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Grapevine downy mildew is an insurmountable disease that endangers grapevine production and the wine industry worldwide. The causal agent of the disease is the obligate biotrophic oomycete  Plasmopara viticola , for which the pathogenic mechanism remains largely unknown. Crinkling and necrosis proteins (CRN) are an ancient class of effectors utilized by pathogens, including oomycetes, that interfere with host plant defense reactions. In this study, 27  CRN-like  genes were cloned from the  P. viticola  isolate YL genome, hereafter referred to as  PvCRN  genes, and characterized  in silico  and  in planta. PvCRN  genes in ‘YL’ share high sequence identities with their ortholog genes in the other three previously sequenced  P. viticola  isolates. Sequence divergence among the genes in the  PvCRN  family indicates that different  PvCRN  genes have different roles. Phylogenetic analysis of the PvCRN and the CRN proteins encoded by genes in the  P. halstedii  genome suggests that various functions might have been acquired by the  CRN  superfamily through independent evolution of  Plasmopara  species. When transiently expressed in plant cells, the PvCRN protein family shows multiple subcellular localizations. None of the cloned PvCRN proteins induced hypersensitive response (HR)-like cell death on the downy mildew-resistant grapevine  Vitis riparia . This was in accordance with the result that most PvCRN proteins, except PvCRN11, failed to induce necrosis in  Nicotiana benthamiana . Pattern-triggered immunity (PTI) induced by INF1 was hampered by several PvCRN proteins. In addition, 15 PvCRN proteins prevented Bax-induced plant programmed cell death. Among the cell death-suppressing members, PvCRN17, PvCRN20, and PvCRN23 were found to promote the susceptibility of  N. benthamiana  to  Phytophthora capsici , which is a semi-biotrophic oomycete. Moreover, the nucleus-targeting member, PvCRN19, promoted the susceptibility of  N. benthamiana  to  P. capsici . Therefore, these PvCRN proteins were estimated to be virulent effectors involved in the pathogenicity of  P. viticola  YL. Collectively, this study provides comprehensive insight into the CRN effector repertoire of  P. viticola  YL, which will help further elucidate the molecular mechanisms of the pathogenesis of grapevine downy mildew.

Characterization of CRN-Like Genes From Plasmopara viticola: Searching for the Most Virulent Ones