Two folds, many faces: The Magnaporthe oryzae MAX effector AVR-Pia targets novel rice HMA domain-containing proteins
Abstract
Phytopathogenic fungi secrete effector proteins to promote virulence. The MAX ( Magnaporthe Avrs and ToxB-like) effectors form a structurally conserved family despite significant sequence diversity. AVR-Pia, a MAX effector from the rice blast fungus Magnaporthe oryzae, is recognised by the model rice nucleotide-binding leucine-rich repeat (NLR) receptor pair OsRGA4/OsRGA5 via direct binding to a heavy metal-associated (HMA) integrated domain (ID) in OsRGA5. While the structural basis of AVR-Pia recognition is well defined, the role of this effector in promoting virulence has remained elusive. Here, we reveal that AVR-Pia specifically interacts with four previously uncharacterised rice HMA domain-containing proteins, three HMA Plant Proteins (OsHPP09, OsHPP10 and OsHPP11), and one HMA Isoprenylated Plant Protein (OsHIPP21). AVR-Pia binds these proteins in vitro and in planta, engaging their HMA domains with differential affinities. Notably, AVR-Pia binds OsHPP09-HMA with considerably higher affinity than the HMA-ID of OsRGA5. By solving the crystal structure of the AVR-Pia/OsHPP09-HMA complex, we identified additional molecular contacts at the interface which underpin high affinity binding. Importantly, the H(I)PPs identified as AVR-Pia interactors are distinct from those bound by the MAX effectors AVR-Pik and Pwl2, underscoring target specialisation within the MAX effector family. Further, structural analyses of the AVR-Pia/OsHPP09-HMA complex revealed a markedly different interface compared to other MAX effector/H(I)PP complexes. Finally, structure-guided mutagenesis of OsHPP09 identified a single residue that is critical for AVR-Pia binding. This work provides structural insight into how distinct MAX effectors exploit HMA domain-containing proteins and offers a foundation towards targeted modification of HMA domains to disrupt effector binding and enhance cereal resistance to blast disease.
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BibTeX
@article{maidment2026folds,
title = {{Two folds, many faces: The Magnaporthe oryzae MAX effector AVR-Pia targets novel rice HMA domain-containing proteins}},
author = {Josephine Maidment and Svenja Saile and Aurélien Bocquet and Céline Thivolle and Léo Bourcet and Lisa-Fatimatou Planel and Muriel Gelin and Thomas Kroj and André Padilla and Karine de Guillen and Stella Cesari},
journal = {PLoS Pathogens},
year = {2026},
month = jul,
doi = {10.1371/journal.ppat.1014382},
url = {https://hal.inrae.fr/hal-05800307v1},
note = {CC BY 4.0},
}
RIS
TY - JOUR
TI - Two folds, many faces: The Magnaporthe oryzae MAX effector AVR-Pia targets novel rice HMA domain-containing proteins
AU - Josephine Maidment
AU - Svenja Saile
AU - Aurélien Bocquet
AU - Céline Thivolle
AU - Léo Bourcet
AU - Lisa-Fatimatou Planel
AU - Muriel Gelin
AU - Thomas Kroj
AU - André Padilla
AU - Karine de Guillen
AU - Stella Cesari
PY - 2026
DA - 2026/07/13
JO - PLoS Pathogens
DO - 10.1371/journal.ppat.1014382
UR - https://hal.inrae.fr/hal-05800307v1
AB - Phytopathogenic fungi secrete effector proteins to promote virulence. The MAX ( Magnaporthe Avrs and ToxB-like) effectors form a structurally conserved family despite significant sequence diversity. AVR-Pia, a MAX effector from the rice blast fungus Magnaporthe oryzae, is recognised by the model rice nucleotide-binding leucine-rich repeat (NLR) receptor pair OsRGA4/OsRGA5 via direct binding to a heavy metal-associated (HMA) integrated domain (ID) in OsRGA5. While the structural basis of AVR-Pia recognition is well defined, the role of this effector in promoting virulence has remained elusive. Here, we reveal that AVR-Pia specifically interacts with four previously uncharacterised rice HMA domain-containing proteins, three HMA Plant Proteins (OsHPP09, OsHPP10 and OsHPP11), and one HMA Isoprenylated Plant Protein (OsHIPP21). AVR-Pia binds these proteins in vitro and in planta, engaging their HMA domains with differential affinities. Notably, AVR-Pia binds OsHPP09-HMA with considerably higher affinity than the HMA-ID of OsRGA5. By solving the crystal structure of the AVR-Pia/OsHPP09-HMA complex, we identified additional molecular contacts at the interface which underpin high affinity binding. Importantly, the H(I)PPs identified as AVR-Pia interactors are distinct from those bound by the MAX effectors AVR-Pik and Pwl2, underscoring target specialisation within the MAX effector family. Further, structural analyses of the AVR-Pia/OsHPP09-HMA complex revealed a markedly different interface compared to other MAX effector/H(I)PP complexes. Finally, structure-guided mutagenesis of OsHPP09 identified a single residue that is critical for AVR-Pia binding. This work provides structural insight into how distinct MAX effectors exploit HMA domain-containing proteins and offers a foundation towards targeted modification of HMA domains to disrupt effector binding and enhance cereal resistance to blast disease.
SN - 1553-7366
SN - 1553-7374
ER -