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Topic 1 : How do pathogen/pest populations respond to deployment of host resistance?

Topic 1 : How do pathogen/pest populations respond to deployment of host resistance?. Natural vs. human-managed systems Selective effects of qualitative resistance (R genes) How does evolution to virulence affect pathogens – is there a cost to virulence?

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Topic 1 : How do pathogen/pest populations respond to deployment of host resistance?

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  1. Topic 1: How do pathogen/pest populations respond to deployment of host resistance? • Natural vs. human-managed systems • Selective effects of qualitative resistance (R genes) • How does evolution to virulence affect pathogens – is there a cost to virulence? • Can durability of R genes be predicted? • Selective effects of quantitative (partial) resistance • Evolution of pathogen populations with host-selective toxins (HSTs) • What affects evolutionary potential of pathogen populations

  2. Pathogen populations evolve differently in human-influenced systems • R-gene breakdowns in agricultural systems tend to be dramatic and relatively complete • In artificial systems, humans constrain host evolution, deploy R genes in vast swaths • Pathogens evolve virulence • Humans deploy new R genes • Etc.

  3. Comomnly deployed wheat powdery mildew (Pm) resistance genes in NC % isolates virulent

  4. Less commonly deployed Pm genes in NC % isolates virulent

  5. How does evolution to virulence affect pathogens? • Is there a “cost to virulence” – a fitness cost to having a virulence gene? • Vanderplank, 1963 & 1968: • Releasing a new R gene causes directional selection: virulent pathotypes increase in frequency • When R gene is defeated, withdrawing it from production leads to “stabilizing selection”: pathogen races with unnecessary virulence genes are eliminated

  6. Types of natural selection Step 1 Step 2

  7. What is pathogen fitness? • The combined ability of an organism to survive and reproduce • Quantifiable • Reproductive rate • Infection efficiency • Aggressiveness (amount of disease caused) • Disease severity • AUDPC • Frequency of a strain relative to other strains can be used as an estimator of fitness

  8. Estimating fitness Genotype A: 10 lesions/lesion/day • Fitness (W) is a relative parameter -- expressed relative to the most fit genotype (with fitness = 1.0) • Relative fitness of B = WB: 0.9 Genotype B: 9 lesions/lesion/day • Selection coefficients (s) are also compared to estimate changes in fitness of isolates over time; they measure the intensity of natural selection on a genotype • Selection coefficient = the proportion by which the fitness of a genotype is less than that of the most fit • Selection coefficient (s) of most fit (most frequent strain) is set to 0, so its W = 1. Relative fitness of other isolates is 1 – s.

  9. For example:(Zhan et al, 2002, Local adaptation and effect of host genotype on the rate of pathogen evolution: an experimental test in a plant pathosystem. J. Evol. Biol. 15:637-647) • Question: Is reproductive fitness of a fungal isolate correlated with aggressiveness of that isolate? • Method: “Mark-release-recapture” -- co-inoculate multiple strains in equal proportions early in season, let them compete throughout season • Measure end-of-season frequencies; most fit strain is inferred to be highest-frequency strain • Calculate selection coefficient of Gi (the ith genotype): si = 1 - pit pj0 1/t • Where p = frequency, t = time, and 0 = inoculation time • 0 ≤ s ≤ 1. • Selection coefficient measures the intensity of selection on that genotype (larger s = higher negative selection against that genotype). Fitness = 1 – s. pjt pi0

  10. Madsen Stephens Fitness measured in field; aggressive-ness measured in greenhouse Was aggressive-ness correlated with fitness? Aggressiveness

  11. Is there a cost to virulence? • How dissociate effect of virulence gene from pathogen’s genetic background? • Near-isogenic lines (NILs) of pathogen (Leonard, 1977, Phytopathology 67:1273-1279; Klittich & Bronson,1986, Phytopathology 76:1294-1298) • Averaging over large isolate collection (Leonard, 1969, Phytopathology 59:1851-1857) • Crosses to dissociate virulence alleles from genetic background (Bronson & Ellingboe, 1986, Phytopathology 76:154-158) • Mutants (Prakash & Heather, 1986, Phytopathology 76:266-269) • Genetic transformation (Keller et al., 1990, Phytopathology 80:1166-1173) • Site-directed mutagenesis (Lindemann and Suslow, 1987, Phytopathology 77:882-886)

  12. Earl Xi et al. , 2003, Mycol. Res. 107:1485-1492 Fig. 1. Frequency of pathotypes E97-2 and H97-2 of Rhynchosporium secalis co-inoculated over 4 cycles on two barley cultivars: (a) ‘Earl,’ susceptible to E97-2, and (b) ‘Harrington,’ susceptible to both. E97-2 had complex virulence (to Earl, Harrington, and 5 more cvs). H97-2 had simple virulence (to Harrington and 1 other cv, not Earl). Harrington

  13. “E97-2, a pathotype with unnecessary virulence genes against a susceptible cultivar, had greater parasitic fitness compared with H97-2, a pathotype without unnecessary genes for virulence.” (Xi et al)

  14. Contrary evidence from malaria parasite • In 1993, Malawi became the first country in Africa to replace chloroquine with the combination of sulfadoxine and pyrimethamine for the treatment of malaria. • At that time, the clinical efficacy of chloroquine was less than 50%. • Molecular marker for chloroquine-resistant Plasmodium subsequently declined in prevalence and was undetectable by 2001 • Chloroquine once again effective in Malawi. • How did the frequency of the drug-resistant allele change in Plasmodium?

  15. Different loci impose different fitness costs Bahri et al, 2009. Tracking costs of virulence in natural populations of the wheat pathogen, Puccinia striiformis f. sp. tritici. BMC Evol. Bio. 9:26.

  16. So: if you remove a defeated R gene from commercial production, will the corresponding virulence in the pathogen population decline in frequency? • One would expect this to happen IF virulence carries a fitness penalty • It’s assumed by some: • E.g.,“Deployment of disease resistance genes by plant transformation – a ‘mix and match’ approach,” Pink and Puddephat, 1999, Trends in Plant Science, 4:71-75

  17. “A great advantage of the strategy is that it does not depend upon a supply of new resistance genes….Existing resistance genes can be recycled. For example, if a gene, or gene combination, is withdrawn because the frequency of the matching virulence increases in the pathogen population it can be re-introduced when thefrequency of the matching virulence allele(s) reduces.” (Pink & Puddephat)

  18. Best guess: • In general, if R gene is removed from use, frequency of virulence may decrease, but will likely remain sufficient to “flare up” again if R gene is redeployed • But magnitude of fitness penalty and length of time needed to restore fitness via compensatory mutations probably varies from virulence mutation to virulence mutation • So R genes may vary in durability (compared “head to head,” i.e., deployed on equal acreage, etc.)

  19. Fitness modifiers / compensatory mutations • Restoration of fitness may occur in the virulence gene itself (further mutations) • Or may occur indirectly in other genes determining aggressiveness / fitness • Insecticide resistance in Australian sheep blowfly (McKenzie and Purvis, 1984, Chromosomal localisation of fitness modifiers of diazinon resistance genotypes of Lucilia Cuprina, Heredity 53:625-634) • Streptomycin resistance in E. coli(Morell, 1997. Antibiotic resistance: road of no return. Science 278:575-576)

  20. Non-obligate pathogens: selection operates on all phases of life cycle Morris et al, 2009. Expanding the paradigms of plant pathogen life history and evolution of parasitic fitness beyond agricultural boundaries, PLoS Pathogens 5:1, www.plospathogens.org • “Dual-use” traits: have dual roles in environmental (e.g., rhizosphere or phyllosphere) and parasitic fitness • Toxins and toxin transport systems: e.g., efflux pumps in Botrytis cinerea confer resistance to antimicrobials from soil and plant microflora, and resistance to plant phytoalexin resveratrol • “Exaptation”: virulence can arise or shift via cooptation of phenotypes arising from natural selection unrelated to interaction with host plant • Environment – biotic and abiotic stresses • Streptomyces bacteria live in soil; apparently some have evolved saponinases, which can confer virulence, to counter saponins produced by plant roots • Saprophytic phase – e.g., Fusarium mycotoxins’ role against competitors • Basic housekeeping genes • Kinesins in Ascochyta rabiei, fungal pathogen of chickpea

  21. Is there some way to predict durability of particular R genes? • Leach et al, 2001. Pathogen fitness penalty as a predictor of durability of disease resistance genes, Annu. Rev. Phytopathology 39:187-224. • Reviews evidence related to hypothesis that durability of a resistance gene is a function of the amount of fitness penalty imposed on pathogen.

  22. Differences in durability of single-gene mediated resistance • Some single R genes have proven durable – • Monogenic resistance to Fusarium oxysporum in crucifers has lasted 90 yrs • Lr34 resistance to wheat leaf rust (Puccinia triticina) has lasted over 30 yrs • Xa3, Xa4 resistance in rice to Xanthomonas oryzae durable 10-15 yrs before virulence emerged, still has some effect.

  23. Some avr genes contribute to fitness • Bacteria: Some avr genes control both virulence and avirulence (both elicitors of HR and agents of pathogenicity) • Xanthomonas spp. (bacterial pathogens of pepper, tomato, citrus, etc.) • avrBs2 -> protein that’s secreted into plant cells; avrBs3 family -> ability to multiply intercellularly; lesion length • Pseudomonas syringae pv. tomato • avrRpt2 -> blocks activation of defense responses

  24. Fungal genes with dual function in virulence and avirulence - necrotrophs • Cladosporium fulvum (tomato pathogen) • Elicitors Avr4, Avr9: Avr4 protects pathogen against chitinase (van den Burg et al, 2006, MPMI, 19:1420–1430) • Rynchosporium secalis (barley scald) • NIP1 = AvrRs1: kills host cells, releases nutrients • Magnaporthe grisea (rice blast) • AVR-Pita -> protease expressed after pathogen is inside plant; fitness function unclear

  25. Avr genes and fitness (summary) • Not all avirulence genes make a measurable contribution to fitness • Mutations in Xanthomonad genes avrXa10 and avrBs3 did not cause measurable loss in aggressiveness • Some do, and relative magnitude of contribution to fitness may vary, even within highly similar gene family • avrXa mutants to virulence exhibit different fitnesses (discussed later) • Avr genes may contribute to different fitness attributes • Intercellular multiplication • Exit of intercellular spaces to leaf surface, etc.

  26. So if avr genes affect fitness differentially, mutations in them should differentially affect fitness, and R genes corresponding to them should be differentially durable. • Fitness penalty due to loss of avr function may be compensated by functional redundancy • There may be many copies (e.g., PWL genes in M. grisea, or avrBs3 genes in xanthomonads) some functioning as fitness but not recognition factors, or vice versa • Some of structural requirements for fitness and avirulence may be different – it may be possible to lose avirulence function without losing virulence function • AvrPto single amino-acid mutants lost avr but not vir function • In some cases, amount of avirulence protein can be down-regulated to avoid induction while maintaining virulence function • Phytophthora parasitica produces v low levels of elicitin

  27. Can we PREDICT which R genes will be more/less durable? Example #1: • Bai et al knocked out individual avr genes in X. oryzae (2000, MPMI 13:1322-1329). • Assayed isolates for fitness (also growth on IR24 leaves, not shown) • Avr gene with biggest effect on fitness predicted to correspond to R gene with greatest durability: which one? avrXa7 Tested in field with NILs, natural inoculum. Over 3 yrs, durability of Xa7 > Xa10.

  28. Example #2: • Laugé et al: screen for elicitors (avr products) that are important virulence factors, then search for resistance (1998, PNAS 95:9014-9018) • Knew avr4 and avr9 could be knocked out without detectable fitness penalty (Cladosporium fulvum on tomato) • Knew ECP2 was important virulence factor because ECP2 knockouts only weakly pathogenic • Identified 21 lines with resistance beyond known R genes, challenged them with ECP2: 4 had HR • If virulence and avirulence do not involve separate domains in ECP2, new R gene Cf-ECP2 expected to be durable

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