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.

In tomato glasshouses, the population structure of airborne inoculum of Botrytis cinerea depends on the production of endogenous inoculum on diseased plants as well as on incoming exogenous inoculum. Both types of inocula may contribute differently to the development of epidemics. Two strains of B. cinerea were introduced in each of four separate compartments of an experimental tomato glasshouse. We monitored their impact on disease development and on the genetic diversity of B. cinerea populations using microsatellite markers. The naturally occurring airborne inoculum of B. cinerea displayed a high level of genetic diversity and was rapidly displaced in the glasshouse, as isolates with microsatellite profiles identical to the introduced strains amounted to 66% of the inoculum sampled from the air 14 days after inoculation and 91% of those collected from stem lesions 60 days after inoculation. This suggested an important role of secondary inoculum in disease development, which is compatible with the hypothesis of a polycyclic development of gray mold epidemics in tomato glasshouses. In controlled-environment tests on tomatoes, a wide range of aggressiveness levels was observed, both for isolates sampled from the air and from lesions on plants. Hypotheses are proposed to explain the negligible impact of naturally incoming isolates on the epidemics observed inside the four glasshouse compartments.

Botrytis cinerea, the causal agent of grey mould, is considered as a major burden on greenhouse tomato production. In heated greenhouses, where leaf pruning is a routine practice and microclimatic conditions are favourable for grey mould development, infections of the pruning wounds result in stem cankers that can rapidly kill the plants. Chemical control is not always sufficiently effective and growers face increasing demands for reducing their dependency on pesticides. Several techniques can be used for the removal of leaves. They differ mainly on the presence or absence and the size of petiole stubs remaining on the stems after pruning. In this study, leaf pruning techniques were compared in an experimental greenhouse and the results validated in four commercial greenhouses, in a variety of agronomic conditions and in various situations of inoculum pressure. All experiments clearly showed that a careful removal of the leaves without leaving any petiole stubs on the stems can significantly decrease the incidence of stem cankers even under high disease pressure. As up to 10-fold differences were observed, this suggests the possibility of improving pruning practices in tomato greenhouses by removing leaves systematically close to the stem. This environmentally-friendly cultural practice appears compatible for integration with other preventative methods for the objective of sustainable crop protection in greenhouse tomatoes. grey mould / Solanum lycopersicum / integrated pest management / sustainable crop protection

Although Botrytis cinerea is known for its ability to produce high amounts of spores on diseased plants, enabling it to complete rapidly numerous developmental cycles in favorable environments, population genetics studies of this fungus indicate enormous diversity and limited clonal spread. Here, we report an exception to this situation in the settings of commercial tomato greenhouses. The genotypic characterization of 712 isolates collected from the air and from diseased plants, following the development of gray mold epidemics in four greenhouses in southern France, revealed the presence of a few predominant genotypes in a background of highly diverse populations. The comparison of genotypic profiles for isolates collected in the air or on the plants was compatible with the hypothesis of an entry in the greenhouse of substantial amounts of inoculum from the outside environment but it also highlighted the importance of secondary inoculum produced within the crop. The overall results of this work suggest that sporulation could be an important target for disease management strategies in the greenhouse.

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