Avirulence proteins of Leptosphaeria maculans involved in suppressive interactions share a common structural pattern and are part of a larger family

Noureddine Lazar (1) , Carl H. Mesarich (2) , Yohann Petit-Houdenot (3) , Nacera Talbi (3) , Inès Li de la Sierra-Gallay (1) , Zelie Emilie (1) , Karine Blondeau (1) , Bénédicte Ollivier (3) , A. van De Wouw (4) , Angélique Gautier (3) , Balesdent Marie-Hélène (3) , Alexander Idnurm (4) , Herman van Tilbeurgh (1) , Isabelle Fudal (3)

1 I2BC - Institut de Biologie Intégrative de la Cellule
2 Massey University
3 BIOGER - BIOlogie et GEstion des Risques en agriculture
4 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 of the AVR gene, 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 the recognition of AvrLm3 and AvrLm5-9 by the R proteins Rlm3 and Rlm9, respectively (Plissonneau et al., 2016; Ghanbarnia et al., 2018). The presence of AvrLm4-7 does not impede AvrLm3 and AvrLm5-9 expression, and the three AVR do not physically interact. To decipher the antagonistic interaction between L. maculans AVR effectors, we determined the crystal structure of AvrLm5-9. Surprisingly, despite a lack of sequence similarity, AvrLm5-9 shares structural analogies with AvrLm4-7 (structure previously characterized by Blondeau et al., 2015). Structure-informed searches identified a larger number of putative structural analogues among L. maculans effector candidates (including AvrLm3), as well as among effector candidates from other phytopathogenic fungi (including ECP11-1 from Passalora fulva; Mesarich et al., 2018). We determined the crystal structure of ECP11-1, deduced the 3D structure of AvrLm3, and confirmed that they shared structural analogies with AvrLm4-7 and AvrLm5-9. Remarkably, transformants of L. maculans producing ECP11-1 triggered Rlm3-mediated immunity. Furthermore, this recognition could be suppressed by AvrLm4-7. These results suggest that ECP11-1 has the same function as AvrLm3, or that the ECP11-1 structure is sufficiently close to that of AvrLm3 to be recognized by Rlm3.

Mots clés: Avirulence; resistance; Plant pathogenic fungus; Effector

Domaines: Sciences du Vivant [q-bio]; Phytopathologie et phytopharmacie

Noureddine Lazar, Carl H. Mesarich, Yohann Petit-Houdenot, Nacera Talbi, Inès Li de la Sierra-Gallay, et al.. Avirulence proteins of Leptosphaeria maculans involved in suppressive interactions share a common structural pattern and are part of a larger family. European Conference of Fungal Genetics, Feb 2020, Rome, France. ⟨hal-04456400⟩