Powdery mildew effectors AVR A1 and BEC1016 target the ER J‐domain protein Hv ERdj3B required for immunity in barley

Li, Zizhang; Velásquez‐Zapata, Valeria; Elmore, J. Mitch; Li, Xuan; Xie, Wenjun; Deb, Sohini; Tian, Xiao; Banerjee, Sagnik; Jørgensen, Hans J. L.; Pedersen, Carsten; Wise, Roger P.; Thordal‐Christensen, Hans

doi:10.1111/mpp.13463

Powdery mildew effectors AVR _A1 and BEC1016 target the ER J‐domain protein Hv ERdj3B required for immunity in barley

Journal Article · Thu May 02 00:00:00 EDT 2024 · Molecular Plant Pathology

DOI:https://doi.org/10.1111/mpp.13463· OSTI ID:2345265

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Department of Plant and Environmental Sciences University of Copenhagen Frederiksberg C Denmark
Program in Bioinformatics &, Computational Biology Iowa State University Ames Iowa USA, Department of Plant Pathology, Entomology and Microbiology Iowa State University Ames Iowa USA
Department of Plant Pathology, Entomology and Microbiology Iowa State University Ames Iowa USA, USDA‐Agricultural Research Service, Corn Insects and Crop Genetics Research Unit Ames Iowa USA
Program in Bioinformatics &, Computational Biology Iowa State University Ames Iowa USA, Department of Statistics Iowa State University Ames Iowa USA
Program in Bioinformatics &, Computational Biology Iowa State University Ames Iowa USA, Department of Plant Pathology, Entomology and Microbiology Iowa State University Ames Iowa USA, USDA‐Agricultural Research Service, Corn Insects and Crop Genetics Research Unit Ames Iowa USA

AbstractThe barley powdery mildew fungus, Blumeria hordei (Bh), secretes hundreds of candidate secreted effector proteins (CSEPs) to facilitate pathogen infection and colonization. One of these, CSEP0008, is directly recognized by the barley nucleotide‐binding leucine‐rich‐repeat (NLR) receptor MLA1 and therefore is designated AVRA1. Here, we show that AVRA1 and the sequence‐unrelated Bh effector BEC1016 (CSEP0491) suppress immunity in barley. We used yeast two‐hybrid next‐generation interaction screens (Y2H‐NGIS), followed by binary Y2H and in planta protein–protein interactions studies, and identified a common barley target of AVRA1 and BEC1016, the endoplasmic reticulum (ER)‐localized J‐domain protein HvERdj3B. Silencing of this ER quality control (ERQC) protein increased Bh penetration. HvERdj3B is ER luminal, and we showed using split GFP that AVRA1 and BEC1016 translocate into the ER signal peptide‐independently. Overexpression of the two effectors impeded trafficking of a vacuolar marker through the ER; silencing of HvERdj3B also exhibited this same cellular phenotype, coinciding with the effectors targeting this ERQC component. Together, these results suggest that the barley innate immunity, preventing Bh entry into epidermal cells, requires ERQC. Here, the J‐domain protein HvERdj3B appears to be essential and can be regulated by AVRA1 and BEC1016. Plant disease resistance often occurs upon direct or indirect recognition of pathogen effectors by host NLR receptors. Previous work has shown that AVRA1 is directly recognized in the cytosol by the immune receptor MLA1. We speculate that the AVRA1 J‐domain target being inside the ER, where it is inapproachable by NLRs, has forced the plant to evolve this challenging direct recognition.

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Research Organization:: Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC)

Grant/Contract Number:: SC0014664

OSTI ID:: 2345265

Alternate ID(s):: OSTI ID: 2469796

Journal Information:: Molecular Plant Pathology, Journal Name: Molecular Plant Pathology Vol. 25 Journal Issue: 5; ISSN 1464-6722

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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Powdery mildew effectors AVR _A1 and BEC1016 target the ER J‐domain protein Hv ERdj3B required for immunity in barley