Disease resistance: vertical, horizontal and gene-for-gene
How plants resist pathogens, Flor's gene-for-gene model, vertical and horizontal resistance, plant immunity, durable resistance, and deploying R genes.
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A resistant variety is the cheapest, safest and most widely used way to control plant disease: farmers simply sow the seed. But resistance is not a fixed property. A wheat variety resistant to stem rust can become susceptible within a few years when a new race of the fungus appears. Understanding why some resistance collapses quickly while other resistance lasts for decades is central to plant breeding and disease management.
The gene-for-gene concept, vertical and horizontal resistance, and durable resistance are classic exam topics in plant pathology and breeding.
Early discoveries
In 1905, R. H. Biffen at Cambridge showed that resistance of wheat to yellow rust was inherited as a single Mendelian recessive factor, one of the first applications of Mendel's laws to a practical trait. Breeders soon found that resistance bred in this way often failed when the pathogen changed. Two ideas, developed in the 1940s to 1960s, explained why.
The gene-for-gene concept
Working with flax and the flax rust fungus (Melampsora lini) in North Dakota from the 1940s, H. H. Flor found that for each gene conferring resistance in the host there is a corresponding gene for avirulence in the pathogen.
- Resistance occurs only when a host resistance (R) gene meets a matching pathogen avirulence (Avr) gene.
- Every other combination results in disease.
- If the pathogen loses or changes the Avr gene, often by a single mutation, it is no longer recognised: a new virulent race has appeared.
Modern molecular biology explained the model: Avr genes encode effectors, proteins the pathogen delivers into the plant to help infection, and most R genes encode intracellular NLR receptors that recognise those effectors, directly or by detecting their effects.
Plant immunity in two layers
J. D. G. Jones and J. L. Dangl's "zigzag" model (2006) describes two layers:
- Pattern-triggered immunity (PTI): receptors on the cell surface recognise conserved molecules of microbes, such as bacterial flagellin or fungal chitin, and trigger general defences. This stops most microbes.
- Effector-triggered immunity (ETI): successful pathogens deliver effectors that suppress PTI; plants with a matching R gene recognise an effector and trigger a strong response, often a hypersensitive response, rapid death of the infected cells that starves biotrophic pathogens.
The pathogen can evolve new effectors or lose recognised ones; the plant can evolve new R genes: an evolutionary arms race.
Vertical and horizontal resistance
J. E. Vanderplank (1963), a South African plant pathologist, distinguished:
| Vertical resistance | Horizontal resistance | |
|---|---|---|
| Also called | race-specific, qualitative, major-gene | race-non-specific, quantitative, partial |
| Genes | one or a few major R genes | many minor genes (polygenic) |
| Effect | often complete (immunity or hypersensitive response) | partial: slows disease |
| Against | only races carrying matching Avr genes | all races, more or less equally |
| Epidemic effect | reduces the initial inoculum (x0) that can infect | reduces the rate of spread (r) |
| Durability | often short, as new races appear | usually long-lasting |
Horizontal resistance works through components such as fewer successful infections, a longer latent period (time from infection to new spores), smaller lesions and less sporulation. Each slows the epidemic.
Boom-and-bust cycles
When a variety with a new vertical resistance gene is grown widely, it gives excellent control (boom) until a virulent race appears, multiplies on the vast area of a single resistance gene, and causes an epidemic (bust). Famous examples include:
- Many cycles of wheat stem and yellow rust resistance breakdown across the twentieth century.
- Ug99, a stem rust race found in Uganda in 1998–99 that overcame the widely used gene Sr31, and spread through East Africa and into the Middle East.
- Southern corn leaf blight in the United States in 1970, when most hybrid maize carried the same Texas male-sterile cytoplasm, which was susceptible to a new race of the fungus.
Durable resistance
R. Johnson (1984) defined durable resistance as resistance that remains effective after wide use for a long time in an environment favourable to the disease. Examples:
- Lr34/Yr18 in wheat, an adult-plant gene giving partial resistance to leaf rust, yellow rust and powdery mildew, used for over a century without breakdown.
- mlo in barley, a recessive mutation giving broad, long-lasting resistance to powdery mildew since the late 1970s.
- Many sources of quantitative resistance in potato, rice and other crops.
Deploying resistance wisely
- Gene pyramiding: combining several R genes in one variety, so a pathogen would need several simultaneous changes to overcome them; marker-assisted selection makes this practical.
- Combining major and minor genes: R genes plus a quantitative background.
- Multiline varieties and variety mixtures: mixtures of lines differing in R genes slow spread, as in some rice and barley systems.
- Regional gene deployment and gene rotation: different genes in different regions or seasons.
- Monitoring races so that breeders know which genes still work.
- Integrating resistance with other controls, so that resistance genes are not left to face the full pathogen population alone.
Predicting reactions with gene for gene
A wheat variety carries two resistance genes, R1 and R2. Three races of a rust fungus differ in their avirulence genes:
| Race | Avr1 | Avr2 | Reaction on the variety |
|---|---|---|---|
| A | present | present | resistant (both genes recognise it) |
| B | lost | present | resistant (R2 still recognises Avr2) |
| C | lost | lost | susceptible |
Race C must have lost two avirulence genes. If each loss occurs in about one of every million spores independently, a spore carrying both changes occurs in only about one in a million million (1012), which is why pyramided genes last longer. Once such a race exists, though, it can spread rapidly.
Key points
- Flor's gene-for-gene model: resistance only when a host R gene matches a pathogen Avr gene; losing Avr creates a virulent race.
- R genes often encode NLR receptors; Avr genes encode effectors; PTI and ETI are the two layers of plant immunity.
- Vanderplank: vertical resistance is race-specific and often complete; horizontal resistance is partial, polygenic and works against all races.
- Vertical resistance reduces initial inoculum; horizontal resistance slows the rate of spread.
- Boom-and-bust cycles follow wide use of single genes; Lr34 and mlo are classic durable resistances.
- Pyramiding, mixtures, gene deployment and monitoring prolong resistance.
What the exams ask
- School-leaving and entrance papers: why resistant varieties matter, and what vertical and horizontal resistance are.
- Degree and research-fellowship entrances: gene-for-gene theory with examples, vertical versus horizontal resistance, components of partial resistance, hypersensitive response, boom-and-bust cycles, and durable resistance.
- Research and breeding examinations: PTI and ETI, NLR genes and effectors, pyramiding with markers, multilines, and monitoring virulence.
Described in general terms: the kind of examination, not a past paper. Laisha never reproduces exam questions.
Questions people ask
Why do new races appear so quickly?
Pathogens such as rusts produce astronomical numbers of spores, so even rare mutations that remove an avirulence gene occur somewhere every season. Where one R gene is grown on millions of hectares, those mutants are strongly selected.
Is horizontal resistance always durable?
Usually more durable than single R genes, but some pathogens can slowly adapt to it as well. It also rarely gives complete control on its own.
Can gene editing help?
Yes. Editing susceptibility genes, such as mlo homologues in wheat, or rice genes exploited by bacterial blight, can give broad resistance, and editing allows new R genes to be combined faster.
Sources
- Flor, H. H. "Current status of the gene-for-gene concept." Annual Review of Phytopathology 9, 275–296 (1971).
- Vanderplank, J. E. Plant Diseases: Epidemics and Control. Academic Press, 1963.
- Jones, J. D. G. and Dangl, J. L. "The plant immune system." Nature 444, 323–329 (2006).
- Johnson, R. "A critical analysis of durable resistance." Annual Review of Phytopathology 22, 309–330 (1984).
- Krattinger, S. G. et al. "A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat." Science 323, 1360–1363 (2009).
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