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Suppression of Plant Immunity by Fungal Chitinase-like Effectors

2018; Elsevier BV; Volume: 28; Issue: 18 Linguagem: Inglês

10.1016/j.cub.2018.07.055

1879-0445

Gabriel L. Fiorin, Andrea Sánchez‐Vallet, Daniela Paula de Toledo Thomazella, Paula Favoretti Vital do Prado, Leandro Costa do Nascimento, Antônio Figueira, Bart P. H. J. Thomma, Gonçalo Amarante Guimarães Pereira, Paulo José Pereira Lima Teixeira,

Plant-Microbe Interactions and Immunity

Crop diseases caused by fungi constitute one of the most important problems in agriculture, posing a serious threat to food security [1Fisher M.C. Henk D.A. Briggs C.J. Brownstein J.S. Madoff L.C. McCraw S.L. Gurr S.J. Emerging fungal threats to animal, plant and ecosystem health.Nature. 2012; 484: 186-194Crossref PubMed Scopus (1931) Google Scholar]. To establish infection, phytopathogens interfere with plant immune responses [2Jones J.D. Dangl J.L. The plant immune system.Nature. 2006; 444: 323-329Crossref PubMed Scopus (8281) Google Scholar, 3Win J. Chaparro-Garcia A. Belhaj K. Saunders D.G. Yoshida K. Dong S. Schornack S. Zipfel C. Robatzek S. Hogenhout S.A. Kamoun S. Effector biology of plant-associated organisms: concepts and perspectives.Cold Spring Harb. Symp. Quant. Biol. 2012; 77: 235-247Crossref PubMed Scopus (243) Google Scholar]. However, strategies to promote virulence employed by fungal pathogens, especially non-model organisms, remain elusive [4Lo Presti L. Lanver D. Schweizer G. Tanaka S. Liang L. Tollot M. Zuccaro A. Reissmann S. Kahmann R. Fungal effectors and plant susceptibility.Annu. Rev. Plant Biol. 2015; 66: 513-545Crossref PubMed Scopus (583) Google Scholar], mainly because fungi are more complex and difficult to study when compared to the better-characterized bacterial pathogens. Equally incomplete is our understanding of the birth of microbial virulence effectors. Here, we show that the cacao pathogen Moniliophthora perniciosa evolved an enzymatically inactive chitinase (MpChi) that functions as a putative pathogenicity factor. MpChi is among the most highly expressed fungal genes during the biotrophic interaction with cacao and encodes a chitinase with mutations that abolish its enzymatic activity. Despite the lack of chitinolytic activity, MpChi retains substrate binding specificity and prevents chitin-triggered immunity by sequestering immunogenic chitin fragments. Remarkably, its sister species M. roreri encodes a second non-orthologous catalytically impaired chitinase with equivalent function. Thus, a class of conserved enzymes independently evolved as putative virulence factors in these fungi. In addition to unveiling a strategy of host immune suppression by fungal pathogens, our results demonstrate that the neofunctionalization of enzymes may be an evolutionary pathway for the rise of new virulence factors in fungi. We anticipate that analogous strategies are likely employed by other pathogens.