Although a vineyard full of decaying grapes infected with noble rot is a blessing for sweet wine producers, the causal agent, Botrytis cinerea (gray mold), causes huge crop losses. Unlike most plant pathogens, individual isolates of the necrotrophic fungus can infect an extremely broad range of plants, including cereals, fruits, vegetables, and ornamentals. Host immune responses to such generalist pathogens are complex, involving multiple defense mechanisms and pathways with resistance to B. cinerea segregating genetically as a quantitative trait (Rowe and Kliebenstein, 2008). Little is known, however, about the intricacies of this host-pathogen genetic interaction.
A new study by Soltis et al. (2019) utilizes the tomato-B. cinerea pathosystem to measure how genetic diversity in both the host plant and a generalist pathogen interact to affect resistance/susceptibility, but on a previously unimaginable scale. They measured 1164 unique plant × pathogen genetic interactions by inoculating 97 genetically distinct B. cinerea isolates on six domesticated (Solanum lycopersicum) and six wild (Solanum pimpinellifolium) tomato accessions, totaling 3276 independent necrotic lesion areas.
Analysis of this high-power data set showed that lesion size was significantly and equally affected by tomato genotype and pathogen isolate. Surprisingly, wild and domestic tomato had a very similar susceptibility to the pathogen. This contrasts with the general domestication theory, which presupposes the domestic germplasm should be highly sensitive, while also exhibiting reduced genetic diversity, as exemplified by lower phenotypic variation. In this study, however, such phenotypic bottlenecks were not observed (see figure). Although these unexpected findings may be peculiar to tomato-B. cinerea, they do raise questions about the contribution of human domestication per se to the virulence of generalist pathogens in crops. Indeed, how applicable is the classic model of an evolutionary arms race between plant and pathogen to a generalist species?
B. cinerea × Tomato Diversity.
Leaves from six domesticated (S. lycopersicum) and six wild (S. pimpinellifolium) tomato accessions were inoculated with 97 B. cinerea isolates and lesion areas quantified. Tomato domestication decreased pathogen resistance, with 80% of isolates more virulent on domesticated tomato leaves. (Adapted from Soltis et al., [2019], Figures 1 and 3)
Specialist pathogens that infect a very narrow host range frequently have only a handful of large-effect qualitative loci controlling virulence. By contrast, genome-wide association mapping across the 97 isolates revealed that B. cinerea virulence on tomato is extremely polygenic, with numerous small-effect single-nucleotide polymorphisms (SNPs) linked to differential virulence. This is directly akin to the polygenic basis of resistance in the host plant (Zhang et al., 2017). Furthermore, most of the identified SNPs were only linked to a subset of tomato accessions, demonstrating that B. cinerea virulence is highly dependent on host genotype. These SNPs were associated with several hundred B. cinerea genes, including both previously characterized and novel virulence loci. Detailed examination of multiple SNPs within one of these, a pectinesterase gene, revealed that most were located in upstream regulatory regions. Subtleties in the transcriptional regulation of virulence-related proteins may therefore exist between individual B. cinerea isolates.
Taken together, these findings truly highlight the tenacity of B. cinerea as a plant pathogen. The high level of standing genetic diversity found in B. cinerea virulence loci, coupled with the ability of different isolates to intermate, means that the pathogen has at its disposal a cornucopia of beneficial alleles. This not only allows selection to customize virulence according to host genotype, but also enables rapid adaptation to any newly evolved plant defense mechanisms or host niches. Thus, breeding durable resistance to B. cinerea in the field is extremely challenging and will likely require a genome-wide appreciation of virulence/resistance at both the pathogen and host levels.
Footnotes
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References
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