Population structure and temporal maintenance of the multihost fungal pathogen Botrytis cinerea: causes and implications for disease management

Abstract

Summary Understanding the causes of population subdivision is of fundamental importance, as studying barriers to gene flow between populations may reveal key aspects of the process of adaptive divergence and, for pathogens, may help forecasting disease emergence and implementing sound management strategies. Here, we investigated population subdivision in the multihost fungus Botrytis cinerea based on comprehensive multiyear sampling on different hosts in three French regions. Analyses revealed a weak association between population structure and geography, but a clear differentiation according to the host plant of origin. This was consistent with adaptation to hosts, but the distribution of inferred genetic clusters and the frequency of admixed individuals indicated a lack of strict host specificity. Differentiation between individuals collected in the greenhouse (on Solanum) and outdoor (on Vitis and Rubus) was stronger than that observed between individuals from the two outdoor hosts, probably reflecting an additional isolating effect associated with the cropping system. Three genetic clusters coexisted on Vitis but did not persist over time. Linkage disequilibrium analysis indicated that outdoor populations were regularly recombining, whereas clonality was predominant in the greenhouse. Our findings open up new perspectives for disease control by managing plant debris in outdoor conditions and reinforcing prophylactic measures indoor.

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

“…cinerea proposed that host plant should be considered as a potent factor structuring populations of the pathogen, based on observed associations between patterns of population subdivision and the host of origin of isolates (see review and examples in Walker, ). In a previous (Walker et al ., ) and the present study, we confirmed that most of the genetic variation segregating in B . cinerea populations is explained by hosts, and that the effect of geography is weaker.…”

“…The case of bramble ‐ associated isolates is more puzzling, given that populations sampled from this host were differentiated from other populations in a previous study (Walker et al ., ) and partially in this one, but tests did not reveal higher aggressiveness of isolates collected from bramble, compared to isolates from other hosts. 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.…”

“…Patterns of pathogenicity were also consistent with generalism, as strains showed significant differences in quantitative pathogenicity on tomato hosts, but not on lettuce. Recently, we have found strong genetic differentiation between isolates collected in the greenhouse on tomato on the one hand and outdoor on bramble ( Rubus fruticosus ) and grapevine ( Vitis vinifera ) on the other hand, suggesting possible specialization of the pathogen to these hosts (Walker et al ., ). Here, we test the hypothesis of host specialization in B .…”

Botrytis pseudocinerea Is a Significant Pathogen of Several Crop Plants but Susceptible to Displacement by Fungicide-Resistant B. cinerea Strains

“…Sexual reproduction has been described for B. cinerea and B. pseudocinerea, but fruiting bodies (apothecia) are only rarely observed in nature. Nevertheless, population genetic studies (41) and the observation of similar frequencies of the mating type alleles MAT1-1 and MAT1-2 (42) have demonstrated that sexual recombination must occur regularly. The existence of both mating types in B. pseudocinerea isolates from the same fields confirms previous suggestions that this species performs sexual reproduction (13).…”

Strain effect on extracellular laccase activities fromBotrytis cinerea

“…The B05.10 strain is the Botrytis research community reference, whose genome is fully sequenced (Van Kan et al 2017). Strain VA612 was collected in 2005 in a vineyard in Hautvillers (Champagne, France) from the Pinot Noir cultivar (Walker et al 2015). Strain VA612 was collected in 2005 in a vineyard in Hautvillers (Champagne, France) from the Pinot Noir cultivar (Walker et al 2015).…”