14.17 Genetic variation in pathogens and their hosts

The genes that determine the varied secreted fungal products essentially constitute the panel of fungal virulence genes, because their products contribute in some way to pathogenicity of the fungus. Equally, the plant genes that determine factors that combat the infection are effectively the plant resistance genes, because their products contribute in some way to combating the infection.

Ellis, Dodds & Lawrence, 2007 described the co-evolution of plant-pathogen disease systems as involving:

 ‘…a complex move-countermove scenario. In step 1, evolution of a plant pathogen from a non-pathogenic ancestor involves the acquisition of molecules called effectors that function to blunt host basal resistance responses that are induced by common microbe-specific molecules, known as pathogen associated molecular patterns (PAMPs). These molecules are recognised by host receptors as ‘non-self’ and trigger a low-level defence response. Step 2 is evolution by the host plant of ‘effector detectors’, more commonly known as resistance (R) proteins that specifically recognise pathogen effectors and then trigger strong host defences. When effector proteins are recognised by polymorphic host resistance proteins they are also called avirulence proteins. In step 3, the pathogen’s evolutionary countermove is envisaged to be more complex and can involve either modification of effectors to escape R protein recognition but retain virulence function, or loss and replacement of old effector repertoires with new ones. An additional flourish that can be added to step 3 by quintessential pathogens is the evolution of inhibitor proteins that either directly or indirectly block recognition of effectors by R proteins…’

Vertical or horizontal resistance categorises the responses of host plants to fungal diseases.

  • Vertical resistance is generally observed in annual crops which are not vegetatively propagated, and it usually depends on one or a very few pathogen-specific genes in the plant; if the resistance is overcome the crop fails.
  • Horizontal resistance (probably the most common in nature) is seen in perennial as well as vegetatively propagated annual crops, it is polygenic and tends to be broadly based and non‑specific.

Tolerance of a disease is defined as the ability to produce a crop in spite of infection. Defence of a plant against pathogens may therefore involve specific resistance conferred by one or a few major genes, which are effective against particular, genetically defined races of a pathogen, or may involve a general polygenic resistance, which is effective against a wide range of pathogens.

These are the defence strategies that the fungal pathogen must overcome to attack the host. We have to remember that we are dealing with fungal pathogens, so heterokaryosis and the parasexual cycle can contribute to the population genetics of the pathogen. Of course, the plant breeder and, increasingly, the molecular biologist and genetic engineer contribute to the population genetics of the host.

In the mid-twentieth century, combined studies on the inheritance of specific resistance in flax and the virulence factors of its fungal pathogen, flax rust, introduced the concept that host and parasite genes both played a role in the determination of whether or not a resistance reaction would be observed.

The concept is that the expression of resistance by the host is dominant while conversely the expression of non-virulence by the parasite is dominant (that is, virulence is a recessive character in the fungus) and, specifically, that each individual resistance gene in the host interacted with a corresponding single gene in the pathogen. This is the gene‑for‑gene concept.

In the simplest gene‑for‑gene interaction the reaction between each pair of resistance and susceptibility alleles in the host with its matching pair of virulence and avirulence alleles in the pathogen is fairly simple, but with several such interactions taking place, the overall relationship between a host and its pathogen is complex. Twenty-nine separate host resistance factors were identified in flax using classic breeding methods, each having a complementary virulence factor in flax rusts, and similar complementary major gene interactions between hosts and pathogens are known or suspected for more than 25 different host-pathogen combinations.

Table 6 illustrates the interaction between one gene locus in the host plant and one locus in the pathogen. The host alleles are symbolised R for resistance and r for susceptibility, while the corresponding pathogen alleles are symbolised V for avirulence and v for virulence.

Table 6. Single factor gene-for-gene interaction
Fungus pathogen genotype*
Host plant genotype*
RR
Rr
rr
V V
resistant
resistant
disease
V v
resistant
resistant
disease
v v
disease
disease
disease
*The host alleles are symbolised R for resistance and r for susceptibility, while the corresponding pathogen alleles are symbolised V for avirulence and v for virulence. From Moore & Novak Frazer, 200

A two-factor interaction is shown in Table 7, with the array simplified to distinct phenotypes using the dominance relationships. In such a multi-factor interaction, the host is resistant to the pathogen if a matching pair of (host) resistance and (pathogen) virulence alleles occurs at any one of the gene‑for‑gene loci. Gene‑for‑gene resistance often causes the hypersensitive response in the host plant to confine the pathogen and limit its proliferation.

Table 7. Two-factor gene-for-gene interaction
Fungus pathogen genotype*
Host plant genotype*
R1-, R2-
R1-, r2r2
r1r1, R2-
r1r1, r2r2
V1-, V2-
resistant
resistant
resistant
disease
V1-, v2v2
resistant
resistant
disease
disease
v1v1, V2-
resistant
disease
resistant
disease
v1v1, v2v2
disease
disease
disease
disease
*The host alleles of factors 1 and 2 are symbolised R for resistance and r for susceptibility, while the corresponding pathogen alleles are symbolised V for avirulence and v for virulence. To reduce the size of the table, homozygous and heterozygous dominants (e.g. R1R1 and R1r1) are combined (shown as, for example, R1-). From Moore & Novak Frazer, 2002.

The panels of gene-for‑gene interactions are interpreted as recognition reactions between the host and the pathogen. The avirulence alleles of the pathogen somehow label it ‘pathogen’; the resistance alleles of the host give the plant the ability to recognise and constrain the fungus, but it only needs one of the several potential recognition events to be successful to achieve resistance. For the fungus, future success as a pathogen depends on avoiding recognition; removing all of its labels so it can blend into the background. For the plant, future success depends on more and more sensitive surveillance. Gene‑for‑gene interactions lock the host and pathogen into a co‑evolutionary conflict between balanced polymorphisms.

Gene-for-gene interactions are also a target for applied genetics manipulation. Extensive use is made of major genes for resistance in disease control strategies for agricultural crops. The applied approach depends on the reproductive strategies of the pathogen. Pathogens with an exclusively asexual mode of reproduction (clonal pathogens) differ markedly from those with periodic cycles of sexual reproduction. In clonal populations the variety of different pathogen genotypes in the population will be restricted. In contrast, sexual reproduction produces a much wider diversity of pathogen genotypes, including new virulence combinations as a result of recombination.
 
Disease resistance genes used in breeding agricultural crops originally arose following co-evolution of the pathogen (which is now the crop disease) with the ancestors of what is now the crop plant. The gene‑for‑gene relationship, particularly in rusts and mildews, is also found in diseases of wild plants in nature. Indeed, wild species related to crops are the commonest sources of the genes used by plant breeders to develop race‑specific resistant cultivars of crops. Well-studied natural host pathogen systems include crown rust (Puccinia coronata f. sp. avenae) of wild oats (Avena fatua) and powdery mildew (Blumeria fischeri) of groundsel (Senecio vulgaris).

Studies of the molecular aspects of virulence have revealed many features contributing to pathogenicity. The only common theme is that no fungus depends on a single molecule for virulence; rather, virulence requires expression of several or even many genes.

Genetic studies of the interaction between the flax plant (Linum usitatissimum) and flax rust (Melampsora lini) have identified about 30 flax resistance (R) genes, and about 30 ‘corresponding’ flax rust avirulence (Avr) genes. In the interaction between barley (Hordeum vulgare) and barley powdery mildew (Blumeria graminis hordei), over 80 resistance genes have been identified. Major gene resistance to smut fungi occurs in wheat and barley and avirulence genes have been genetically mapped in the barley pathogen Ustilago hordei but no major gene resistance to smut has been identified in the maize genome (Ellis et al., 2007).

Research into the molecular genetics of fungal pathogenesis has been stimulated by the availability of increasingly sophisticated molecular analytical methods such as insertional mutagenesis (Brown & Holden, 1996) and whole genome, transcriptome, proteome, secretome and metabolome studies (Lorenz, 2002; Jeon et al., 2007; Talbot, 2007). Jeon et al. (2007) used Agrobacterium tumefaciens–mediated transformation (AMT; see Section 18.9) to create more than 20,000 mutant strains of the rice blast fungus Magnaporthe grisea (= Magnaporthe oryzae). This fungus infects plants by forming specialised infection structures, appressoria, that penetrate the rice cuticle, leading to tissue invasion and disease symptoms (see Section 14.3). The insertional mutants were grown in multiwell plates and analysed for growth, conidiation, appressorium development and pathogenicity in a high-throughput plant infection assay. The resulting data were stored in a relational database and mutants were selected for in-depth phenotyping and molecular characterisation of the mutation; 202 new pathogenicity genes were identified in this study.

Talbot (2007) described the work of Jeon et al. (2007) as an industrial-scale study for using insertional mutagenesis and whole genome sequence information on such a large scale. It is inevitable that by the time you read this similarly detailed and comprehensive information will be available about more of the fungi responsible for important crop diseases; probably at least some of the rusts, mildews, blasts, rots, eyespots and wilts that afflict so many of our most important crop plants.

Updated December 17, 2016