21st Century Guidebook to Fungi, SECOND EDITION, by David Moore, Geoffrey D. Robson and Anthony P. J. Trinci

Table of Contents

1. Chapter 13: Ecosystem mycology: saprotrophs, and mutualisms between plants and fungi
2. Chapter 14: Fungi as pathogens of plants
   1. Fungal diseases and loss of world agricultural production
   2. A few examples of headline crop diseases
   3. The Rice Blast fungus Magnaporthe grisea (Ascomycota)
   4. Armillaria (Basidiomycota)
   5. Pathogens that produce haustoria (Ascomycota and Basidiomycota)
   6. Cercospora (Ascomycota)
   7. Ophiostoma (Ceratocystis) novo-ulmi (Dutch Elm disease or DED) (Ascomycota)
   8. Black stem rust (Puccinia graminis f. sp. tritici) threatens global wheat harvest
   9. Plant disease basics: the disease triangle
   10. Necrotrophic and biotrophic pathogens of plants
   11. The effects of pathogens on their hosts
   12. How pathogens attack plants
   13. Host penetration through stomatal openings
   14. Direct penetration of the host cell wall
   15. Enzymatic penetration of the host
   16. Pre-formed and induced defence mechanisms in plants
   17. Genetic variation in pathogens and their hosts: co-evolution of disease systems
   18. Chapter 14 References and further reading
   19. Buy a PDF of Chapter 14
3. Chapter 15: Fungi as symbionts and predators of animals

14.11 The effects of pathogens on their hosts

Identifying a disease is not always straightforward and requires careful consideration of all the symptoms (see Fig. 5). Once the nature, ideally the identity, of the pathogen, its host range and the environmental factors that favour disease symptoms have been established, appropriate control methods can be applied. These might include:

• Using disease resistant cultivars of the plant. Resistance can vary from ‘very resistant’ (the plant rarely, or never, gets the disease), ‘somewhat resistant’ (the plant usually does not get the disease, but might in a bad year), ‘somewhat susceptible’ (the plant often gets the disease) and ‘very susceptible’ (the plant almost always gets the disease and may be killed by it).
• Another plant-oriented disease-control method is to practice good sanitation, by removing infected leaves or pruning plants to increase air circulation.
• Similarly, as poorly nourished plants are more susceptible to disease, the water and nutrient availability of the soil can be controlled.
• Biological control methods offer sustainable approaches to disease management (Maloy, 2005; Massart & Jijakli, 2007) but are not always available or practicable, and ultimately chemical pesticides can be the final resort (Mares et al., 2006).

The symptoms observed in a diseased plant depend on the effect of the pathogen on the physiology of the plant. Photosynthesis is the essential function of plants and any pathogen that interferes with it will cause disease that may appear as chlorosis (yellowing) and necrosis (browning and death) of the leaves and stems. Even mild impairment of photosynthesis weakens the plant and increases susceptibility to other pests and pathogens.

Pathogens can affect translocation of water and nutrients through the vascular system of the host plant. This might be an effect on transpiration through the aerial parts of the plant or poor uptake of nutrients and water through diseased roots. Consequentially sluggish translocation through the vascular system will itself lead to wilting and chlorosis, and possibly necrosis, ‘upstream’ of the disease focus.

Most, if not all, infectious diseases increase respiration, this being a general reaction of the plant to most types of stress. The majority of the increase in respiration occurs in the infected host tissue and appears to be a basic response to injury. Consequences of increased oxygen uptake and enhanced activity of respiratory enzymes include: a slight increase in temperature, accumulation of metabolites around points of infection, and even an increase in dry weight of the host tissue.

Changes in plasma membrane and organelle membrane permeability are often the first detectable responses of plant cells to infection by pathogens, and this often leads to loss of electrolytes (calcium and potassium ions in particular). The permeability change is a response to toxins produced by the invading fungus.  For example, victorin, a cyclic peptide, is produced by Cochliobolus (which used to be called Helminthosporium) victoriae in oat leaves. Victorin binds to a membrane protein and changes membrane permeability, eventually causing chlorosis and necrotic stripes (‘leaf spots’) on the leaves. Victorin is the most phytotoxic and most selective compound known, being active against sensitive oats at 10 pg ml^-1 (13 pM), though it does not affect resistant oats or any other plant even at a million-times higher concentration; so, this is a host-specific (or host-selective) toxin (Tada et al., 2005; Gilbert & Wolpert, 2013). Other host-specific toxins are (Dyakov & Ozeretskovskaya, 2007):

• the HMT-toxin of Cochliobolus heterostrophus Race T, which causes leaf blight in maize. The name of the toxin derives from the old name of the pathogen, which used to be called Helminthosporium maydis Race T. This toxin increases membrane permeability of mitochondria to protons by reacting with unique site(s) on the inner mitochondrial membrane of Texas (T) cytoplasmic male-sterile maize.
• The HC-toxin produced by Race 1 of Cochliobolus carbonum that makes this race exceptionally virulent to certain genotypes of maize is a cyclic tetrapeptide. The toxin is active at 20 ng ml^-1 and inhibits maize histone deacetylase, consequently affecting histone acetylation, which is implicated in control of chromatin structure, cell cycle progression, and gene expression. The peptide is synthesised by HC-toxin synthase 1 (coded for by gene HTS1); when all HTS1 genes are disrupted the fungus is unable to produce HC-toxin and causes only small chlorotic flecks on the host. Non-specific resistance of maize to Race 1 is due to a detoxifying enzyme, HC-toxin reductase. Another fungus, Alternaria jesenskae, also produces HC-toxin and genomic sequencing shows that the proteins share 75-85% amino acid identity, and the genes for HC-toxin biosynthesis are duplicated in both fungi. The genomic organisation of the genes in the two fungi show a similar but not identical partial clustering arrangement. The genes may have moved by horizontal transfer between the two fungi (see Section 17.15), though they may have been present in a common ancestor and lost from other species of Alternaria and Cochliobolus (Wight et al., 2013).

Fusaric acid (5-butylpyridine-2-carboxylic acid) is a non-host-specific mycotoxin with low to moderate toxicity, which is consistently produced by Fusarium spp. pathogenic on several cereals, tomato, banana, and tobacco. Fusaric acid may cause many, but not all, of the disease symptoms; it is decarboxylated by tomato plants to the more toxic (100 times) 3-n-butyl-pyridone. Fusaric acid is mildly toxic to mice, but has potential value as a clinical pharmaceutical, because it reduces blood pressure by inhibiting dopamine hydroxylase (Deutch & Roth, 2014).

Pathogens also exert influence on transcription and translation in host cells. This is clearly aimed at changing the host metabolism in ways that benefit the pathogen. It may lead to a simple adaptation of plant secondary metabolism to enhance the production of chemicals that favour the fungus in some way; for example by attracting vectors to transport the fungus to other hosts (McLeod et al., 2005).  Equally interesting are cases of excess production of plant hormones that cause, for example, plant tissue proliferation. Changes in plant hormones can result from the influence of the pathogen on metabolism of the host or from production of a plant growth hormone or its analogue by the pathogen:

• Albugo candida (Oomycota, kingdom Chromista) causes increased indole acetic acid (IAA) production by infected plants of the genus Brassica (which contains more important agricultural and horticultural crops than any other genus: swedes, turnips, kohlrabi, cabbage, sprouts, cauliflower, broccoli, mustard seed, oilseed rape, among others). The disease is called white rust. IAA, the original plant auxin, controls plant cell elongation, apical dominance (prevents lateral bud formation), prevents abscission, and promotes continued growth of fruit tissues, cell division in vascular and cork cambium, and formation of lateral and adventitious roots.
• The gibberellin plant hormones were actually isolated in the 1930s from rice suffering the bakanae disease disease (Japanese for ‘foolish seedling’), which is caused by Gibberella fujikuroi (Fusarium moniliforme) (Ascomycota). The fungus itself produces a surplus of gibberellic acid, which acts as a growth hormone for the plant. It causes hypertrophy leading to etiolation and chlorosis, and the plants finally collapse and die. In the normal plant gibberellin growth regulators affect cell elongation in stems and leaves, seed germination, dormancy, flowering, enzyme induction, and leaf and fruit senescence. Bakanae still affects rice crops in Asia, Africa, and North America. Crop losses in 2003 were estimated at 20% to 50%; remember that almost half the human population of the world depends on rice (Slavica et al., 2017; and see the International Rice Research Institute’s Rice Knowledge Bank at http://www.knowledgebank.irri.org/).

Updated July, 2019