A new family of structurally conserved fungal effectors displays epistatic interactions with plant resistance proteins

Noureddine Lazar (1) , Carl Mesarich (2) , Yohann Petit-Houdenot (3) , Nacera Talbi (3) , Ines Li de La Sierra-Gallay (1) , Emilie Zélie (1) , Karine Blondeau (1) , Jérome Gracy (4) , Bénédicte Ollivier (3) , Françoise Blaise (3) , Thierry Rouxel (3) , Marie-Hélène Balesdent (3) , Alexander Idnurm (5) , Herman van Tilbeurgh (1) , Isabellle Fudal (3)

1 I2BC - Institut de Biologie Intégrative de la Cellule
2 Laboratory of Molecular Plant Pathology, School of Agriculture and Environment, Massey University, Palmerston North, New Zealand
3 BIOGER - BIOlogie et GEstion des Risques en agriculture
4 CBS - Centre de Biologie Structurale [Montpellier]
5 University of Melbourne

Recognition of a pathogen avirulence (AVR) effector protein by a cognate plant resistance (R) protein triggers a set of immune responses that render the plant resistant. Pathogens can escape this so-called Effector-Triggered Immunity (ETI) by different mechanisms including the deletion or loss-of-function mutation of the AVR gene, the incorporation of point mutations that allow recognition to be evaded while maintaining virulence function, and the acquisition of new effectors that suppress AVR recognition. The Dothideomycete Leptosphaeria maculans , causal agent of oilseed rape stem canker, is one of the few fungal pathogens where suppression of ETI by an AVR effector has been demonstrated. Indeed, AvrLm4-7 suppresses Rlm3- and Rlm9-mediated resistance triggered by AvrLm3 and AvrLm5-9, respectively. The presence of AvrLm4-7 does not impede AvrLm3 and AvrLm5-9 expression, and the three AVR proteins do not appear to physically interact. To decipher the epistatic interaction between these L . maculans AVR effectors, we determined the crystal structure of AvrLm5-9 and obtained a 3D model of AvrLm3, based on the crystal structure of Ecp11-1, a homologous AVR effector candidate from Fulvia fulva . Despite a lack of sequence similarity, AvrLm5-9 and AvrLm3 are structural analogues of AvrLm4-7 (structure previously characterized). Structure-informed sequence database searches identified a larger number of putative structural analogues among L . maculans effector candidates, including the AVR effector AvrLmS-Lep2, all produced during the early stages of oilseed rape infection, as well as among effector candidates from other phytopathogenic fungi. These structural analogues are named LARS (for Leptosphaeria AviRulence and Suppressing) effectors. Remarkably, transformants of L . maculans expressing one of these structural analogues, Ecp11-1, triggered oilseed rape immunity in several genotypes carrying Rlm3 . Furthermore, this resistance could be suppressed by AvrLm4-7. These results suggest that Ecp11-1 shares a common activity with AvrLm3 within the host plant which is detected by Rlm3, or that the Ecp11-1 structure is sufficiently close to that of AvrLm3 to be recognized by Rlm3.

Mots clés: plant pathogenic fungi; avirulence; resistance; effector; structural family

Domaines: Biodiversité et Ecologie; Biologie moléculaire; Génomique, Transcriptomique et Protéomique [q-bio.GN]; Phytopathologie et phytopharmacie

Noureddine Lazar, Carl Mesarich, Yohann Petit-Houdenot, Nacera Talbi, Ines Li de La Sierra-Gallay, et al.. A new family of structurally conserved fungal effectors displays epistatic interactions with plant resistance proteins. PLoS Pathogens, 2022, 18 (7), pp.e1010664. ⟨10.1371/journal.ppat.1010664⟩. ⟨hal-03324327⟩