustilli et al., 1999). The suppression of DET1 in tomatoes by RNAi technology resulted in signiﬁcant increases of both carotenoids and ﬂavonoids without deleterious effects on other parameters (Davuluri et al., 2005). It appears that modeling the expression of genes which regulated the biosynthesis pathway but not directly the genes of the biosynthesis pathway is more efﬁcient in genetic engineering of the tomato and should be further considered in modern genetic engineering strategies. Together with color, the taste and ﬂavor of fruit are very important criteria for tomato selection today. Taste is determined by an equilibrium between sugars (sweet) and organic acids (acid). Because it is important to maintain low acidity of the fruit for processing tomatoes (discussed previously), it is not of interest to modify the acid content of the fruit. Just the opposite, it is probably preferable to modify the sweetness of the fruit. This can be achieved by increasing the sugar content, but in a society where people ﬁght obesity, this would not be a good strategy. The African plant katemfe (Thaumatococcus daniellii Benth.) produces a sweet-tasting protein called thaumatin (Van der Wel and Loeve, 1972). In addition to its sweet taste, thaumatin has the property of intensifying some ﬂavors while attenuating others. The mechanisms of thaumatin action are still unknown. Thaumatin extracted from fruit or synthesized by microorganism was, and still is, widely used in the food industry. In order to modify the taste of tomato, the sequence encoding thaumatin was introduced by Agrobaterium-mediated transformation. The transgenic plants produced fruits with enhanced sweetness (Bartoszewski et al., 2003). This emphasizes the fact that in order to overcome the lack of taste characteristic of late ripening varieties thaumatin could be introduced into tomato cultivars with rin or nor background. The enrichment of tomato ﬂavor can be achieved by synthesizing molecules which are known to participate in the ﬂavor and aroma signature of different aromatic plants, such as monoterpenes. Because monoterpenes, like carotenoids, are synthesized from IPP and DMAPP, their synthesis can be initiated in tomato fruits by introgression of the proper gene. Geraniol is the main aromatic compound of basil (Ocinum basilicum) and confers a characteristic sweet ﬂoral aroma. Thus, Davidovich-Rikanati et al. (2007) expressed the Ocimum basilicum geraniol synthase gene under the control of the ripening-speciﬁc PG promoter. The ﬂavor signature of the tomato fruit was modiﬁed by the accumulation of geraniol in the fruit and greatly appreciated by the tasters. The negative point of the new transgenic lines is that the modiﬁcation of the ﬂavor/taste was made in detriment to lycopene accumulation, resulting in a depreciation of the nutritional value of the fruit. β-carotene is the precursor of vitamin A, which has a high antioxidant property, making it of interest in human health. As mentioned earlier, the early step of β-carotene synthesis is the production of lycopene from phytoene by the action of the phytoene desaturase. The carotene E 1165 1147 1148 T 1164 evolved two mechanisms which can be genetically engineered: 1) delay of drought stress by developing a deep root system, reducing transpiration or increasing wax layers on the leaf surface, 2) tolerance to drought by reducing the need for water for efﬁcient growth (Kramer and Boyer, 1995). As previously mentioned, mechanisms conferring tolerance to one stress can also confer tolerance to another one. This is the case of the CBF1 gene, which was initially found to improved salt tolerance in tomato (Hsieh et al., 2002a). The same authors demonstrated that the ectopic expression of Arabidopsis CBF1 in tomato also confers resistance to drought stress (Hseih et al., 2002b). In order to withstand drought stress, plants accumulate solutes into their vacuole, modifying the overall osmotic status of the cell favoring water uptake from the soil. This can be done either by increasing the activity of the vacuolar sodium/ proton antiporter or by increasing the uptake of protons into the vacuole, energizing secondary transporters (Pasapula et al., 2011). Vacuolar proton uptake is ensured by proton pumps (VP1). Overexpression of the Arabidopsis vacuolar H+-pyrophosphate (AVP1) in tomato conferred tolerance to both salt and drought stress. This was marked by greater import of cations into root vacuoles and higher root biomass (Park et al., 2005). 1145 1146 Please cite this article as: Bergougnoux V, The history of tomato: From domestication to biopharming, Biotechnol Adv (2013), http://dx.doi.org/ 10.1016/j.biotechadv.2013.11.003 1209 1210 1211 1212 1213 1214 1215 1216 1217 1218 1219 1220 1221 1222 1223 1224 1225 1226 1227 1228 1229 1230 1231 1232 1233 1234 1235 1236 1237 1238 1239 1240 1241 1242 1243 1244 1245 1246 1247 1248 1249 1250 1251 1252 1253 1254 1255 1256 1257 1258 1259 1260 1261 1262 1263 Q95 1264 1265 1266 1267 1268 1269 1270 1271 1272 1273 1274 V. Bergougnoux / Biotechnology Advances xxx (2013) xxx–xxx 1329 5. Conclusion 1330 1331 Since its discovery in the 16th century and its ﬁrst steps into domestication and breeding more than 600 years ago, tomato has become one of, if not the most important vegetable crop worldwide. Interest in tomato is increasing with the population. With current predictions of population increase and climatic changes, it is assumed that traditional breeding of tomato is not sufﬁcient to satisfy future demand and climatic changes. Development of the plant's molecular biology coupled to its 1301 Q96 1302 1303 Q97 1304 1305 1306 1307 1308 1309 1310 1311 1312 1313 1314 1315 1316 1317 1318 1319 1320 1321 1322 1323 1324 1325 1326 1327 1332 1333 1334 1335 1336 C 1299 1300 E 1297 1298 R 1295 1296 R 1294 O 1292 1293 C 1290 1291 N 1288 1289 U 1286 1287 R O O F 1328 In the past few years, a new concept, called biopharming, has been developing. Biopharming consists of using plants to produce therapeutic molecules which will be further puriﬁed or introduced directly into the human or animal diet. Despite the fact that bacterial fermentation, yeast systems and mammalian cell cultures are still widely used to produce molecules important in treating cancers or different human diseases in huge amounts, the costs of development linked to puriﬁcation are very signiﬁcant. Up to now, more than 100 therapeutic and diagnostic recombinant proteins and vaccines have been produced in various plants, including tobacco, cereals, legumes, fruit and vegetable crops. Plants have several advantages over the classical modes of production in term of economy, production scale and safety (Ahmad et al., 2012; Chen et al., 2009). Alzheimer's disease (AD) is a neurodegenerative disease leading to neuron destruction. The toxic brain protein responsible for AD, betaamyloid (Aβ), has been identiﬁed and is accumulated in patients developing AD. One strategy to prevent and cure AD would be the use of vaccines directed against Aβ. Attempts to produce and purify Aβ as an antigen in Escherichia coli or yeast systems have been laborious because of the toxicity of the protein itself. Thus Youm et al. (2008) initiated the production of Aβ in tomato fruit. They were able to produce the protein in a satisfactory amount and to use it in an immunization assay on mice. Thymosin α1, a booster of the immune system, is widely used in treatment against viral infections (hepatitis B and C) and cancers. Until now it has been derived from animal thymus or produced chemically; nevertheless, the amount of Tα1 produced is not sufﬁcient faced with increasing demand for the medicine. Using Agrobacterium-mediated transformation, Tα1 was speciﬁcally expressed in the fruit of tomato. The protein could be easily extracted from the fruit and the yield was up to 6 μg/g fresh weight. Moreover, the activity of the Tα1 produced by tomato was higher than that produced by E. coli (Chen et al., 2009). Examples of tomato genetic engineering for the purposes of biopharming are becoming more and more numerous, and tomato has already been used for the production of different vaccines (reviewed in Ahmad et al., 2012). Beside its use to produce vaccines and therapeutic molecules, the tomato is also used as a bioreactor to produce molecules which are “more exotic”. This is the case of “miraculin”. Miraculin is the active compound of the miracle fruit, Synsepalum dulﬁcum. It has the property to change any sour taste into a sweet and pleasant savor (Kurihara and Beidler, 1968). The production and puriﬁcation of miraculin in E. coli systems was not sufﬁcient enough and it is very recently that researchers have used tomatoes as bioreactors for widerproduction of the compound. The amount of miraculin in transgenic tomato fruit was up to 90 μg per g of fresh weight (Hirai et al., 2010). P 1284 1285 1281 1337 1338 1339 1340 1341 1342 1343 1344 1345 1346 1347 1348 1349 1350 1351 1352 1353 1354 1355 1356 1357 1358 1359 6. Uncited references 1360 Q98 Dibble et al., 1998 Grover et al., 2013 Livingston, 1893 Peralta et al., 2006 1361 D 4.4. Biopharming 1279 1280 E 1283 1277 1278 genome sequencing and the study of wild relative species, have allowed researchers to go beyond the limits of classical breeding. The culture of genetically modiﬁed (GM) tomatoes encounters problems in most of the leading producer countries. Indeed since the arrest of GM tomato culture in the USA in 2002, only China remains a producer of GM tomatoes. This is mainly due to the negative opinion of the population that GM crops are deleterious or, even worse, dangerous for human health and the environment; this is the consequence of misinformation. As scientists, our duty is not only to produce crops with engineered agronomical traits, but also to educate and inform the people around us. The use of marker-free transgenic plants – i.e. devoid of resistance of antibiotic or herbicides – should provide a good argument in favor of the use of such plants. Moreover, we also have to take advantage of knowledge from wild relative species. Indeed introgression of genetic information from wild or related species into the cultivated tomato and limitation of the transfer of alien information would limit the risk of deleterious effects on the environment and on human or animal health. Finally, while GM tomatoes are promising, their potential has rarely been validated in ﬁeld trials. Such trials, as well as study of impact on health and the environment, have to be developed and the results have to be brought to the awareness of society. If we do not invest part of our time in doing this, why should we continue developing crops useful to humanity? T 1282 desaturase (Crtl) gene from Erwinia uredovora was introduced into tomato in order to increase β-carotene content. Because the production of phytoene mediated by phytoene synthase is the limiting step of carotenoid synthesis, no difference in the total amount of carotene could be measured in transgenic tomato fruits. Instead, the quality of the carotenoids produced was modiﬁed with a three-fold increase of β-carotene content, representing up to 45% of the total carotenoid content (Römer et al., 2000). 1275 1276 17 1362 1363 1364 Acknowledgments 1365 The author would like to thank J. Humplik and P. Galuszka for their criticism during the preparation of the present manuscript and M. Sweney for English correction of the text. Finally, the author thanks K. Janošíková for the design of Fig. 3. 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Bergougnoux / Biotechnology Advances xxx (2013) xxx–xxx U N C O R R E C T E D P R O 1789 Please cite this article as: Bergougnoux V, The history of tomato: From domestication to biopharming, Biotechnol Adv (2013), http://dx.doi.org/ 10.1016/j.biotechadv.2013.11.003 1768 1769 1770 1771 1772 1773 1774 1775 1776 1777 1778 1779 1780 1781 1782 1783 1784 1785 1786 1787 1788

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