Genomics analysis of Aphanomyces spp. identifies a new class of oomycete effector associated with host adaptation

Elodie Gaulin (1) , Michiel Pel (2) , Laurent Camborde (1) , Hélène San Clemente (2) , Sarah Courbier (2, 3) , Marie-Alexane Dupouy (2) , Julie Lengellé (2) , Marine Veyssière (2) , Aurélie Le Ru (4) , Frédéric Grandjean (5) , Richard Cordaux (5) , Bouziane Moumen (5) , Clément Gilbert (6) , Liliana Cano (7, 8) , Jean-Marc Aury (9) , Julie Guy (10) , Patrick Wincker (11) , Olivier Bouchez (12) , Christophe C. Klopp (13, 12) , Bernard Dumas (1)

1 Interactions Microbiennes dans la Rhizosphère et les Racines
2 LRSV - Laboratoire de Recherche en Sciences Végétales
3 Universiteit Utrecht / Utrecht University [Utrecht]
4 Plateforme TRI FR-AIB
5 EES - Écologie, Évolution, Symbiose [Équipe du laboratoire EBI Poitiers]
6 EGCE - Évolution, génomes, comportement et écologie
7 TSL - The Sainsbury Laboratory [Norwich]
8 UF - University of Florida [Gainesville]
9 LBGB - Laboratoire de Bioinformatique pour la Génomique et la Biodiversité
10 GENOSCOPE - Genoscope - Centre national de séquençage [Evry]
11 UMR 8030 - Génomique métabolique
12 GeT-PlaGe - Génome et Transcriptome - Plateforme Génomique
13 SIGENAE - Système d'Information des GENomes des Animaux d'Elevage

Background: Oomycetes are a group of filamentous eukaryotic microorganisms that have colonized all terrestrial and oceanic ecosystems, and they include prominent plant pathogens. The Aphanomyces genus is unique in its ability to infect both plant and animal species, and as such exemplifies oomycete versatility in adapting to different hosts and environments. Dissecting the underpinnings of oomycete diversity provides insights into their specificity and pathogenic mechanisms. Results: By carrying out genomic analyses of the plant pathogen A. euteiches and the crustacean pathogen A. astaci, we show that host specialization is correlated with specialized secretomes that are adapted to the deconstruction of the plant cell wall in A. euteiches and protein degradation in A. astaci. The A. euteiches genome is characterized by a large repertoire of small secreted protein (SSP)-encoding genes that are highly induced during plant infection, and are not detected in other oomycetes. Functional analysis revealed an SSP from A. euteiches containing a predicted nuclearlocalization signal which shuttles to the plant nucleus and increases plant susceptibility to infection. Conclusion: Collectively, our results show that Aphanomyces host adaptation is associated with evolution of specialized secretomes and identify SSPs as a new class of putative oomycete effectors.

Mots clés: CRAYFISH PLAGUE PATHOGEN; MEDICAGO-TRUNCATULA; PARTIAL RESISTANCE; ROOT-ROT; PHYTOPHTHORA-CAPSICI; UNITED-STATES; Aphanomyces; Oomycete; Effector; Secretome; Host adaptation; SSP; POTATO FAMINE PATHOGEN; DIFFERENTIAL EXPRESSION ANALYSIS

Mots clés: FILAMENTOUS PLANT-PATHOGENS; IMMUNE-RESPONSE

Domaines: Sciences du Vivant [q-bio]; Ecologie, Environnement

Elodie Gaulin, Michiel Pel, Laurent Camborde, Hélène San Clemente, Sarah Courbier, et al.. Genomics analysis of Aphanomyces spp. identifies a new class of oomycete effector associated with host adaptation. BMC Biology, 2018, 16 (1), ⟨10.1186/s12915-018-0508-5⟩. ⟨hal-01891875⟩