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Coupling calcium/calmodulin-mediated signaling and herbivore-induced plant response through calmodulin-binding transcription factor AtSR1/CAMTA3

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Abstract

Calcium/calmodulin (Ca2+/CaM) has long been considered a crucial component in wound signaling pathway. However, very few Ca2+/CaM-binding proteins have been identified which regulate plant responses to herbivore attack/wounding stress. We have reported earlier that a family of Ca2+/CaM-binding transcription factors designated as AtSRs (also known as AtCAMTAs) can respond differentially to wounding stress. Further studies revealed that AtSR1/CAMTA3 is a negative regulator of plant defense, and Ca2+/CaM-binding to AtSR1 is indispensable for the suppression of salicylic acid (SA) accumulation and disease resistance. Here we report that Ca2+/CaM-binding is also critical for AtSR1-mediated herbivore-induced wound response. Interestingly, atsr1 mutant plants are more susceptible to herbivore attack than wild-type plants. Complementation of atsr1 mutant plants by overexpressing wild-type AtSR1 protein can effectively restore plant resistance to herbivore attack. However, when mutants of AtSR1 with impaired CaM-binding ability were overexpressed in atsr1 mutant plants, plant resistance to herbivore attack was not restored, suggesting a key role for Ca2+/CaM-binding in wound signaling. Furthermore, it was observed that elevated SA levels in atsr1 mutant plants have a negative impact on both basal and induced biosynthesis of jasmonates (JA). These results revealed that Ca2+/CaM-mediated signaling regulates plant response to herbivore attack/wounding by modulating the SA-JA crosstalk through AtSR1.

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Abbreviations

CaM:

Calmodulin

CML:

CaM-like protein

CaMBD:

CaM-binding Domain

AtSR:

Arabidopsis thaliana signal responsive gene

CAMTA:

CaM-binding transcription activator

CDPK:

Calcium-dependent protein kinase

SA:

Salicylic acid

JA:

Jasmonate

JA-Ile:

Jasmonoyl-l-isoleucine

JR2:

Jasmonate-responsive 2

WR3:

Wound-responsive 3

VSP1:

Vegetative storage protein 1

NahG:

Salicylate hydroxylase

EDS1:

Enhanced disease susceptibility 1

EDS5:

Enhanced disease susceptibility 5

PAD4:

Phytoalexin deficient 4

ICS1:

Isochorismate synthase 1

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Acknowledgments

This research was supported by National Science Foundation grant no. 1021344 and the National Research Initiative Competitive Grant no. 2008-35100-04566 from the U.S. Department of Agriculture, National Institute of Food and Agriculture. We thank Linda L. Huckle of the U.S. Department of Agriculture, Agricultural Research Service, Northern Crop Science Laboratory, Fargo, ND for her help with SA, JA and JA-Ile quantification, and Lorie Mochel, Washington State University, for her help with preparing the manuscript.

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Authors and Affiliations

  1. Molecular Plant Science, Department of Horticulture, Washington State University, PO Box 646414, Pullman, WA, 99164-6414, USA

    Yongjian Qiu, Jing Xi, Liqun Du & B. W. Poovaiah

  2. College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, 310036, Zhejiang, People’s Republic of China

    Liqun Du

  3. U.S. Department of Agriculture, Agricultural Research Service, Northern Crop Science Laboratory, 1605 Albrecht Blvd. N, Fargo, ND, 58102-2675, USA

    Jeffrey C. Suttle

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  1. Yongjian Qiu
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  2. Jing Xi
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  3. Liqun Du
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  5. B. W. Poovaiah
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Correspondence to B. W. Poovaiah.

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Yongjian Qiu and Jing Xi contributed equally to this work.

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Qiu, Y., Xi, J., Du, L. et al. Coupling calcium/calmodulin-mediated signaling and herbivore-induced plant response through calmodulin-binding transcription factor AtSR1/CAMTA3. Plant Mol Biol 79, 89–99 (2012). https://doi.org/10.1007/s11103-012-9896-z

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