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

• Published in: PLoS pathogens Vol. 18; no. 7; p. e1010664
• Main Authors: Lazar, Noureddine, Mesarich, Carl H, Petit-Houdenot, Yohann, Talbi, Nacera, Li de la Sierra-Gallay, Ines, Zélie, Emilie, Blondeau, Karine, Gracy, Jérôme, Ollivier, Bénédicte, Blaise, Françoise, Rouxel, Thierry, Balesdent, Marie-Hélène, Idnurm, Alexander, van Tilbeurgh, Herman, Fudal, Isabelle
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 06-07-2022; Public Library of Science (PLoS)
• Subjects: AVR gene; Biochemistry, Molecular Biology; Biodiversity and Ecology; Biology and Life Sciences; Brassica napus; Canker; Cell culture; Crystal structure; Effectors; Environmental Sciences; Epistasis; Fungal Proteins - genetics; Fungal Proteins - metabolism; Fungi; Gene deletion; Genes; Genetic aspects; Genomics; Genotypes; Health aspects; Homology; Host plants; Immune response; Immunity; Life Sciences; Molecular biology; Mutation; Oilseeds; Pathogens; Peptides; Physical Sciences; Phytopathogenic fungi; Phytopathology and phytopharmacy; Plant Diseases - genetics; Plant Diseases - microbiology; Plant Proteins - metabolism; Plant resistance; Proteins; Rape plants; Rapeseed; Recognition; Research and Analysis Methods; Stem canker; Three dimensional models; Vegetal Biology; Virulence; Virulence - genetics; France; avirulence; effector; plant pathogenic fungi; structural family; resistance
• ISSN: 1553-7374; 1553-7366; 1553-7374
• DOI: 10.1371/journal.ppat.1010664

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.