Fungal plant pathogens are major threats to food security worldwide. Sclerotinia sclerotiorum and Botrytis cinerea are closely related Ascomycete plant pathogens causing mold diseases on hundreds of plant species. There is no genetic source of complete plant resistance to these broad host range pathogens known to date. Instead, natural plant populations show a continuum of resistance levels controlled by multiple genes, a phenotype designated as quantitative disease resistance. Little is known about the molecular mechanisms controlling the interaction between plants and S. sclerotiorum and B. cinerea but significant advances were made on this topic in the last years. This minireview highlights a selection of nine themes that emerged in recent research reports on the molecular bases of plant-S. sclerotiorum and plant-B. cinerea interactions. On the fungal side, this includes progress on understanding the role of oxalic acid, on the study of fungal small secreted proteins. Next, we discuss the exchanges of small RNA between organisms and the control of cell death in plant and fungi during pathogenic interactions. Finally on the plant side, we highlight defense priming by mechanical signals, the characterization of plant Receptor-like proteins and the hormone abscisic acid in the response to B. cinerea and S. sclerotiorum, the role of plant general transcription machinery and plant small bioactive peptides. These represent nine trends we selected as remarkable in our understanding of fungal molecules causing disease and plant mechanisms associated with disease resistance to two devastating broad host range fungi.

Plant pathogens with a broad host range are able to infect plant lineages that diverged over 100 million years ago. They exert similar and recurring constraints on the evolution of unrelated plant populations. Plants generally respond with quantitative disease resistance (QDR), a form of immunity relying on complex genetic determinants. In most cases, the molecular determinants of QDR and how they evolve is unknown. Here we identify in Arabidopsis thaliana a gene mediating QDR against Sclerotinia sclerotiorum, agent of the white mold disease, and provide evidence of its convergent evolution in multiple plant species. Using genome wide association mapping in A. thaliana, we associated the gene encoding the POQR prolyl-oligopeptidase with QDR against S. sclerotiorum. Loss of this gene compromised QDR against S. sclerotiorum but not against a bacterial pathogen. Natural diversity analysis associated POQR sequence with QDR. Remarkably, the same amino acid changes occurred after independent duplications of POQR in ancestors of multiple plant species, including A. thaliana and tomato. Genome-scale expression analyses revealed that parallel divergence in gene expression upon S. sclerotiorum infection is a frequent pattern in genes, such as POQR, that duplicated both in A. thaliana and tomato. Our study identifies a previously uncharacterized gene mediating QDR against S. sclerotiorum. It shows that some QDR determinants are conserved in distantly related plants and have emerged through the repeated use of similar genetic polymorphisms at different evolutionary time scales.

Comparative transcriptome analyses reveal a major contribution of regulatory divergence in conserved genes during the response of Pentapetalae plants to the fungal pathogen Sclerotinia sclerotiorum.