SPINDLY, a Negative Regulator of Gibberellic Acid Signaling, Is Involved in the Plant Abiotic Stress Response

Feng Qin,Feng Qin,Kazuko Yamaguchi-Shinozaki,Kazuko Yamaguchi-Shinozaki,Kyoko Morimoto,Kazuo Shinozaki,Kazuo Shinozaki,Yasunari Fujita,Yasunari Fujita,Junya Mizoi,Junya Mizoi,Ken-Suke Kodaira,Ken-Suke Kodaira,Lam-Son Phan Tran,Lam-Son Phan Tran,Kyonoshin Maruyama,Kyonoshin Maruyama

doi:10.1104/pp.111.187302

Feng Qin, Feng Qin + Show 15 more

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https://doi.org/10.1104/pp.111.187302

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Abstract

The SPINDLY (SPY) gene was first identified as a negative regulator of plant gibberellic acid (GA) signaling because mutation of this gene phenocopies plants treated with an overdose of bioactive GA and results in insensitivity to a GA inhibitor during seed germination. The SPY gene encodes an O-linked N-acetylglucosamine transferase that can modify the target protein and modulate the protein activity in cells. In this study, we describe the strong salt and drought tolerance phenotypes of Arabidopsis (Arabidopsis thaliana) spy-1 and spy-3 mutants in addition to their GA-related phenotypes. SPY gene expression was found to be drought stress inducible and slightly responsive to salt stress. Transcriptome analysis of spy-3 revealed that many GA-responsive genes were up-regulated, which could explain the GA-overdosed phenotype of spy-3. Some stress-inducible genes were found to be up-regulated in spy-3, such as genes encoding late embryogenesis abundant proteins, Responsive to Dehydration20, and AREB1-like transcription factor, which may confer stress tolerance on spy-3. CKX3, a cytokinin (CK) catabolism gene, was up-regulated in spy-3; this up-regulation indicates that the mutant possesses reduced CK signaling, which is consistent with a positive role for SPY in CK signaling. Moreover, overexpression of SPY in transgenics (SPY overexpressing [SPY-OX]) impaired plant drought stress tolerance, opposite to the phenotype of spy. The expression levels of several genes, such as DREB1E/DDF1 and SNH1/WIN1, were decreased in SPY-OX but increased in spy-3. Taken together, these data indicate that SPY plays a negative role in plant abiotic stress tolerance, probably by integrating environmental stress signals via GA and CK cross talk.

Highlights

The SPINDLY (SPY) gene was first identified as a negative regulator of plant gibberellic acid (GA) signaling because mutation of this gene phenocopies plants treated with an overdose of bioactive GA and results in insensitivity to a GA inhibitor during seed germination
Different components involved in these signal cascades have been identified, including genes involved in stress-induced transcriptional regulation and complex cross talk among different hormones at either the biosynthesis or action level (Fujita et al, 2006; Shinozaki and Yamaguchi-Shinozaki, 2007)
The SPY gene was first identified as a negative regulator in GA signaling, because the mutant displayed a set of GAtreated phenotypes, such as insensitivity to PAC during germination, early flowering, partial male sterility, and pale green color (Jacobsen and Olszewski, 1993; Jacobsen et al, 1996)

Summary

Present address

Loss-of-function mutations of DELLA proteins can rescue the dwarf phenotype of the GA biosynthesis mutant ga (Dill and Sun, 2001; King et al, 2001), indicating that DELLA proteins function as negative regulators in GA signaling. Another important component of GA signal transduction is an F-box protein, SLY1, that functions as a subunit of the E3 ubiquitin ligase complex SCFSLY1. Mutations in or knockout of the SPY gene leads to elevated GA responses, indicating that SPY functions as a negative regulator of GA signaling, whereas loss-of-function mutations of the SEC gene do not result in any obvious phenotypic changes in plants. The function of the SPY gene in plant abiotic stress response and plant hormone cross talk is discussed

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MATERIALS AND METHODS