Rice blast resistance-inducing mechanisms via effector recognition by NLR immune receptors.

• Project/Area Number: 18K05657
• Research Category: Grant-in-Aid for Scientific Research (C)
• Allocation Type: Multi-year Fund
• Section: 一般
• Review Section: Basic Section 39040:Plant protection science-related
• Research Institution: Tokyo University of Agriculture
• Principal Investigator: SAITOH Hiromasa 東京農業大学, 生命科学部, 教授 (20414336)
• Project Period (FY): 2018-04-01 – 2021-03-31
• Project Status: Completed (Fiscal Year 2020)
• Budget Amount: ¥4,420,000 (Direct Cost: ¥3,400,000、Indirect Cost: ¥1,020,000); Fiscal Year 2020: ¥1,170,000 (Direct Cost: ¥900,000、Indirect Cost: ¥270,000); Fiscal Year 2019: ¥1,560,000 (Direct Cost: ¥1,200,000、Indirect Cost: ¥360,000); Fiscal Year 2018: ¥1,690,000 (Direct Cost: ¥1,300,000、Indirect Cost: ¥390,000)
• Keywords: イネいもち病 / 細胞内免疫受容体 / 抵抗性遺伝子 / NLRs / エフェクター / ID / HMA / AVR / エフェクタータンパク質 / NLR受容体 / 免疫反応 / イネいもち病菌 / AVR-Pik / Pik-1 / HMA領域 / OsHIPP19 / NLRペア / Nicotiana benthamiana / 過敏感細胞死 / 植物免疫反応 / P-loop / MHDモチーフ / Magnaporthe oryzae / タンパク質－タンパク質相互作用 / NLR / integrated domain / 植物免疫 / 宿主－病原体相互作用 / NLRタンパク質

Outline of Final Research Achievements

Unconventional integrated domains in plant intracellular immune receptors of the nucleotide-binding leucine-rich repeat (NLRs) type can directly bind translocated effector proteins from pathogens and thereby initiate an immune response. The rice immune receptor pairs Pik-1/Pik-2 and RGA5/RGA4 both use integrated heavy metal-associated (HMA) domains to bind the effectors AVR-Pik and AVR-Pia, respectively, from rice blast fungal pathogen. Here, using plant cell death and pathogenicity assays and protein-protein interaction analyses, we show that the rice NLR pair Pikp-1/Pikp-2 triggers an immune response leading to partial disease resistance toward the “mis-matched” effector AVR-Pia in planta and that the Pikp-HMA domain binds AVR-Pia in vitro. The results of our work indicate that a single NLR immune receptor can bind multiple pathogen effectors via an integrated domain, insights that may enable engineering plant immune receptors with extended disease resistance profiles.

Academic Significance and Societal Importance of the Research Achievements

植物耐病性研究において、宿主NLRによる病原菌AVRエフェクターの認識は最も重要な研究課題の一つである。以前に研究代表者らは、病原菌AVRが植物NLRに組み込まれている特殊な領域（ID）に直接結合することを示し、AVR/NLR複合体結晶構造を世界で初めて明らかにした。本研究では、一つのNLRがIDを介して複数のエフェクターを認識することを見出し、それにより植物NLRのIDと病原体エフェクター相互作用の適応性が示唆された。この成果は多様なエフェクターを認識できる免疫受容体の人工設計の可能性を示すものであり、将来的に植物免疫受容体の機能の理解や病害抵抗性エンジニアリングへの展望を開くものと考える。

Research Products

• [Int'l Joint Research] John Innes Centre/The Sainsbury Laboratory(英国)
• [Int'l Joint Research] John Innes Centre/The Sainsbury Laboratory(英国)
• [Int'l Joint Research] John Innes Centre/The Sainsbury Laboratory(英国)
• [Journal Article] Multiple variants of the fungal effector AVR-Pik bind the HMA domain of the rice protein OsHIPP19, providing a foundation to engineer plant defense (2021)
  • Author(s): Maidment Josephine H.R.、Franceschetti Marina、Maqbool Abbas、Saitoh Hiromasa、Jantasuriyarat Chatchawan、Kamoun Sophien、Terauchi Ryohei、Banfield Mark J.
  • Journal Title: Journal of Biological Chemistry Volume: 296 Pages: 100371-100371
  • DOI: 10.1016/j.jbc.2021.100371
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] The rice NLR pair Pikp-1/Pikp-2 initiates cell death through receptor cooperation rather than negative regulation (2020)
  • Author(s): Zdrzaek Rafal、Kamoun Sophien、Terauchi Ryohei、Saitoh Hiromasa、Banfield Mark J.
  • Journal Title: PLOS ONE Volume: 15 Issue: 9 Pages: 1-10
  • DOI: 10.1371/journal.pone.0238616
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] RNA-Seq of in plants-expressed Magnaporthe oryzae genes identifies MoSVP as a highly expressed gene required for pathogenicity at the initial stage of infection (2019)
  • Author(s): Shimizu, M., Nakano, Y., Hirabuchi, A., Yoshino, K., Kobayashi, M., Yamamoto, K., Terauchi, R., Saitoh, H.
  • Journal Title: Molecular Plant Pathology Volume: 20 Issue: 12 Pages: 1682-1695
  • DOI: 10.1111/mpp.12869
  • Peer Reviewed / Open Access
• [Journal Article] Cross-reactivity of a rice NLR immune receptor to distinct effectors from the rice blast pathogen Magnaporthe oryzae provides partial disease resistance (2019)
  • Author(s): Varden, F.A., Saitoh, H., Yoshino, K., Franceschetti, M., Kamoun, S., Terauchi, R., Banfield, M.J.
  • Journal Title: Journal of Biological Chemistry Volume: 294 Issue: 35 Pages: 13006-13016
  • DOI: 10.1074/jbc.ra119.007730
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Cross-reactivity of a rice NLR immune receptor to distinct effectors from the blast pathogen leads to partial disease resistance (2019)
  • Author(s): Varden, F.A., Saitoh, H., Yoshino, K., Franceschetti, M., Kamoun, S., Terauchi, R., Banfield, M.J.
  • Journal Title: bioRxiv Volume: 530675 Pages: 1-19
  • DOI: 10.1101/530675
  • Open Access / Int'l Joint Research
• [Journal Article] Polymorphic residues in rice NLRs expand binding and response to effectors of the blast pathogen (2018)
  • Author(s): De la Concepcion, J.C., Franceschetti, M., Maqbool, A., Saitoh, H., Terauchi, R., Kamoun, S., Banfield, M.J.
  • Journal Title: Nature Plants Volume: 4 Issue: 8 Pages: 576-585
  • DOI: 10.1038/s41477-018-0194-x
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Lessons in Effector and NLR Biology of Plant-Microbe Systems (2018)
  • Author(s): Bialas Aleksandra、Zess Erin K.、De la Concepcion Juan Carlos、中略 Fujisaki Koki、Saitoh Hiromasa、Terauchi Ryohei、Banfield Mark J.、Kamoun Sophien
  • Journal Title: Molecular Plant-Microbe Interactions Volume: 31 Issue: 1 Pages: 34-45
  • DOI: 10.1094/mpmi-08-17-0196-fi
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Presentation] RNA-Seq of in planta-expressed Magnaporthe oryzae genes identifies MoSVP as a highly expressed gene required for pathogenicity at the initial stage of infection (2020)
  • Author(s): Hiromasa Saitoh
  • Organizer: The 6th International Conference on Agricultural and Biological Sciences (ABS 2020)
  • Int'l Joint Research / Invited
• [Presentation] イネいもち病菌感染組織のRNA-seq解析によって同定された新奇病原性遺伝子MoSVP (2019)
  • Author(s): 清水元樹、平渕亜紀子、小林光智衣、山本紘輔、寺内良平、齋藤宏昌
  • Organizer: 令和2年度日本植物病理学会大会
• [Presentation] エフェクター分泌によるいもち病菌の感染および抵抗性誘導機構 (2019)
  • Author(s): 齋藤宏昌
  • Organizer: 第３回 植物病理を紡ぐ会
  • Invited
• [Book] Applied Plant Biotechnology for Improving Resistance to Biotic Stress (2019)
  • Author(s): Terauchi, R., Fujisaki, K., Shimizu, M., Oikawa, K., Takeda, T., Takagi, H., Abe, A., Okuyama, Y., Yoshida, K., Saitoh, H.
  • Total Pages: 355
  • Publisher: Academic Press
  • ISBN: 9780128160305