Roles of pepper bZIP protein CaDILZ1 and its interacting partner RING-type E3 ligase CaDSR1 in modulation of drought tolerance

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Abstract

Abscisic acid (ABA) is a plant hormone that plays a key role in the environmental stress response, especially the induction of ABA-responsive and stress-responsive genes and modulation of the stomatal aperture in response to drought stress. Here, we identified CaDILZ1 (Capsicum annuum Drought-Induced Leucine Zipper 1) belonging to subgroup D of the bZIP protein family; gene functions of this family in response to ABA and drought signaling still remain unknown. CaDILZ1 expression was significantly induced in pepper leaves after exposure to ABA, drought, and NaCl. The CaDILZ1 protein localized in the nucleus of plant cells. In response to drought stress, CaDILZ1-silenced pepper and CaDILZ1-overexpressing Arabidopsis plants exhibited drought-sensitive and drought-tolerant phenotypes, respectively, via altered ABA content, stomatal closure, and expression of ABA-responsive and drought-responsive marker genes. We isolated the RING finger protein CaDSR1 (Capsicum annuum Drought Sensitive RING finger protein 1), which interacted with CaDILZ1 in the nucleus. The CaDSR1 protein exhibited E3 ligase activity and promoted CaDILZ1 degradation via the 26S proteasome pathway. Under drought stress conditions, CaDSR1-silenced pepper and CaDSR1-overexpressing Arabidopsis plants exhibited contrasting phenotypes to those of CaDILZ1-silenced pepper and CaDILZ1-overexpressing Arabidopsis plants. Taken together, our data suggest that CaDSR1 and CaDILZ1 function in ABA-mediated drought stress signaling in pepper plants.

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Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells.

Z M Pei, Y Murata, G Benning … (2000)

Drought is a major threat to agricultural production. Plants synthesize the hormone abscisic acid (ABA) in response to drought, triggering a signalling cascade in guard cells that results in stomatal closure, thus reducing water loss. ABA triggers an increase in cytosolic calcium in guard cells ([Ca2+]cyt) that has been proposed to include Ca2+ influx across the plasma membrane. However, direct recordings of Ca2+ currents have been limited and the upstream activation mechanisms of plasma membrane Ca2+ channels remain unknown. Here we report activation of Ca2+-permeable channels in the plasma membrane of Arabidopsis guard cells by hydrogen peroxide. The H2O2-activated Ca2+ channels mediate both influx of Ca2+ in protoplasts and increases in [Ca2+]cyt in intact guard cells. ABA induces the production of H2O2 in guard cells. If H2O2 production is blocked, ABA-induced closure of stomata is inhibited. Moreover, activation of Ca2+ channels by H2O2 and ABA- and H2O2-induced stomatal closing are disrupted in the recessive ABA-insensitive mutant gca2. These data indicate that ABA-induced H2O2 production and the H2O2-activated Ca2+ channels are important mechanisms for ABA-induced stomatal closing.

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The ubiquitin-26S proteasome system at the nexus of plant biology.

Richard Vierstra (2009)

Plants, like other eukaryotes, rely on proteolysis to control the abundance of key regulatory proteins and enzymes. Strikingly, genome-wide studies have revealed that the ubiquitin-26S proteasome system (UPS) in particular is an exceedingly large and complex route for protein removal, occupying nearly 6% of the Arabidopsis thaliana proteome. But why is the UPS so pervasive in plants? Data accumulated over the past few years now show that it targets numerous intracellular regulators that have central roles in hormone signalling, the regulation of chromatin structure and transcription, tailoring morphogenesis, responses to environmental challenges, self recognition and battling pathogens.

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AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation.

Takuya Yoshida, Yasunari Fujita, Hiroko Sayama … (2010)

A myriad of drought stress-inducible genes have been reported, and many of these are activated by abscisic acid (ABA). In the promoter regions of such ABA-regulated genes, conserved cis-elements, designated ABA-responsive elements (ABREs), control gene expression via bZIP-type AREB/ABF transcription factors. Although all three members of the AREB/ABF subfamily, AREB1, AREB2, and ABF3, are upregulated by ABA and water stress, it remains unclear whether these are functional homologs. Here, we report that all three AREB/ABF transcription factors require ABA for full activation, can form hetero- or homodimers to function in nuclei, and can interact with SRK2D/SnRK2.2, an SnRK2 protein kinase that was identified as a regulator of AREB1. Along with the tissue-specific expression patterns of these genes and the subcellular localization of their encoded proteins, these findings clearly indicate that AREB1, AREB2, and ABF3 have largely overlapping functions. To elucidate the role of these AREB/ABF transcription factors, we generated an areb1 areb2 abf3 triple mutant. Large-scale transcriptome analysis, which showed that stress-responsive gene expression is remarkably impaired in the triple mutant, revealed novel AREB/ABF downstream genes in response to water stress, including many LEA class and group-Ab PP2C genes and transcription factors. The areb1 areb2 abf3 triple mutant is more resistant to ABA than are the other single and double mutants with respect to primary root growth, and it displays reduced drought tolerance. Thus, these results indicate that AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent gene expression for ABA signaling under conditions of water stress.

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Author and article information

Journal

Title: The Plant Journal

Abbreviated Title: Plant J

Publisher: Wiley

ISSN: 09607412

Publication date Created: October 2018

Publication date (Print): October 2018

Publication date (Electronic): September 05 2018

Volume: 96

Issue: 2

Pages: 452-467

Affiliations

[1 ]Department of Life Science (BK21 program); Chung-Ang University; Seoul 06974 Korea

Article

DOI: 10.1111/tpj.14046

PubMed ID: 30051516

SO-VID: de2be974-d9d5-4149-95f6-bf0367c2ac22

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Roles of pepper bZIP protein CaDILZ1 and its interacting partner RING-type E3 ligase CaDSR1 in modulation of drought tolerance

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Most cited references 60

Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells.

The ubiquitin-26S proteasome system at the nexus of plant biology.

AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation.

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