Quantitative interactions driveBotrytis cinereadisease outcome across the plant kingdom

Abstract

Host-pathogen interactions display a continuum of host ranges from extreme specialists limited to single hosts to broad generalists with hundreds of hosts. However, the existing models for host-pathogen dynamics are dominated by observations derived from specialist pathogens with qualitative virulence and tight host-pathogen co-evolution. It is not clear how appropriate the co-evolutionary model is in generalist pathogens that present quantitative virulence and broad host specificity. We infected 98 strains of the generalist necrotroph fungus Botrytis cinerea on 90 genotypes representing eight plant species with wild and domestic lines. We show that plant-Botrytis interactions don't fit traditional co-evolution models as Botrytis interacts with the Eudicot species individually, with little link to the relatedness between plant species or plant domestication. Furthermore, Botrytis host specificity and virulence have distinct polygenic architectures suggesting that the evolution of the Eudicot/Botrytis interactions relies on genome-wide allelic diversity rather than few major virulence loci.

The polyphagous plant pathogenic fungusBotrytis cinereaencompasses host‐specialized and generalist populations

“…Surprisingly, the difference in aggressiveness between tomato ‐ and grapevine ‐ collected strains was observed when inoculating on bramble, whereas it belongs to a botanical family, the Rosaceae, distant from Solanaceae and Vitaceae. However, plant susceptibility to Botrytis cinerea shows very little association to the evolutionary distances between the plant species (Caseys et al ., ). Henceforth, theses aggressiveness variations could be linked to species‐specific interactions.…”

Population Genomics Reveals Molecular Determinants of Specialization to Tomato in the Polyphagous Fungal PathogenBotrytis cinereain France

“…One noticeable exception is the population of B. cinerea collected from various hosts in California (Ma & Michailides 2005), for which whole-genome sequencing data and cross-infectivity assays revealed small differences in pathogenicity against different hosts and shallow population structure (Atwell et al . 2015; Caseys et al . 2020; Soltis et al .…”

“…in Chile, Tunisia, Hungary, United Kingdom; Walker 2016). One noticeable case is the population of B. cinerea collected from various hosts in California (Ma & Michailides 2005), for which whole-genome sequencing data did not detect any host-associated population structure despite differences in pathogenicity against different hosts (including tomato) in cross-infectivity assays (Atwell et al 2015; Caseys et al 2020; Soltis et al 2019). In France, previous research concluded that B. cinerea populations were differentiated according to some of their hosts, including tomato, grapevine and, to a lesser extent, bramble (Fournier & Giraud 2008; Walker et al 2015).…”

“…a set of populations specialized to different host species. Indeed, with the exception of California (Ma and Michailides, 2005; Caseys et al, 2020; Soltis et al, 2019; Atwell et al, 2015), studies conducted in multiple regions of the world reveal that populations were structured (reviewed in Walker 2016), and recognize the host as the factor with the highest explanatory power for population structure in B. cinerea , ahead of geography. In France, our previous work revealed population subdivision in B. cinerea , with genetic differentiation between field populations infecting tomato ( Solanum lycopersicum ) and grapevine ( Vitis vinifera ), respectively (Walker et al .…”

Tackling microbial threats in agriculture with integrative imaging and computational approaches

“…Using a global set of populations of the major wheat pathogen Z. tritici , a large set of loci associated with pathogen virulence and reproduction on different hosts were identified [38] , [162] . A large infection matrix of 98 strains of Botrytis cinerea and 90 plant genotypes of eight species revealed a highly polygenic architecture of pathogen virulence and host specialization [163] . Hence, simultaneously extending genetic diversity screens of the host and pathogen provides a powerful approach to comprehensively map the genetic architecture of virulence and resistance.…”