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N-hydroxypipecolic acid triggers systemic acquired resistance through extracellular NAD(P)

Author

Listed:
  • Qi Li

    (University of Florida, P.O. Box 110700)

  • Mingxi Zhou

    (University of Florida, P.O. Box 110700
    University of Florida, P.O. Box 110690)

  • Shweta Chhajed

    (University of Florida, P.O. Box 118525)

  • Fahong Yu

    (University of Florida, P.O. Box 103622)

  • Sixue Chen

    (University of Mississippi)

  • Yanping Zhang

    (University of Florida, P.O. Box 103622)

  • Zhonglin Mou

    (University of Florida, P.O. Box 110700
    University of Florida, P.O. Box 110690)

Abstract

Systemic acquired resistance (SAR) is a long-lasting broad-spectrum plant defense mechanism induced in distal systemic tissues by mobile signals generated at the primary infection site. Despite the discoveries of multiple potential mobile signals, how these signals cooperate to trigger downstream SAR signaling is unknown. Here, we show that endogenous extracellular nicotinamide adenine dinucleotide (phosphate) [eNAD(P)] accumulates systemically upon pathogen infection and that both eNAD(P) and the lectin receptor kinase (LecRK), LecRK-VI.2, are required in systemic tissues for the establishment of SAR. Moreover, putative mobile signals, e.g., N-hydroxypipecolic acid (NHP), trigger de novo systemic eNAD(P) accumulation largely through the respiratory burst oxidase homolog RBOHF-produced reactive oxygen species (ROS). Importantly, NHP-induced systemic immunity mainly depends on ROS, eNAD(P), LecRK-VI.2, and BAK1, indicating that NHP induces SAR primarily through the ROS-eNAD(P)-LecRK-VI.2/BAK1 signaling pathway. Our results suggest that mobile signals converge on eNAD(P) in systemic tissues to trigger SAR through LecRK-VI.2.

Suggested Citation

  • Qi Li & Mingxi Zhou & Shweta Chhajed & Fahong Yu & Sixue Chen & Yanping Zhang & Zhonglin Mou, 2023. "N-hydroxypipecolic acid triggers systemic acquired resistance through extracellular NAD(P)," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42629-0
    DOI: 10.1038/s41467-023-42629-0
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    1. Marion Wenig & Andrea Ghirardo & Jennifer H. Sales & Elisabeth S. Pabst & Heiko H. Breitenbach & Felix Antritter & Baris Weber & Birgit Lange & Miriam Lenk & Robin K. Cameron & Joerg-Peter Schnitzler , 2019. "Systemic acquired resistance networks amplify airborne defense cues," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    2. Ana M. Maldonado & Peter Doerner & Richard A. Dixon & Chris J. Lamb & Robin K. Cameron, 2002. "A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis," Nature, Nature, vol. 419(6905), pages 399-403, September.
    3. Vladimir Shulaev & Paul Silverman & Ilya Raskin, 1997. "Correction: Airborne signalling by methyl salicylate in plant pathogen resistance," Nature, Nature, vol. 386(6626), pages 738-738, April.
    4. Jonathan D. G. Jones & Jeffery L. Dangl, 2006. "The plant immune system," Nature, Nature, vol. 444(7117), pages 323-329, November.
    5. Vladimir Shulaev & Paul Silverman & Ilya Raskin, 1997. "Airborne signalling by methyl salicylate in plant pathogen resistance," Nature, Nature, vol. 385(6618), pages 718-721, February.
    6. Chenggang Wang & Xiaoen Huang & Qi Li & Yanping Zhang & Jian-Liang Li & Zhonglin Mou, 2019. "Extracellular pyridine nucleotides trigger plant systemic immunity through a lectin receptor kinase/BAK1 complex," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
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