Genomic, Network, and Phylogenetic Analysis of the Oomycete Effector Arsenal

ABSTRACT The oomycetes are a class of microscopic, filamentous eukaryotes within the stramenopiles-alveolate-Rhizaria (SAR) supergroup and include ecologically significant animal and plant pathogens. Oomycetes secrete large arsenals of effector proteins that degrade host cell components, manipulate host immune responses, and induce necrosis, enabling parasitic colonization. This study investigated the expansion and evolution of effectors in 37 oomycete species in 4 oomycete orders, including Albuginales, Peronosporales, Pythiales, and Saprolegniales species. Our results highlight the large expansions of effector protein families, including glycoside hydrolases, pectinases, and necrosis-inducing proteins, in Phytophthora species. Species-specific expansions, including expansions of chitinases in Aphanomyces astaci and Pythium oligandrum, were detected. Novel effectors which may be involved in suppressing animal immune responses in Ap. astaci and Py. insidiosum were also identified. Type 2 necrosis-inducing proteins with an unusual phylogenetic history were also located in a number of oomycete species. We also investigated the "RxLR" effector complement of all 37 species and, as expected, observed large expansions in Phytophthora species numbers. Our results provide in-depth sequence information on all putative RxLR effectors from all 37 species. This work represents an up-to-date in silico catalogue of the effector arsenal of the oomycetes based on the 37 genomes currently available. IMPORTANCE The oomycetes are a class of microscopic, filamentous eukaryotes and include ecologically significant animal and plant pathogens. Oomycetes secrete large arsenals of effector proteins that degrade host cell components, manipulate host immune responses, and induce necrosis, enabling parasitic colonization. In this study, we catalogued the number and evolution of effectors in 37 oomycete species whose genomes have been completely sequenced. Large expansions of effector protein families in Phytophthora species, including glycoside hydrolases, pectinases, and necrosis-inducing proteins, were observed. Species-specific expansions were detected, including chitinases in Aphanomyces astaci and Pythium oligandrum. Novel effectors which may be involved in suppressing animal immune responses were identified in Ap. astaci and Py. oligandrum. Type 2 necrosis-inducing proteins with an unusual phylogenetic history were also located. This work represents an up-to-date in silico catalogue of the effector arsenal of the oomycetes based on the 37 genomes currently available.