Diseases of Fruit Crops in Australia

1 PLANT DISEASES – AN INTRODUCTION

Humankind has struggled with plant diseases since the dawn of agriculture. There are references in the Old Testament to the ravages of rust and blight on cereals and grapevines in the ancient world. The potato famine in Ireland in the 1840s led to the mass migration of Irish refugees to Australia, Britain and North America so that today, almost one in 10 Australians can trace their ancestry back to Ireland. The cause of the famine was the potato blight pathogen Phytophthora infestans, which destroyed plants and tubers under prolonged wet and cold weather.

Plant diseases are intimately connected with current issues facing agriculture and the environment. Global warming and rainfall reliability will have a considerable influence on disease distribution and severity in crops. Plant diseases are a major factor in world food security and biosecurity issues are a key component in international trade agreements. The absence of many damaging pathogens in Australia provides competitive advantage in trade and access to new markets. Furthermore, savings in costs associated with managing or eradicating these pathogens means that, in some cases, production is more efficient and sustainable than in overseas countries.

Fig 1.1 Healthy produce is a team effort between growers, horticulturists and plant pathologists.

Fig 1.2 The healthy farm (above) used the latest disease management systems. The sick farm (below) allowed the root rot disease Phytophthora to develop.

Causes of disease in plants

A simple definition of a plant disease is any disturbance that interferes with the plant’s normal structure, function or economic value. Plant diseases divide conveniently into (a) those caused by parasitic microorganisms or pathogens, and (b) non-parasitic diseases or disorders. These latter include mineral excesses and imbalances, incorrect storage conditions after harvest, environmental influences (such as atmospheric pollutants) and herbicide damage. Table 1.1 lists some physiological disorders of perennial fruit crops.

Fig 1.3 We also live with diseases that have been with us since the early days of horticulture in Australia.

Fig 1.4 Today’s modern herbarium retains original specimens and uses modern facelift packaging and state-of-the-art database technology.

Fig 1.5 The economic and social effects of incursions of major plant pathogens can be devastating, demonstrated by a recent outbreak of citrus canker in Queensland (now eradicated).

This handbook is concerned with diseases caused by pathogens. The major groups of plant pathogens are fungi, bacteria, viruses and nematodes. All diseases caused by pathogens are the result of an interaction between a susceptible plant, a pathogen capable of causing disease and a favourable environment.

The following sections outline the key characteristics of plant pathogens.

Fig 1.6 Conventional research and modern molecular techniques allow today’s plant pathologists to develop recommendations for managing plant pathogen outbreaks.

Fig 1.7 Cooperative, international research is important for Australia’s farming future. It enables a better understanding of potential threats to our horticulture.

Fig 1.8 Fungi are major causes of disease in horticulture crops. They attack every organ of the plant including leaves, fruit and roots. Left: blueberry rust (Pucciniastrum vaccinii ); centre: stem-end rot in mango (Lasiodiplodia theobromae ); right: Phytophthora in avocado roots (Phytophthora cinnamomi ).

Fungi

Fungi are mostly filamentous organisms that lack the green pigment chlorophyll and must obtain energy from the material on which they grow. Most fungi are saprobes, living entirely on dead or decaying organic matter. Fungi are the most important and most common cause of plant disease, with about 23 000 species known to infect plants, although it has been estimated that the actual number may be as high as 270 000 species. Some fungal pathogens can survive only by growing in their living host plants; these are termed obligate parasites or biotrophs. Examples include the rusts, smuts and powdery mildews. The majority of fungal pathogens are non-obligate or facultative parasites requiring a living host plant for only part of their life cycle. Fungi consist of individual living filaments called hyphae, which collectively form mycelium. As in other organisms, reproduction is an essential part of the life cycle of a fungus. Most fungi have the ability to reproduce both sexually or asexually. Usually, the asexual (imperfect, anamorphic) stage is the active pathogen and the sexual (perfect, teleomorphic) stage may occur only rarely. The sexual stage helps the fungus survive adverse, often seasonal conditions, and provides genetic diversity for the organism. The basic reproductive unit of fungi is the spore, which germinates to produce hyphae. Spores may result from both asexual and sexual reproduction and often a single fungal species may produce several different types of spores. The sexual stage of some fungi is unknown, or may not even exist, and so only the asexual stage is known. Formerly called Fungi Imperfecti, most are actually ascomycetes or basidiomycetes.

Spores develop in special structures called fruiting bodies, which provide some protection against desiccation and ultraviolet radiation. Often produced in enormous numbers, spores disperse by wind currents, rain, running water or insects. Thick-walled spores resistant to adverse conditions allow fungi to survive for long periods in the soil and on both living and dead plants.

Fungal mycelium may also form small, hard structures called sclerotia, which are important survival structures for many fungi.

Table 1.1 Some physiological disorders of perennial fruit crops

The true fungi are classified in their own kingdom, the Fungi. Now we know that the true fungi are more closely related to animals than to plants. The four major groups (phyla) of true fungi are the Ascomycota, Basidiomycota, Chytridimycota and Glomeromycota (includes traditional Zygomycota). The first two groups contain most of the plant pathogenic fungi.

Some important and widespread plant pathogens known as oomycetes were once considered part of the fungal kingdom. Their name derives from the round oospores produced by sexual reproduction and serve as thick-walled survival spores. Oomycetes are adapted to living in moist environments and produce asexual zoospores with flagella that allow them to swim. The best-known oomycetes are the plant pathogens Phytophthora, Pythium and the downy mildews. Structural, molecular and biochemical studies show that oomycetes are more closely related to diatoms, kelps and golden-brown algae. These organisms are now placed into the Kingdom Stramenopila.

The main characteristics of the plant pathogenic fungi and oomycetes are listed in Table 1.2.

Bacteria and phytoplasmas

Bacteria are tiny, single-celled organisms that lack chlorophyll. Cells reproduce rapidly by dividing into two (fission). Many bacteria produce extracellular polysaccharides that form a slime layer or capsule around the cell, which assists in plant infection. Members of the genera Agrobacterium, Clavibacter, Erwinia, Pseudomonas, Xanthomonas, Ralstonia and Xylella account for most species that cause diseases in plants.

Most bacterial plant pathogens are facultative parasites that adapt readily to different environments and can usually be cultured easily in the laboratory. Some bacteria that infect plants have never been cultured or only with great difficulty, using specialised media, and are described as fastidious bacteria. These include the xylem-limited Xylella fastidiosa, the cause of Pierce’s disease of grapevine, and the phloem-limited Spiroplasma citri, the cause of citrus stubborn disease.

Bacteria can survive for some time on plant surfaces as epiphytes, becoming active when conditions favour their development. The organisms can also survive in soil and crop debris, and in seeds and other plant parts. With the exception of Streptomyces, plant bacterial pathogens do not form spores.

Bacteria spread in infected seed and propagating material, water splash and wind-driven rain. Overhead irrigation is often an important means of spreading bacteria within a crop. Bacteria also spread with insects and with workers and machinery moving through a crop that is wet from rain or dew. Some species such as Xylella have specific insect vectors.

Table 1.2 Fungal and fungal-like pathogens

Bacteria infect plants through wounds or natural openings such as stomata and hydathodes. Warm, wet weather favours their development, whereas growth is often arrested by hot, dry conditions.

Phytoplasmas, previously called mycoplasma-like organisms, are similar to the true bacteria. They are of various shapes, including spherical, ovoid and filamentous, and lack a rigid cell wall. Phytoplasmas are spread by sap-sucking leafhoppers and planthoppers and infect only the phloem tissue of plants. Typical diseases caused by phytoplasmas are the ‘big bud’ and ‘little leaf’ diseases of many crop and weed plants.

Fig 1.9 Bacteria growing in culture. Right: a cell viewed through the microscope. Left: bacterial ooze from plant tissue.

Fig 1.10 A papaya tree infected with yellow crinkle showing distorted, new growth and phytoplasma in an infected cell.

Viruses and viroids

Viruses are extremely small, obligate parasites consisting of a nucleic acid core, which contains the genetic information necessary for replication, surrounded by a protective protein or lipoprotein coat. Viruses cannot reproduce outside a host cell and use the plants cell structures and components to produce more virus particles, to the detriment of the plant.

Plant viruses are spread by sap-sucking insects, in particular, aphids, leafhoppers, thrips and whiteflies. Transmission is an intricate biological process, often requiring the virus to form a close relationship with insect tissues before transmission is possible. Particular viruses are, almost always, spread by only one insect type. For example, aphids can transmit papaya ringspot virus but not tomato yellow leaf curl virus, which, in turn, is transmitted only by the silver leaf whitefly.

Viruses can be spread through vegetative propagation using infected plant parts (e.g. bulbs, corms, cuttings and tissue-cultured plantlets) and some are also transmitted through seed, contact or infected pollen.

A summary of some important plant viruses occurring in Australia is given in Table 1.3.

Symptoms caused by viruses are varied and several viruses infecting one crop type may have similar symptoms, requiring laboratory tests to determine which virus is present. Symptoms of virus infection are sometimes difficult to separate from those caused by chemical damage, insect feeding and nutrient imbalances.

Viroids are smaller than viruses and are among the smallest infectious agents known. A viroid consists of small, circular, infectious nucleic acid and is entirely dependent on the host for its reproduction. Viroids spread from plant to plant in infected propagation material and in infected sap carried on hands or on cutting and pruning instruments. Viroids occurring in Australia include avocado sun blotch, citrus exocortis, potato spindle tuber and pear blister canker.

Types of insect vector transmission

Non-persistent: the virus can be acquired from an infected plant, or transmitted to another plant in less than one minute; the virus is usually retained on the insect’s mouthparts for only a few hours.

Fig 1.11 Plant viruses viewed through an electron microscope. There are many shapes but isometric and flexuous rods are common.

Semi-persistent: the insect can be acquired after 15–30 minutes of feeding and the ability to transmit is retained for a few days.

Persistent or circulative transmission: the insect needs to feed for up to several hours on an infected plant to acquire virus, which then needs to circulate through the insect’s body to the salivary glands for transmission to occur. The insect may retain the ability to transmit for life.

In some instances, the virus may also replicate or reproduce in the insect during the circulative transmission process (propagative).

Nematodes

Nematodes are microscopic, non-segmented roundworms that belong to the animal kingdom. They occur in almost every soil and water habitat in the world and most nematode species feed on bacteria and organic matter. Nematodes attacking plants have a hollow, spear-like structure (stylet) near the mouth, used to pierce the wall of plant cells and ingest cell contents. Feeding often results in the formation of galls or lesions on roots or distortion of other plant parts. Nematodes move by swimming in films of water between soil particles or on plant surfaces. They spread by water, movement in infested soil and on contaminated machinery, and in infected planting material.

Table 1.3 Some plant viruses in Australia

Fig 1.12 The head of plant parasitic nematode showing the stylet, a spear-like structure. Below: root-knot nematode symptoms.

Symptoms of disease

The first step in the diagnosis of a disease is recognising the visible signs or symptoms in the plant. Symptoms are the results of disturbing one or more of the vital functions of the plant, such as:

•  uptake of water and minerals by roots (e.g. root rots)

•  translocation of carbohydrates, water and minerals (e.g. vascular wilts and cankers)

•  photosynthesis and respiration (e.g. leaf blights, leaf spots, mosaics)

•  reproduction (e.g. fruit rots, smuts)

Fig 1.13 The disease triangle.

Most diseases produce characteristic symptoms that often allow an accurate diagnosis or, alternatively, narrowed down to a few possibilities. Sometimes a definite diagnosis can be made only by using laboratory tests that allow the pathogen to be isolated from diseased tissue and identified. These tests should always be done if there is any doubt about the cause of a particular disease or if problems are being encountered during its control. Information that helps identify the cause of a disease includes the cultivar affected, location of affected plants in a field, weather conditions, crop sequences, and fertiliser and chemical treatments applied to the crop.

Disease development and management

All diseases caused by pathogens are the result of an interaction between the host plant, a pathogen, and environmental factors such as light, temperature and moisture. Environmental factors affect the development of both the host and the pathogen. This interaction is known as the ‘disease triangle’ and all components must be compatible for a disease to develop (Fig 1.13).

Disease-management strategies aim to favour the host plant’s growth and development while attacking vulnerable stages in the life cycle of the pathogen to prevent or restrict its development. The three key means of disease management are: exclude the pathogen; reduce inoculum levels of the pathogen; and protect the host plant.

Exclusion or eradication

•  Use of pathogen-tested seed and vegetative propagation material (e.g. budwood, cuttings and nursery trees produced under strict hygiene procedures).

•  Quarantine, including international, national and State quarantine zones, prevents movement of infected plant material. Illegal movement of material is a major threat to several of Australia’s horticultural industries.

•  The eradication of a pathogen before it becomes widespread. This is more likely to succeed if an incursion is detected soon after it has occurred and the pathogen cannot be dispersed by air-borne spores or insect vectors.

Reduction in inoculum levels

•  Crop rotation reduces pathogen populations during the growth of nonhost crops.

•  Incorporating organic manures into the soil increases the activity of microorganisms antagonistic to soil-borne plant pathogens.

•  Sanitation includes all activities aimed at eliminating or reducing the amount of inoculum present in a plant, field or packing house. Measures include removing diseased plant parts to reduce disease carryover by pruning, promptly destroying crop residues and alternative weed hosts, removing diseased fruit and thoroughly cleaning packing facilities and equipment.

•  Chemical and physical soil treatments, such as fumigation, solarisation and mulching reduce levels of soil-borne pathogens.

•  Heat treating planting material.

Protection of the host

•  Resistant varieties. Resistance to a pathogen either prevents infection or slows disease development.

•  Fungicide application. Protectant fungicides on seed or plant surfaces either kill fungal spores or prevent their germination. They are essential for managing foliar and fruit diseases and often used in combination with systemic products. The primary activity of systemic fungicides is as a protectant. A small proportion of the chemical is absorbed into the treated parts of plants where it has a curative or post-infection activity. Regular, routine use of systemic fungicides is not recommended, because resistant strains may develop, leading to reduced efficiency. Strategies have been developed that prevent the build-up of resistant strains.

•  Defence activators. These non-pesticide agents are applied before pathogen infection to activate the plants’ inherent resistance mechanisms. They may be of synthetic origin (e.g. a formulated chemical), or biological, (e.g. non-pathogenic microorganisms or their products). Defence activators are used in conjunction with traditional methods of disease-management.

•  Insecticide application. Insect vectors of some viruses are managed effectively with insecticides, but the mode of virus transmission is a crucial factor. Persistently transmitted viruses that require long feeding times by the vector may be controlled. However, spread of non-persistently transmitted viruses may actually be increased because vectors require feeding times of only seconds and in the short term, their activity may be increased after contact with insecticide.

Modern disease management aims to provide a combination of suitable methods to obtain effective, economically sound disease control with minimal risk to the environment.

Further information

General

Agrios GN (2005) Plant pathology (5th edn). Elsevier Academic Press: New York.

Annual Review of Phytopathology (ongoing series) http://www.annualreviews.org

Beattie BB, McG lasson WB & Wade NL (Eds) (1989) Post harvest diseases of horticultural produce: Volume 1 Temperate fruit. CSIRO Publications: Melbourne.

Brown JF & Ogle HJ (Eds) (1997) Plant pathogens and plant diseases. Rock vale Publications: Armidale.

Carefoot ER & Sprott GL (1967) Famine on the wind. Rand McNally & Co: Chicago.

Coates L, Cooke T, Persley D, Beattie B, Wade, N & Ridgway R (1995) (Eds) Postharvest diseases of horticultural produce: Volume 2 Tropical fruit . Department of Primary Industries: Brisbane, Queensland.

Dugan FW (2008) Fungi in the ancient world . APS Press: St Paul, Minnesota.

Hall IR, Brown GT & Z ambonelli A (2008) Taming the truffle: the history, lore and science of the ultimate mushroom. APS Press: St Paul, Minnesota.

Holliday P (1998) A dictionary of plant pathology (2nd edn). Cambridge University Press: Cambridge.

Horst KR (2001) Westcott’s plant disease handbook (6th ed). Kluwer Academic Publishers: Massachusetts.

Large EC (2003) The advance of the fungi . APS Press: St Paul, Minnesota.

Madden LV, Hughes G & van den Bosch F (2007) The study of plant disease epidemics. APS Press: St Paul, Minnesota.

Mariau D (Ed.) (2001) Diseases of tropical tree crops . CIRAD: Montpellier.

Persley DM (Ed.) (1993) Diseases of fruit crops . Department of Primary Industries: Brisbane, Queensland.

Ploetz RC (Ed.) (2003) Diseases of tropical fruit crops. C A B I Publishing: Wallingford.

Ploetz RC, Zentmyer, GA, Nishijima W, Rohrbach K & Ohr HD (Eds) (1994) Compendium of tropical fruit diseases . APS Press: St Paul, Minnesota.

Schumann G (1991) Plant diseases: their biology and social impact. APS Press: St Paul, Minnesota.

Schumann GL & D ’Arcy CJ (2006) Essential plant pathology. APS Press: St Paul, Minnesota.

Shivas RG & Hyde KD (1996) Biodiversity of plant pathogenic fungi in the tropics. In Biodiversity of Tropical Fungi . (Ed. KD Hyde) pp. 47 – 62. University of Hong Kong Press: Hong Kong.

Snowden AL (1990) A colour atlas of post-harvest diseases and disorders of fruits and vegetables: Volume 1 General introduction and fruits . Wolfe Scientific: London.

Waller JM, Lenne JM & Waller SJ (Eds) (2002) Plant pathologists pocketbook (3rd edn). CABI Publishing: Wallingford.

The American Phytopathological Society http://www.apsnet.or.

The Australasian Plant Pathology Society http://www.australasianplantpathologysociety.org.au

Plant Health Australia http://www.planthealthaustralia.com.a.

Bacterial diseases

Fahy PC & Persley GJ (1983) Plant bacterial diseases, a diagnostic guide. Academic Press: Australia.

Streten C & Gibb K (2006) Phytoplasma diseases in sub-tropical and tropical Australia. Australasian Plant Pathology 35, 129–146.

Fungi and fungal diseases

Dugan F (2006) The identification of fungi: an illustrated introduction. APS Press: St Paul, Minnesota.

Holliday P (1980) Fungus diseases of tropical crops. Cambridge University Press: Cambridge.

Kirk P M, Cannon PF, David JC & Staplers JA (Eds) (2001) Ainsworth and Bisby’s dictionary of the fungi (9th edn). CABI Publishing: Wallingford.

Nematode diseases

Bridge J & Starr J (2007) Plant nematodes of agricultural importance – a colour handbook . Manson Publishing: United Kingdom.

O’Brien PC & Stirling GR (1991) Plant nematology for practical agriculturalists (3rd edn). Department of Primary Industries: Brisbane, Queensland.

Shurtleff MC & Averre CW (2000) Diagnosing plant diseases caused by nematodes. APS Press: St Paul, Minnesota.

Stirling GR, Harrower K & Webb LE (Eds) (2008) Plantand soil nematology in Australia and New Zealand. Australasian Plant Pathology 37, 3 (special issue).

Virus diseases

Hadidi A, Khetarpal RK & Koganezawa H (Eds) (1998) Plant virus disease control . APS Press: St Paul, Minnesota.

Hull R (2002) Matthews’ plant virology (4th edn). Academic Press: New York.

Loebenstein G & Thottappilly G (Eds) (2003) Virus and virus-like diseases in major crops in developing countries . Kluwer Academic Publishers: London.

Walkey D (1991) Applied plant virology (2nd edn). Chapman and Hall:London.

2 COMMON DISEASES OF PERENNIAL FRUIT CROPS

   ANTHRACNOSE

Anthracnose refers to a group of fungal diseases characterised by the development of dark, sunken spots or lesions, often with a raised rim, on affected foliage, stems and fruit. Under warm, humid conditions, the surface of the lesion is covered by a sticky pink spore mass (conidia) produced in a fungal fruiting body termed an acervulus.

Fig 2.1 The distinct, concave shape of an anthracnose lesion on persimmon skin.

Fig 2.2 Cultures of Colletotrichum gloeosporioides and C. acutatum (inset).

Cause

Fungi belonging to several genera cause anthracnose diseases. These include Diplocarpon (black spot of roses), Elsinoe (anthracnose or black spot of grape) and, in particular, species of Colletotrichum . Anthracnose diseases caused by C. gloeosporioides are a major cause of loss in many tropical fruit crops.

Although the fungus has a teleomorph or sexual stage – Glomerella cingulata – this plays only a minor role in the disease cycle and it is C. gloeosporioides, the anamorph or asexual stage of the fungus, which causes anthracnose diseases.

Fig 2.3 A germinated spore of Colletotrichum gloeosporioides on papaya skin showing a germ tube and an appressorium. Inset: spores.

Fig 2.4 Disease cycle of avocado anthracnose caused by Colletotrichum gloeosporioides.

Symptoms and life cycle

Large numbers of spores (conidia) form in acervuli in lesions on foliage, branches, twigs and fruit. The fungus is most active during warm, wet conditions and the spores disperse by rain splash. Young growth on new leaf flushes is the most susceptible to infection. Fruits can be infected at any stage of development. Spores germinate on the fruit surface, producing an infection structure (an appressorium). This produces an infection peg, which penetrates the fruit skin. Here it remains dormant or quiescent until fruit begins to ripen. The fungus then resumes activity and rapidly invades the fruit, causing extensive decay.

Hosts

Colletotrichum gloeosporioides causes important problems, particularly as a fruit pathogen, on most tropical fruit crops including avocado, breadfruit, carambola, cherimoya, citrus, durian, fig, guava, lychee, mango, papaya, passionfruit and rambutan.

Management

Effective management of the pathogen includes orchard hygiene and good crop management, pre- and postharvest fungicide applications, postharvest temperature and ripening management, and resistant varieties, where available. Further details are provided in specific sections for each crop.

   ARMILLARIA ROOT ROT

Cause

The fungus Armillaria luteobubalina.

Importance and hosts

Armillaria luteobubalina is a native fungal pathogen distributed widely in Australian native forest and woodland areas. The fungus infects more than 200 species across more than 50 plant families, and most host species are endemic to Australia.

Losses are most likely to occur when orchards and vineyards are planted on land recently cleared of native vegetation susceptible to the fungus. Armillaria root rot may cause serious losses in apple, banana, citrus, custard apple, grape, macadamia, pear and stone fruit orchards.

Symptoms

Because Armillaria damages the root system, the symptoms above-ground are similar to those caused by other root-infecting pathogens. Plants slowly decline, showing leaf yellowing, reduced leaf growth and twig dieback. Armillaria first causes death of limbs and finally death of the plant. Gumming often occurs on the trunk and crown roots.

Diagnostic symptoms are the presence of cream-coloured fungal growth, sometimes fan shaped, just beneath the bark of the crown and large roots, and a strong mushroom smell. Black, cord-like threads of the fungus, commonly called rhizomorphs or ‘shoestrings’, often occur on the surface of the roots, forming a branched network that may extend 200 to 300 mm into the soil.

Fig 2.5 Advanced symptoms of Armillaria root rot in peach.

Fig 2.6 Root symptoms of Armillaria showing black strands or rhizomorphs, which grow around the external root surface and may help the disease spread.

Fig 2.7 Armillaria in bark. Sheets of white fungal growth have developed beneath the bark.

Fig 2.8 Honey-coloured mushrooms of Armillaria. These develop as clusters at the base of affected trees. Inset: underside, showing gills.

Fig 2.9 Disease cycle of Armillaria species.

Honey-coloured mushrooms with widely separated gills can form at the base of an affected tree during wet, cold weather in early winter.

Source of infection and spread

The fungus can survive in the soil for many years on stumps and roots. Infection occurs by root contact with infected plants or more commonly, by rhizomorphs present in the soil. Rhizomorphs on small, infected root pieces are distributed by flowing water or by moving cultivating implements from infested areas, which is the main source of infection. Rhizomorphs grow through the soil, attaching to young roots and infecting the outer root tissues. Mushrooms of Armillaria do not have a role in the infection cycle.

Armillaria is common in native vegetation where it can cause considerable damage. When native vegetation is cleared for orchards and vineyards, the fungus survives on decaying roots and stumps of infected plants. Introduced crops planted into these locations often sustain serious damage, particularly high-density, irrigated orchards where vigorous growth of the fungus occurs along the moist, irrigated rows. Abundant rhizomorphs then