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Distinct domains of the AVRPM3A2/F2 avirulence protein from wheat powdery mildew are involved in immune receptor recognition and putative effector function

McNally, Kaitlin Elyse, Menardo, Fabrizio, Lüthi, Linda, Praz, Coraline Rosalie, Müller, Marion Claudia, Kunz, Lukas, Ben‐David, Roi, Chandrasekhar, Kottakota, Dinoor, Amos, Cowger, Christina, Meyers, Emily, Xue, Mingfeng, Zeng, Fangsong, Gong, Shuangjun, Yu, Dazhao, Bourras, Salim, Keller, Beat
Thenew phytologist 2018 v.218 no.2 pp. 681-695
Nicotiana benthamiana, alleles, genetic variation, hypersensitive response, immunologic receptors, mildews, powdery mildew, protein domains, sequence diversity, wheat
Recognition of the AVRPM3ᴬ²/F² avirulence protein from powdery mildew by the wheat PM3A/F immune receptor induces a hypersensitive response after co‐expression in Nicotiana benthamiana. The molecular determinants of this interaction and how they shape natural AvrPm3ᵃ²/ᶠ² allelic diversity are unknown. We sequenced the AvrPm3ᵃ²/ᶠ² gene in a worldwide collection of 272 mildew isolates. Using the natural polymorphisms of AvrPm3ᵃ²/ᶠ² as well as sequence information from related gene family members, we tested 85 single‐residue‐altered AVRPM3ᴬ²/F² variants with PM3A, PM3F and PM3Fᴸ⁴⁵⁶ᴾ/Y⁴⁵⁸ᴴ (modified for improved signaling) in Nicotiana benthamiana for effects on recognition. An intact AvrPm3ᵃ²/ᶠ² gene was found in all analyzed isolates and the protein variant recognized by PM3A/F occurred globally at high frequencies. Single‐residue alterations in AVRPM3ᴬ²/F² mostly disrupted, but occasionally enhanced, the recognition response by PM3A, PM3F and PM3Fᴸ⁴⁵⁶ᴾ/Y⁴⁵⁸ᴴ. Residues enhancing hypersensitive responses constituted a protein domain separate from both naturally occurring polymorphisms and positively selected residues of the gene family. These results demonstrate the utility of using gene family sequence diversity to screen residues for their role in recognition. This approach identified a putative interaction surface in AVRPM3ᴬ²/F² not polymorphic in natural alleles. We conclude that molecular mechanisms besides recognition drive AvrPm3ᵃ²/ᶠ² diversification.