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Up-regulation of Arabidopsis thaliana NHL10 in the hypersensitive response to Cucumber mosaic virus infection and in senescing leaves is controlled by signalling pathways that differ in salicylate involvement

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Abstract

The Arabidopsis thaliana (L.) Heyhn. genome contains 45 genes that show substantial sequence similarity to the tobacco (Nicotiana tabacum L.) HIN1 (harpin-induced) gene and the Arabidopsis NDR1 (non-race-specific disease resistance) gene. Of these, the nine (NHL1 to NHL3, NHL8 to NHL12 and NHL22) that bear the highest identity to HIN1 were selected and their expression in various situations was examined. We found that NHL10 behaves like the tobacco HIN1 gene in that its transcripts are abundant in senescing leaves and they specifically accumulate during the hypersensitive response (HR) caused by exposure to an avirulent Cucumber mosaic virus (CMV) strain. Spermine, a novel inducer of tobacco PR (pathogenesis-related) genes, was found to up-regulate expression of NHL3, NHL10 and NDR1. Green fluorescent protein-fusion experiments indicated that NHL2 and NHL10, and possibly NDR1 are localized in the chloroplasts. Studies using Arabidopsis mutants defective in salicylic acid (SA), ethylene and jasmonic acid signalling revealed that the senescence-associated expression of NHL10 is mediated by a pathway that involves SA but that NHL10 expression during CMV-induced HR and spermine treatment is totally independent of SA.

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Abbreviations

aa :

Amino acid

CC :

Coiled-coil

CMV :

Cucumber mosaic virus

Col :

Columbia

ET :

Ethylene

GFP :

Green fluorescent protein

HR :

Hypersensitive response

HIN1 :

Harpin-induced gene

JA :

Jasmonic acid

LRR :

Leucine-rich repeat

NBS :

Nucleotide-binding site

NDR1 :

Non-race-specific disease resistance

NHL :

NDR1/HIN1-like

No :

Nössen

PR :

Pathogenesis-related

SA :

Salicylic acid

Spm :

Spermine

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Acknowledgements

We thank Drs. K. Natsuaki (Tokyo University of Agriculture), J.G. Turner (University of East Anglia) and F. Ausubel (Massachusetts General Hospital) for kindly providing CMV-B2, A. thaliana coi1 seeds and eds5 seeds, respectively. We also thank the Arabidopsis Biological Resource Center at Ohio State, USA, for providing the Arabidopsis Col., C24 and No wild-type seeds and etr1 and ein2 mutant seeds, and Drs. N.-H. Chua (Rockefeller University), H. Wada (University of Tokyo), Y. Niwa (University of Shizuoka) and T. Berberich (Goethe University) for providing various GFP plasmids and for critically reading the manuscript. This work was supported in part by a grant from the Research for the Future Program (JSPS-RFTF00L01604) of the Japan Society for the Promotion of Science and a Grant-in-aid for scientific research on priority areas (Molecular Mechanisms of Plant–Pathogenic Microbe Interactions—Toward Production of Disease Resistant Plants). The manuscript was edited by Dr. Patrick Hughes of The Bioedit.

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Authors and Affiliations

  1. Graduate School of Life Sciences, Tohoku University, 2-1-1 Katahira, Aoba-ku, Sendai, 980-8577, Miyagi, Japan

    Ming Shu Zheng, Atsushi Miyazaki & Tomonobu Kusano

  2. Graduate School of Agricultural Sciences, Tohoku University, 1-1 Tsutsumidori, Amamiyamachi, Aoba-ku, Sendai, 981-8555, Miyagi, Japan

    Hideki Takahashi

  3. RIKEN Plant Science Center, 1-7-22 Suehiro, Tsurumi, Yokohama, 230-0045, Kanagawa, Japan

    Hiroshi Hamamoto & Isamu Yamaguchi

  4. Molecular Cellular and Developmental Biology Program, Division of Biology, Kansas State University, 303 Ackert Hall, Manhattan, KS 66506-4901, USA

    Jyoti Shah

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  1. Ming Shu Zheng
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Correspondence to Tomonobu Kusano.

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Zheng, M.S., Takahashi, H., Miyazaki, A. et al. Up-regulation of Arabidopsis thaliana NHL10 in the hypersensitive response to Cucumber mosaic virus infection and in senescing leaves is controlled by signalling pathways that differ in salicylate involvement. Planta 218, 740–750 (2004). https://doi.org/10.1007/s00425-003-1169-2

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