Lambers2020 Article TowardsMoreSustainableCropping

Theor. Exp. Plant Physiol.
https://doi.org/10.1007/s40626-020-00180-z (0123456789().,-volV)
(0123456789().,-volV)
Towards more sustainable cropping systems: lessons

from native Cerrado species
Hans Lambers . Patrı́cia de Britto Costa . Rafael S. Oliveira .
Fernando A. O. Silveira
Received: 10 May 2020 / Accepted: 7 July 2020

Ó Brazilian Society of Plant Physiology 2020
Abstract Our aim was to explore the potential of provided by the Cerrado that support agriculture. We
Cerrado, a biodiversity hotspot which is a reservoir of conclude that the Cerrado is a rich source of plant
genetic resources of agriculture-relevant traits to be species and plant traits to deal with environmental
used towards enhancing the sustainable use of agri- constraints such as soils with a low availability of P, a
culture in the region. We searched for pertinent low pH, high availability of Al, and a low availability
articles dealing with all relevant aspects of Cerrado of water. Allowing species extinction to continue will
that we cover in our review. We focus on P-acquisition make many untapped resources unavailable for future
and P-use strategies, aluminium resistance, and plant generations for incorporation into agriculture. Rather
water relations. We review results from a wide range than allow further destruction to continue, scientists
of sources, to develop a case to curtail further should explore relevant traits in native Cerrado species
destruction of native Cerrado vegetation, and works towards sustainable yields of currently used land.
towards more sustainable crop and pasture systems in
the region. We highlight many genetic resources that Keywords Biodiversity hotspot Cerrado Habitat
have tremendous potential to improve sustainable crop destruction Phosphorus Plant water relations
yield, while maintaining the key ecosystem services Sustainable agriculture
H. Lambers (&) P. de Britto Costa R. S. Oliveira

School of Biological Sciences, Institute of Agriculture, Departamento de Biologia Vegetal, Institute of Biology,
The University of Western Australia, 35 Stirling University of Campinas – UNICAMP, Campinas, Brazil
Highway, Crawley (Perth), WA 6009, Australia
e-mail: hans.lambers@uwa.edu.au F. A. O. Silveira
Departamento de Genética, Ecologia e Evolução,
H. Lambers Universidade Federal de Minas Gerais, Av. Antônio
College of Resources and Environmental Sciences, Key Carlos, Belo Horizonte, MG 6627, Brazil
Laboratory of Plant-Soil Interactions, National Academy
of Agriculture Green Development, Ministry of
Education, China Agricultural University,
Beijing 100193, China
P. de Britto Costa
Programa de Pós Graduação em Biologia Vegetal,
Institute of Biology, P.O.Box: 610, University of
Campinas – UNICAMP, Campinas, SP 13083-970, Brazil
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1 Introduction Fig. 1 Landscapes, plant species and root structure in Cerrado. c

a, b Typical landscapes in Cerrado sensu stricto, in Delfinópo-
lis, Minas Gerais; the taller trees in A are Vochysia thyrsoidea.
Brazil’s Cerrado savannah (Fig. 1) is the second- c A typical Cerrado in Três Marias, Minas Gerais. The tree in
largest biome in South America, covering an area the the foreground is Salvertia convallariodora. d Gallery forest
size of England, France, Germany, Italy and Spain along Preto River in Chapada dos Veadeiros, Goiás. e Campo
combined (Lahsen et al. 2016). It has long been known sujo in Chapada dos Veadeiros, Goiás. f Sand-binding roots of
Discocactus placentiformis. g Vellozia epidendroides, which
for its high biodiversity (Eiten 1972), and recognised belongs to a family (Velloziaceae) of species that are highly
as a global biodiversity hotspot; that is, a region efficient at acquiring phosphorus and coping with water stress.
‘‘where exceptional concentrations of endemic species h Natural habitat of Discocactus placentiformis in Serra do
are undergoing exceptional loss of habitat’’ (Myers Cabral, Minas Gerais state; this non-mycorrhizal cactus has
specialised roots that release carboxylates. i Sand-binding roots
et al. 2000). The Cerrado has the richest flora among of Discocactus placentiformis, which release phosphorus-
the world’s savannahs, with more than 12,000 species mobilising carboxylates into the nutrient-impoverished sand.
and high levels of endemism (Klink and Machado Photos: a-b, e–i Rafael S. Oliveira; c Fernando A.O. Silveira;
2005; Filardi et al. 2018). Yet, it is experiencing d Patrı́cia de Britto Costa; f Hans Lambers
increasing rates of habitat destruction and biodiversity
loss. Brazil has reduced deforestation in the Amazon
by almost 80% until 2015, but the neighbouring Cerrado (Lahsen et al. 2016). It is a clear case of
Cerrado biome has not experienced a similar decline in robbing Peter to pay Paul. The carbon emissions may
devastation, although it hosts some 4,800 species of be less than when clearing Amazon rainforest, but they
plants and vertebrates found nowhere else (Brann- still equate to 34 Mg C-equivalent ha-1 (cropland) or
strom et al. 2008; Strassburg et al. 2017). Less than 41 Mg C-equivalent ha-1 (pasture) for the period of
half of the original two million square kilometres of 1970–2005 due to land use change (Cerri et al. 2018).
the Cerrado vegetation remains, and there are many Others believe that large areas of Cerrado should be
uncertainties as to how to conserve remaining areas targeted with tree planting, to enhance carbon seques-
effectively (Morandi et al. 2020; Ratter et al. 1997). tration and mitigate climate change; we deal with this
Landscapes are fragmented and reconfigured (Car- aspect in a separate section below. Framing the
valho et al. 2009) around simplified commodity Cerrado as a ‘barren wasteland’ ignores numerous
production, redefining all else as ‘weeds or waste’, values and uses of the land and disregards the massive
and some agronomists regard the Cerrado as a ‘barren scale of environmental destruction brought about by
wasteland’ (Ofstehage 2017, 2018). the conversion of the Cerrado into soybean fields
Agricultural expansion has driven rapid economic (Ofstehage 2017, 2018). In this review, we argue that it
development, but also has major impacts on biodiver- would be far better using the available farmland more
sity and ecosystem services in Brazil (Ferreira et al. effectively, rather than destroy more native vegeta-
2012). The soybean production chain in Brazil has tion, drive more species to extinction, further pollute
strived to present to its overseas customers a story of a the adjacent environment, erode ecosystem services,
commodity produced in a sustainable manner, with no disturb the hydrological balance, and contribute
net forest loss, but if we zoom in on the Cerrado, significantly to the rise in atmospheric CO2 concen-
sustainable soy production in Brazil turns out to be a tration. All these negative effects, combined or in
myth (Lima et al. 2019). Across 200 million hectares isolation, will have detrimental repercussions for the
of tropical savannah, agribusiness continues to expand long-term success of the Brazilian agribusiness and
rapidly; with limited conservation incentives, extinc- food security.
tions of global significance are expected (Strassburg Stress-resistant crops are needed to ensure yield
et al. 2016). Cerri et al. (2018) reported that carbon stability under stressful conditions and to minimise the
emissions from agroecosystems are 4 to 5.5 times environmental impacts of crop production (Zhang
greater by bringing new land under production in the et al. 2018). The Cerrado is a rich reservoir of genetic
Amazon than in the Cerrado, for pastures and cropland resources and ‘biological innovations’ to deal with
production, respectively. They then use these figures to environmental constraints (Haridasan 2008; de
justify agricultural intensification in the Cerrado, Andrade et al. 2011; Lannes et al. 2016; Silveira
disregarding the enormous biodiversity values of the et al. 2016; Ferreira et al. 2017; Schiassi et al. 2018).
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Native vegetation in the Cerrado is key to the 1.1 Characteristics of soils in Cerrado: very
maintenance of climate and natural resources essential low P availability and seasonally with a low
to human survival, but the 41% increase in the region’s availability of water
deforestation rate between 2010 and 2014 goes largely
unnoticed (Lahsen et al. 2016). Extinction of any plant Most of the soils of the Cerrado are highly weathered
species in the Cerrado and destruction of the vegeta- oxisols and ultisols, and some entisols, with serious
tion are, therefore, not only of ecological, but also of limitations to food production mainly due to the very
great economic importance. For example, it has low soil fertility. Cerrado soils are acid, with a low
recently been discovered that some species in campos natural availability of nitrogen (N), phosphorus (P),
rupestres, which is part of the Cerrado sensu lato, potassium (K), calcium (Ca), magnesium (Mg), zinc
exhibit phosphorus (P)-acquisition strategies that are (Zn), boron (B), and copper (Cu), and the P-sorption
based on carboxylate release These include Discocac- capacity is very high because of high concentrations of
tus placentiformis (Cactaceae), a common species on oxides of Fe and Al (Lopes and Guimarães Guilherme
severely nutrient-impoverished white sands (Abrahão 2016; Goedert 1983). As a result, the extractable (or
et al. 2014) (Fig. 1h, i) and two Barbacenia species ‘plant-available’) P concentrations is low, whereas the
(Velloziaceae) that colonise quartzite rocks (Teodoro total P concentration is fairly high (Goedert 1983;
et al. 2019) (Fig. 1g). There are also fascinating Hayes et al. 2018). We have to bear in mind that
adaptations at the leaf level. Unlike species that have ‘plant-available’ P for most crop plants is low,
evolved in fertile landscapes that allocate a relatively whereas much more P can be acquired from the same
large proportion of leaf P to metabolically-inactive soil by plants with a P-mining carboxylate-releasing
epidermal cells, Cerrado species in several eudicot strategy, as discussed below (Lambers et al. 2008).
families preferentially allocate P to photosyntheti- Aluminium (Al) may also become toxic, because of
cally-active cells (Guilherme Pereira et al. 2018). This the low soil pH and high soil Al concentrations
trait contributes to their high photosynthetic P-use (Haridasan 1982), and this is likely also the case for
efficiency (Hayes et al. 2018; Guilherme Pereira et al. manganese (Mn) (Lambers and Oliveira 2019). Cu-
2019). The traits of some Cerrado species discussed pania tenuivalvis (Sapindaceae) is a native species
above are unseen in any crop species, but are highly naturally occurring on acidic soils in Cerradão vege-
desirable in future programs of genetic improvement tation in Brazil, with leaf [Mn] of 3300 lg Mn g-1 dry
of our crops (Cong et al. 2020), so losing the species weight (Viani et al. 2014). Therefore, the mechanism
that express these traits before we have had a chance to of native Cerrado species to deal with Al and Mn
explore them may be at our peril. We should take toxicity (de Souza et al. 2017; Nogueira et al. 2019)
advantage of the valuable traits in thousands of may also be useful to improve crop performance.
naturally stress-tolerant Cerrado species to increase Liming in combination with fertilisation with P, K, S
global food security and human health (Zhang et al. and micronutrients has allowed the Cerrado region to
2018), and minimise predicted increases in conflicts become available for over 60% of the Brazil’s
between food production and nature conservation soybean, corn, coffee and beef production (Yamada
(Laurance et al. 2014). 2005).
The aim of this review is to explore the potential of The Cerrado’s native flora and fauna are highly
Cerrado, a biodiversity hotspot and a reservoir of adapted to the region’s seasonally-dry climate, and
genetic resources of agriculture-relevant traits avail- survive during the dry season in either an active or a
able to enhance the sustainable use of agriculture in dormant state; crops planted in this region, however,
the region. We, therefore, do not cover a wide range of are often irrigated, especially during the six-month
other fascinating aspects of Cerrado such as traits long dry season (Sanches et al. 2017; Santin et al.
related to coping with fire (Fidelis et al. 2019; da Silva 2019). The Cerrado vegetation is considered an
and Rossatto 2019) and pollination and reproductive ‘inverted forest’, because most plants invest in deep
biology (Oliveira and Gibbs 2002; Silveira et al. roots: low shrubs and trees barely visible above the
2016). surface invest up to 75% of their biomass below-
ground (Oliveira et al. 2005; Lahsen et al. 2016),
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allowing resprouting following droughts, fires and produce extensive aerial roots that secrete carbohy-
herbivory. drate-rich mucilage that harbours diazotrophic taxa
A low availability of soil P, acidic soils and high and exhibit nitrogenase activity. Field experiments
availability of soil Al, and a low availability of water using 15N natural abundance or 15N-enrichment
tends to restrict the growth of most crop plants, but assessments have shown that atmospheric N2 fixation
native plants in Cerrado obviously cope with these contributes 29-82% of the N nutrition of this maize
conditions, and hence must have specific adaptations. landrace.
We will explore what we know about these adapta- Given the success with N2-fixing endophytes in
tions below. sugarcane in Cerrado, it would appear worth exploring
it this can be extended to other non-legume crops.
2 Cerrado soils also show low N availability 2.1 Economic losses due to drought, excessive
use of fertilization and liming
Whilst P is typically more limiting for plant produc-
tivity on old soils than N (Walker and Syers 1976), In addition to the relatively low total P availability in
Cerrado soils also exhibit a low N availability (Lopes Cerrado oxisols, ultisols and entisols, we also have to
and Guimarães Guilherme 2016). In young soils, N consider the high soil P-sorption capacity of these soils
availability gradually increases during pedogenesis as (Roy et al. 2017). The minerals responsible for the
a result of biological N2 fixation, but because this strong sorption of P in the Cerrado soils are iron (Fe)
process requires substantial amounts of P (Raven and aluminium (Al) oxides and hydroxides, which
2012), N availability declines again as P availability comprise the dominant mineralogy in the clay fraction
declines to very low levels at later stages of soil of most soils in the central-western (tropical) regions
development (Walker and Syers 1976; Turner and of Brazil (Nitzsche et al. 2008; Schaefer et al. 2008).
Condron 2013). Different soil nutrient availability Thus, about 50% of the P-fertilisers used for cropping
selects for species differing in nutrient-acquisition and is actually trapped in soil particles, unavailable for
-use strategies (especially below-ground traits) which plant uptake (Lun et al. 2018; Peñuelas et al. 2020),
explains the very high species turnover at a very small thus, inefficient to increase crop yield. As a conse-
scale between soil types in Cerrado (Abrahão et al. quence, the conventional way of using fertilisers have
2019). great economic loss, being about 50% of the money
In a fire-prone environment like Cerrado, N is spent being wasted, with no increase in crop yield, but
continually lost during fires (Silva et al. 2013; Schmidt with significant, detrimental offsite effects on terres-
and Eloy 2020). These losses are predominantly trial and aquatic ecosystems (Laurance et al. 2014).
compensated by biological N2 fixation, especially Phosphorus is poorly mobile in soil, but may be lost
symbiotic N2 fixation involving legumes, for example from the system through wind erosion and runoff, and
Mimosa species associated with Burkholderia as through leaching on a geological time scale (Cong
symbiont (Bueno dos Reis et al. 2010). et al. 2020). Thus, most of the sorbed P-fertiliser stays
Several authors have reported a low response of in the systems for a long time, but could be used by
Saccharum officinarum (sugarcane) to N fertilisation plants with P-acquisition strategies that are common in
in Cerrado, and found evidence for biological N2 Cerrado plants (Oliveira et al. 2015). This could also
fixation as one of the processes involved with the improve the yield of the next crop in areas that have
observed effect (Boddey et al. 2003). Acetobacter already been converted to croplands, but are consid-
diazotrophicus, an acid-tolerant endophytic bacterium ered marginal. As our understanding of plant-soil
that grows best on a sucrose-rich medium, has been interactions increases, we will have means to turn
isolated from sugarcane stems (James et al. 1994), but these nutrients that are considered unavailable for
other microbes likely also play a role (Boddey et al. conventional crop plants into a source of nutrients for
2003; Reis and dos Santos Teixeira 2015). Recently, plants that show traits that are common in adapted
an N2-fixing symbiosis was discovered in a landrace of Cerrado plants (Abrahão et al. 2019, 2020; Teodoro
Zea mays (maize), which grows well in N-depleted et al. 2019). This includes the release of phosphorus-
soil in Mexico (Van Deynze et al. 2018). These plants mobilising carboxylates. Within currently used crop
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species, there are some that express these traits such as Despite claims in a highly-cited article in a high-
lupins (Lambers et al. 2013). Several Lupinus species profile journal that arsenic can replace P in DNA of a
are native to Cerrado (Simon and Pennington 2012), bacterium (Wolfe-Simon et al. 2011), there is not
but none have been explored for their potential as really an alternative for phosphate. Arsenodiester
crops. In chickpea, there is a large variation in linkages in the putative arsenic-containing DNA
carboxylate release, which can readily be selected would undergo very rapid hydrolytic cleavage in
for by measuring leaf Mn concentrations (Pang et al. water at 25 °C with an estimated half-life of 0.06 s. In
2018; Wen et al. 2020). We envisage that a similar contrast, the phosphodiester linkages of native DNA
variation in carboxylate release exists in soybean undergo spontaneous hydrolysis with a half-life of
germplasm (Cong et al. 2020). approximately 30,000,000 year at 25 °C (Fekry et al.
2011). Possible reasons that nature really ‘chose’
phosphate is an interplay between two counteracting
3 Phosphorus as a non-renewable resource effects: on the one hand, phosphates are negatively
and non-replaceable nutrient charged and the resulting charge-charge repulsion
with the attacking nucleophile contributes to the very
Phosphorus is a macronutrient that frequently limits high barrier for hydrolysis, making phosphate esters
plant productivity in natural systems in ancient among the most inert compounds known. The same
landscapes, whereas N tends to be the most limiting charge-charge repulsion that makes phosphate ester
macronutrient in young landscapes (Walker and Syers hydrolysis so unfavourable, also makes it possible to
1976). Species that evolved in N-limited landscapes regulate, by exploiting the electrostatics (Kamerlin
have received most attention in the plant science et al. 2013). Mass spectrometry showed that the DNA
literature, because these include most crop plants as of bacteria that putatively replaced phosphate by
well as Arabidopsis thaliana (Plett et al. 2020). arsenate contains only trace amounts of free arsenate
However, vast numbers of species evolved in ancient and no detectable covalently bound arsenate (Reaves
and megadiverse regions of the world, including et al. 2012). So, we can safely conclude that for either
Cerrado, where P is the major limiting nutrient. Some native or crop plants, or for other living organisms and
of these may harbour traits that may be highly viruses, there is no alternative for phosphate, so we
desirable in crops plants, and hence deserve far greater had better use this non-renewable resource
attention (Prodhan et al. 2019). judiciously.
Most of the phosphate that is used for our crops is
derived from rock phosphate, which is a non-renew- 3.1 Numerous examples of very high
able resource. We are gradually running out of global P-acquisition efficiency in Cerrado
phosphate resources in an era when we need more P and similar vegetation
fertilisers to produce more food and fibre to sustain a
growing global population (Fixen and Johnston 2012; Old climatically-buffered infertile landscapes harbour
Johnston et al. 2014). In that context, there are likely numerous species with highly-efficient non-mycor-
numerous lessons to be learned from species that rhizal P-acquisition mechanisms, for example cluster
evolved highly P-efficient traits in ancient landscapes roots in Proteaceae and some other families in
(Lambers et al. 2015b; Prodhan et al. 2019). Australia and South Africa (Shane and Lambers
Unlike nitrate and sulfate, phosphate is not reduced 2005). Cluster roots release massive amounts of
in plants, but remains in its highest oxidised form. carboxylates in an exudative burst, and mobilise P
Therefore, even though the more reduced oxide of that is poorly mobile in soil (Dinkelaker et al. 1995). In
phosphorus (phosphite) is sometimes advertised as a addition, they mobilise a range of micronutrients
fertiliser, it is distinctly harmful when given to plants including Mn (Lambers et al. 2015c). Cluster roots can
that are already short of phosphate, because it is an also be found in Proteaceae in Cerrado, e.g., in
analogue of phosphate and inhibits its uptake (Car- Roupala montana, albeit in low numbers (Lambers
swell et al. 1996, 1997; Ratjen and Gerendás 2009; et al. 2015a). The leaf Mn concentration of Roupala
Loera-Quezada et al. 2015). montana is relatively high (de Campos 2012), which
makes it highly likely that this species uses a
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carboxylate-releasing P-mobilising strategy (Lambers the very high availability of Al in Cerrado soils, and
et al. 2015c). Functionally equivalent structures, i.e. the fact that Al-resistance is based on the release of
dauciform roots (Fig. 1f), are common in many carboxylates, we also expect numerous species releas-
Cyperaceae (Shane et al. 2006) including species in ing carboxylates, thus both mobilising P and immo-
Cerrado (Zemunik et al. 2018). In many phylogenet- bilising Al (Magalhaes et al. 2018). Cerrado species
ically-unrelated, non-mycorrhizal species, sand-bind- sensu stricto, rather than species from campos
ing roots also release carboxylates (Hayes et al. 2014), rupestres within Cerrado sensu lato, likely offer better
and this strategy is also common in Cerrado (Oliveira examples for crops, because the total soil P concen-
et al. 2015; Zemunik et al. 2018). tration is an order of magnitude greater, whereas the P
In addition to strategies that are known from other availability is similarly low as in campos rupestres
parts of the world, some Cerrado species exhibit (Hayes et al. 2018; Abrahão et al. 2019, 2020). Within
carboxylate-releasing structures that were new to crop species (e.g., Cicer arietinum, chickpea), there is
science till quite recently. Abrahão et al. (2014) substantial variation in carboxylate release, and
investigated P acquisition in Discocactus placen- among 100 genotypes, leaf [Mn] strongly correlate
tiformis (Cactaceae) (Fig. 1h, i), a common species with rhizosphere carboxylate concentrations (Pang
in nutrient-poor campos rupestres over white sands. et al. 2018). Breeding for crop cultivars that release
Cactaceae are generally considered, mycorrhizal, but substantial amounts of carboxylates would make
about 10% of all species are non-mycorrhizal (Wang perfect sense for strongly P-sorbing soils in Cerrado.
and Qiu 2006). Abrahão et al. (2014) found no Given the wide availability of germplasm in Glycine
mycorrhizal colonisation in this cactus, but rather a max (soybean) (Qin et al. 2017), there is tremendous
sand-binding root specialisation with rhizosheath potential to explore traits related to P-acquisition
formation (Fig. 1f, i). They first provided circumstan- efficiency (Vengavasi et al. 2017; Vengavasi and
tial evidence for carboxylate exudation in field Pandey 2018). In Western Ethiopia with low-P and
material, based on very high shoot Mn concentrations, acidic soils, a breeding program is under way to select
and then confirmed that Discocactus placentiformis low-P tolerant soybean genotypes (Tesfaye et al.
releases oxalate, and some malate, citrate and other 2020).
carboxylates, stimulated by P deficiency. The authors The large legacy stores of P in fertilised Cerrado
concluded that a sand-binding root specialisation in soil is estimated at 30 Tg, in 2016 worth over
this non-mycorrhizal cactus functions similar to that of $40 billion, and rising to 105 Tg by 2050 (Withers
cluster roots. Teodoro et al. (2019) found a similar et al. 2018). If genotypes with greater P-acquisition
strategy in two Barbacenia species (Velloziaceae) that efficiency were to be used, this legacy P could enable a
colonise quartzite rocks (Fig. 1). Their carboxylate- transition to more sustainable P-input strategies. This
releasing vellozioid roots occur in many species in this could reduce current annual P surpluses by 65%
family (Abrahão et al. 2020), and are capable of (Withers et al. 2018). In the longer-term, farming
growing inside quartzite rock, and gradually dissolve systems using crops that function at a lower plant-
the rock. These unique Cerrado traits may prove useful available soil P concentration would reduce the risk of
in developing more desirable agricultural systems, but erosion via wind and water, and tighten the P cycle in
are at risk of being lost before their potential is agriculture (Cong et al. 2020).
explored (Fernandes et al. 2018).
Given the strongly P-sorbing nature of Cerrado
soils (Lopes and Guimarães Guilherme 2016), we 4 Highly efficient P-use efficiency in P-
expect to find a wealth of species that access P based impoverished environments
on carboxylate-releasing strategies. A simple screen-
ing for leaf [Mn] relative to community-weighted Species that evolved in landscapes with a low soil P
average values would provide valuable information availability frequently exhibit a high P-use efficiency
(Lambers et al. 2015c; Oliveira et al. 2015). In fact, (Lambers et al. 2015b), in addition to their high
species of Fabaceae, Rubiaceae, Cyperaceae and P-acquisition efficiency, discussed above. They func-
Eriocaulaceae exhibit high leaf [Mn] in Cerrado areas tion at low leaf P concentrations, yet exhibit rapid rates
of northern Minas Gerais (Oliveira et al. 2015). Given of photosynthesis, and this a high photosynthetic P-use
123
efficiency, PPUE (Denton et al. 2007; Sulpice et al. Callisthene fasciculata, belonging to the same family
2014; Guilherme Pereira et al. 2019). Photosynthetic (Vochysiaceae), is rather unusual in accumulating Al
P-use efficiency is a complex trait, reflecting both whilst being calcicole, i.e. preferring soils with a high
allocation of P to different leaf P fractions including Ca availability (de Souza et al. 2020). This tree is
replacing phospholipids by lipids that do not contain P restricted to Ca-rich soils with a low availability of Al.
(Lambers et al. 2012) and functioning at low levels of These results illustrate the wide variation in soil types
nucleic acid P, especially low investment in ribosomal and plant strategies in the Cerrado that offer potential
RNA (Sulpice et al. 2014; Yan et al. 2019). In addition, for crop improvement.
species that evolved in P-impoverished landscapes Aluminium resistance in crops is often based on Al
preferentially allocate P to their photosynthetically- exclusion, rather than Al accumulation and internal
active mesophyll cells, rather than metabolically- detoxification (Kochian et al. 2015), but there are
inactive epidermal cells (Hayes et al. 2018), and this exception, for example Camellia sinensis (tea, Thea-
includes species in many lineages that evolved in the ceae) (Morita et al. 2004). Many Al-resistant geno-
Cerrado biome (Guilherme Pereira et al. 2018). types release carboxylates, which chelate and thus
detoxify Al (Delhaize et al. 1993; Klug and Horst
2010). A herbaceous Cerrado species, Stylosanthes
5 Aluminium resistance guianensis (Fabaceae) accumulates less Al in its roots
and displays less inhibition of root elongation than
Given the high availability of Al in Cerrado soils, we Stylosanthes capitata (Cassol et al. 2016). Citrate is
can expect many Cerrado lineages having evolved Al- the only carboxylate released into the rhizosphere in
detoxification and –resistance mechanisms in many Al-treated plants of both species, but the Al-resistant
lineages. Indeed, Haridasan (1982) found many Cer- Stylosanthes guianensis releases more. Clearly, we
rado species belonging to 17 families to accumulate Al can expect both Al-exclusion and Al-tolerance mech-
in their leaves in considerable amounts. High leaf Al anisms in Cerrado species that would be useful in
levels are not associated with low foliar levels of Ca, promoting Al resistance in crops.
Mg, K, Fe, Mn or Zn, compared with Cerrado species
that do not accumulate Al, and hence they exhibit
effective mechanisms for absorbing these cations from 6 Plant water relations
Cerrado soil. Whilst some Cerrado woody species are
Al-accumulating species, most exclude Al and species The seasonal contrast between the dry and rainy
of both groups grow well on acidic Al-rich soils season and the high temperatures and irradiance are
(Nogueira et al. 2019). characteristic for the Cerrado; these affect plant
Rudgea viburnoides (Rubiaceae) hyperaccumu- development and productivity (Eiten 1972). Cerrado
lates Al predominantly in its cell walls (Malta et al. plant species vary to a very large extent in their
2016). In Al-accumulating Miconia albicans, Miconia response to drought. Examples of morphological and
rubiginosa (Melastomataceae), Qualea grandiflora physiological traits exhibited by Cerrado plants to
and Q. parviflora (Vochysiaceae), silica granules are cope with seasonal drought include: (1) investment in
associated with Al in cell walls of non-lignified leaf deep roots (Bucci et al. 2004; Oliveira et al. 2005); (2)
tissues (Bressan et al. 2016). This suggests internal strong stomatal control in the dry season resulting in
detoxification of Al by the formation of aluminosil- high water use efficiency (Bucci et al. 2008; Meinzer
icate in Al -accumulating Cerrado species, as found et al. 1999; Franco 2002; Oliveira et al. 2015); (3) high
before (Britez et al. 2002; Hodson and Evans 2020; leaf drought resistance expressed as more negative
Sangster and Hodson 2001). Two rather unusual Al- turgor loss point (WTLP) (Brum et al. 2017); (4) high
hyperaccumulating Vochysiaceae, Qualea grandiflora leaf hydraulic conductance (K leaf) and leaf capaci-
and Callisthene major, store Al in their chloroplasts, tance (Hao et al. 2008); (5) drought deciduousness of
without apparent damage (de Andrade et al. 2011). trees on richer soils (Ratter et al. 1997); (6) desiccation
Most Al-accumulating species tend to be calcifuge, i.e. tolerance as observed in Velloziaceae on rock out-
preferring acidic soils, including the tree Vochysia crops (Alcantara et al. 2015). Plant desiccation-
tucanorum (Vochysiaceae) (de Souza et al. 2017). tolerance traits represent exceptional opportunities
123
for a climate-smart agriculture (Hilhorst and Farrant Cashew (Anacardium occidentale), which originates
2018). Resurrection plants withstand virtually com- from north-eastern Brazil (Johnson 1973), is already
plete desiccation (Gaff 1971; Lambers and Oliveira of global significance, whereas Cerrado cashew
2019) and are quite rare among vascular plants (Gaff (Anacardium othonianum) is currently used as food
and Oliver 2013), but the molecular mechanisms of source at a local scale. The fatty acid profile of its
desiccation-tolerance are beginning to be unravelled edible nuts is similar to that of traditional oilseeds
(Silva Artur et al. 2019). (Alves et al. 2016). The same holds for other oilseeds
Although resurrection species are not desirable as native to the Cerrado (baru almonds, from Dipteryx
crop plants, some of their traits definitely are. For alata, and pequi almonds, from Caryocar brasiliense),
example, late embryogenesis abundant (LEA) genes which all exhibit a fatty acid profile that is beneficial
encode a diverse group of stress-protection (LEA) for cardiovascular health (Alves et al. 2016). Pineap-
proteins expressed during embryo maturation in all ple (Ananas comosus) is another example. One of its
angiosperms (Bartels and Sunkar 2005). The LEA centres of domestication of the main cultivars is
proteins are not normally expressed in vegetative believed to be between the Brazilian and Venezuelan
tissues, but induced by osmotic stress or application of Amazon and their boundaries, and this is probably
ABA. Given the wide variation in Velloziaceae in the close to a centre of diversification (Loison-Cabot
way they cope with waters tress (Alcantara et al. 2015; 1992). However, the wild pineapple (Ananas ananas-
Brum et al. 2019), this family offers huge potential to soides) is an understorey species in Cerrado wood-
discover genes that enhance stress tolerance in crop lands (Almeida et al. 1998). It produces small fruits,
plants (Costa et al. 2017). Improved drought tolerance erect leaves and a long, fairly thin spike; is the hardiest
in wheat (Triticum aestivum) is considered essential to species in the genus, and grows in poor dry soils,
unlock the production potential of the Cerrado (Pereira where it can withstand very sunny positions (Loison-
et al. 2019). Cabot 1992). Those are just a few examples among
numerous Cerrado species that can potentially be
6.1 The need to use both P and water more turned into economically important crops that can
effectively in cropping systems support more sustainable agriculture systems (Pinto
et al. 2016).
Numerous Cerrado species can guide us towards
future crop genotypes and cropping systems that use P 6.2 The story of Arachis, a genus endemic
and water more efficiently. Velloziaceae species in to Cerrado that gave rise to Arachis
particular offer a good model for studying mecha- hypogaea (peanut)
nisms of both P-acquisition efficiency (Teodoro et al.
2019; Abrahão et al. 2020) and water-use strategies Arachis hypogaea, peanut or groundnut, is a very
(Porembski and Barthlott 2000; Alcantara et al. important food crop throughout the tropics and
2015, 2018). Crop wild relatives are a key component subtropics, but the genus is endemic to South America,
of the world’s flora, because since they offer the mostly associated with Cerrado (Bertioli et al. 2011).
potential to contribute traits for crop improvement. All 80 species in the genus are unusual among legumes
The rich flora of the Brazilian Cerrado (Simon et al. in that they produce their fruit below the ground.
2009) harbours a large number of crop wild relatives, Arachis species occur in diverse habitats including
but we know remarkably little about their distribution grasslands, open patches of forest and temporarily
and conservation status. A clear example is that of flooded areas. Most wild species are diploid, but
wild relatives of cassava (Manihot) in the Cerrado cultivated peanut is a tetraploid (AABB) descending
(Simon et al. 2020). Lessons from Cerrado native plant from two diploid ancestors, Arachis duranensis and
species could increase productivity and reduce envi- Arachis ipaensis (Bertioli et al. 2016). Arachis
ronmental impact. hypogaea originated about 400,000 years ago by a
Rather than restrict ourselves to traditional crops natural interspecific hybridisation followed by poly-
like soybean, maize and wheat, we could also develop ploidisation (Zhuang et al. 2020). Tetraploid peanut
‘novel’ crops, using Cerrado species that have been may have experienced genetic information exchange
used traditionally for centuries (Lannes et al. 2016).
123
with diploids more recently, recasting its complexity Massive agricultural expansion into the Cerrado
in evolution. region since the 1970s and the large extent of the
Cultivated peanut has a very narrow genetic base, Cerrado biome have increased awareness of the role of
and for traits such as disease and pest resistance, this Cerrado in the global carbon cycle and climate change.
has been a limitation to crop improvement (Bertioli Clearing and cultivation of native lands in the Cerrado
et al. 2011). Wild resistance genes have been trans- in general leads to a decrease in soil organic carbon
ferred to cultivated peanut, e.g., the gene for resistance when no fertilization is applied or when monocrop-
to Meloidogyne arenaria (root-knot nematode) from ping (Batlle-Bayer et al. 2010). More intensive forms
Arachis cardenasii (Clevenger et al. 2017). Arachis of agriculture and recommended best management
duranensis and Arachis stenosperma, which gave rise practices have the potential to reduce soil organic
to the reference Arachis A-genome, differ in their carbon losses on agricultural lands. The values and
response to water stress. A drought-tolerant genotype expectations only consider soil organic matter, and
of Arachis duranensis and a drought-sensitive geno- ignore the vast amounts of belowground biomass in
type of Arachis stenosperma have been used to Cerrado vegetation (Buisson et al. 2019). This below-
identify genes encoding regulators and effectors ground pool is estimated at 117 Mg C ha-1 (Busta-
involved in drought tolerance responses such as mante et al. 2006), whereas the soil organic is
activation of osmosensing molecular cascades, control 100–174 Mg C ha-1, both for a depth of 1 m
of hormone and osmolyte concentrations, and protec- (Bustamante et al. 2006; Batlle-Bayer et al. 2010).
tion of macromolecules (Vinson et al. 2018). Many studies have considered soil organic carbon
The genetic traits available in wild Arachis species stocks following land-use change (Batlle-Bayer et al.
in Cerrado provide a rich and valuable resource of wild 2010; Noojipady et al. 2017). In most agricultural
germplasm, which we might explore as novel sources system, however, management practices such as
of diversity and useful wild alleles to develop climate- fertilisation or soil drainage also alter fluxes of other
resilient peanut varieties (Leal-Bertioli et al. potent greenhouse gases such as N2O and CH4
2012, 2018). (Carvalho et al. 2014; Martins et al. 2015). For a full
assessment of the effects on global changes and their
6.3 Effects of ecosystem services: soil carbon mitigation, it is necessary to know the complete
storage and provision of freshwater balance of all greenhouse gases.
In terms of water security, the Cerrado contributes
The Cerrado is not only exceptionally biodiverse, but 43% of all Brazilian freshwater outside the Amazon,
also provides numerous essential ecosystem services despite occupying only 22% of the country’s surface
that we need to maintain to sustain agricultural (Lima et al. 2011; Strassburg et al. 2017). Water
systems. Carbon emissions from cropland expansion quality studies showed N enrichment in agricultural
in Cerrado have increased over the past decade in a catchments, indicating N-fertiliser impacts and poten-
new frontier of agricultural production that includes tial susceptibility to eutrophication following conver-
portions of Maranhão, Tocantins, Piauı́, and Bahia sion of native Cerrado. Pesticides are consistently
states, often referred to as Matopiba (Noojipady et al. detected throughout aquatic systems potentially
2017). Gross carbon emissions from cropland expan- accompanied by serious health implications (Hunke
sion in the Cerrado averaged 16.3 Tg C year-1 et al. 2015). Land-use changes tend to diminish
between 2003 and 2013, with forest-to-cropland ecosystem services provision, particularly sediment
conversion accounting for 29% of emissions. The retention and nutrient retention. These, in turn, result
fraction of forest carbon emissions from Matopiba was in lower stream sedimentation and eutrophication of
much higher; between 2010 and 2013, large-scale Cerrado rivers, thus impacting water quality (Resende
cropland conversion in Matopiba contributed 45% of et al. 2019). Therefore, the combined effects of land-
total Cerrado forest carbon emissions. Comprehensive use intensification under climate change will likely
national estimates of forest carbon fluxes, including all severely limit the Cerrado’s future agricultural pro-
biomes, are critical to achieve climate-mitigation ductivity and ecosystem stability (Hunke et al. 2015).
targets to reduce emissions from land use, land-use However, there are alternatives for this undesirable
change, and forestry (Noojipady et al. 2017). scenario. Establishing restoration programmes on
123
private properties with currently less native vegetation studies report changes in microbial functional group
than legally required could create habitat for 25% (Souza et al. 2016), which may make the establish-
more threatened species than now found in these ment of essential symbioses that protect native species
places, and could also enhance water security and against soil pathogens impossible (de Pontes et al.
carbon stock (Vieira et al. 2018). Narrower riparian 2017).
vegetation has less potential to buffers soil erosion After many studies on Cerrado restoration, by
than wider riparian forests. Therefore, instead of more different methods and approaches, researchers agree
deforestation, farmers should conserve and restore that there is still much complexity about the system to
riparian forests to reduce stream sedimentation, and learn before being able to predict any kind of
thus secure the supply of freshwater (Guidotti et al. restoration trajectory (Buisson et al. 2019). Studies
2020). Inevitably, promoting conservation and foster- on passive restoration of abandoned pastures, indicate
ing large-scale restoration are essential to guarantee that despite the high regeneration of Neotropical
water security (Strassburg et al. 2017), thus protecting savannahs, this vegetation will not regain the attributes
intermittent springs and watersheds that stabilise of old-growth savannahs (Cava et al. 2018). Similarly,
ecosystems and support agricultural productivity active restoration efforts such as direct seeding, have
(Hunke et al. 2015; Callisto et al. 2019). encountered positive results in terms of rapid soil
cover after seed dispersal, which limits the spread of
exotic invasives; however, fast-growing species still
7 Prevention is better than cure: restoration persist, indicating that functional traits will not match
of degraded land the ones of native Cerrado (Sampaio et al. 2019).
Recent and further studies on restoration of degraded
Liming and fertilisation with superphosphate have Cerrado effectively contribute to more sustainable
been used to improve cropping in natural grasslands, cropping systems (Haridasan 1989; Miccolis et al.
with detrimental effect for native vegetation. Invasive 2019).
African C4 species like Melinis minutiflora (molasses In addition to selecting the species and the method,
grass) and Urochloa spp. are superior competitors restoring the native Cerrado involves restoring the
under higher soil nutrient availability, while Cerrado positive feedbacks that maintain the native vegetation
native species are inferior competitors (Eller and resilient to exotic species invasion. There are a few
Oliveira 2017). Thus, due to land-use change and experiments being undertaken that evaluate if lower-
fertilisation, we observe a decline in plant species ing the soil pH and decreasing soil nutrient availability
richness and biodiversity in these areas (Bustamante can result in a competitive advantage of native species,
et al. 2012), even after years with efforts to restore the and the effects of initial functional group composition
native Cerrado (Durigan et al. 2007), with a prominent in the species and functional traits assembly (Coutinho
invasion of fast-growing exotic species. Such exotic et al. 2019). However, we are still far from under-
species are also cause of worldwide threats to standing how these restoration practises can help us
agricultural systems (Paini et al. 2016). restore key soil functions that would sustain the
The use of fertiliser and lime use change many soil Cerrado resilience.
properties, from mineralogy to organism community Grasslands are extremely vulnerable to anthro-
(micro- and macro-organisms), thus altering important pogenic disturbances, and their restoration after severe
soil functions that sustain the native Cerrado vegeta- soil disturbances rarely achieves management targets,
tion. Altered soil mineralogy favours exotic invasive species-diverse plant communities and endemic spe-
species that grow faster and outcompete native slower- cies recover very slowly (Buisson et al. 2019). Given
growing plants (Eller and Oliveira 2017). The persis- the high cost of ecological restoration, and the
tence of these alien species can promote imbalances of impossibility of returning ecosystems to pre-distur-
nutrient/carbon inputs in the soil, lowering microbial bance levels (Buisson et al. 2019), preventing large-
biomass and further increasing rates of nutrient scale disturbances by conserving existing natural
(P) mineralisation, maintaining a positive feedback vegetation is to be preferred.
that maintains nutrient-enriched soils, although not
enough to maintain crop yield. Additionally, many
123
Fig. 2 A conceptual model showing the need for a paradigm resources, and helping secure ecosystem services essential for a
shift in Cerrado agriculture. Currently (a), expansion of sustainable agriculture. Red arrows indicate negative effects,
agriculture relies on the large-scale devastation of the natural blue arrows indicate positive effects, and arrow widht indicates
Cerrado ecosystem. This compromises negative impacts on effect size. b Anticipated profits from traditional (red) and more
biodiversity and a decrease of the provision of ecosystem sustainable cropping systems (blue). Net profits are expected to
services that support agricultural systems. In more sustainable decline in the long run due to exhaustion of natural resources
cropping systems (b), expansion of agricultural activites relies and erosion of ecosystem services. In more sustainable systems,
on a sustainable use of resources and improved productivity on lower initial profit due to significant investment in research is
cleared marginal land. Impacts on Cerrado biodiversity and sustained in the long run
ecosystem services are smaller. Biodiversity provides genetic
8 Cerrado conservation: under attack storage will likely result in major C loss to the
from both friend and foe atmosphere during the recurrent natural and man-
made fires during the dry season (Veldman et al.
Oddly enough, the fate of the Cerrado is, paradoxi- 2019). This enterprise will most likely represent a
cally, also threatened by many conservation biolo- waste of time and resources, and contribute to further
gists, who fundamentally misunderstand the ecology climate change, rather than mitigate it (Zastrow 2019).
of open ecosystems (Bond 2019). Unfounded claims Understanding the functioning and drivers of Cerrado
that open ecosystems can be considered ‘dysfunctional vegetation are of utmost importance to define appro-
lands’, and need to accommodate more trees per priate conservation and management practices.
hectare, probably emerge from misconceptions of the
ecology of open ecosystems (Veldman et al. 2017).
Uncritical, extensive carbon-based tree plantations in 9 Concluding remarks
open ecosystems including the Cerrado have been
argued to provide suitable solutions to mitigate The scientific literature on Cerrado falls into two
climate change through C sequestration (Veldman extreme categories. Some papers celebrate the rise of
et al. 2019). Such recommendations are at odds with agriculture production in the Brazilian savannah as
scientific evidence, showing that planting trees where one of the greatest achievements of worldwide agri-
they do not belong causes significant loss of both cultural science in the twentieth century (Lopes and
animal and plant life (Abreu et al. 2017). It also leads Guimarães Guilherme 2016) and consider the region
to erosion of ecosystem services including provision as no more than ‘wasteland’. In the same spirit, the
of fresh water and carbon storage (Jackson et al. 2005; development of agriculture in Cerrado is considered as
Veldman et al. 2015a, b, 2019; Liu et al. 2020). Poorly an excellent way to protect the Amazon rainforest
planned tree plantings in the Cerrado will likely fail, (Cerri et al. 2018). At the other extreme, the Cerrado is
even in terms of C sequestration. The replacement of considered a biodiversity hotspot of global signifi-
its native plants, which typically store C belowground cance (Myers et al. 2000), which is under serious
(Buisson et al. 2019), by trees with little belowground threat from land-use change in favour of agriculture
123
(Strassburg et al. 2017). In their view, the notion that Acknowledgements HL acknowledges the support received
Cerrado comprises no more than ‘wasteland’ belongs as a keynote speaker at a recent meeting of the Brazilian Society
of Plant Physiologists which led to the initiative to write this
to a long-past era. review and Coordenação de Aperfeiçoamento de Pessoal de
There is no doubt that the rapid expansion and Nı́vel Superior (CAPES) – Brazil – Finance Code 001 (Capes,
intensification of agribusiness in Cerrado has signif- Project Grant PVE 88881.068071/2014-01 fellowship). FAOS
icantly impacted nitrogen enrichment in agricultural acknowledges grants from CNPq and FAPEMIG. RSO
acknowledges grants from CNPq and FAPESP-NERC (2019/
catchments (Taniwaki et al. 2017), and pesticides are 07773-1). PdBC acknowledges scholarship from Capes and
consistently detected throughout aquatic systems CNPq)
(Hunke et al. 2015). Conversion of native Cerrado
vegetation into crop and pasture land has also had a
significant impact on carbon emissions (Noojipady References
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Lambers2020 Article TowardsMoreSustainableCropping

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Theor. Exp. Plant Physiol.

Towards more sustainable cropping systems: lessons

Received: 10 May 2020 / Accepted: 7 July 2020

H. Lambers (&) P. de Britto Costa R. S. Oliveira

1 Introduction Fig. 1 Landscapes, plant species and root structure in Cerrado. c

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