The Arabidopsis Transcription Factor ANAC032 Represses Anthocyanin Biosynthesis in Response to High Sucrose and Oxidative and Abiotic Stresses

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Abstract

Production of anthocyanins is one of the adaptive responses employed by plants during stress conditions. During stress, anthocyanin biosynthesis is mainly regulated at the transcriptional level via a complex interplay between activators and repressors of anthocyanin biosynthesis genes. In this study, we investigated the role of a NAC transcription factor, ANAC032, in the regulation of anthocyanin biosynthesis during stress conditions. ANAC032 expression was found to be induced by exogenous sucrose as well as high light (HL) stress. Using biochemical, molecular and transgenic approaches, we show that ANAC032 represses anthocyanin biosynthesis in response to sucrose treatment, HL and oxidative stress. ANAC032 was found to negatively affect anthocyanin accumulation and the expression of anthocyanin biosynthesis ( DFR, ANS/LDOX) and positive regulatory ( TT8) genes as demonstrated in overexpression line (35S:ANAC032) compared to wild-type under HL stress. The chimeric repressor line (35S:ANAC032-SRDX) exhibited the opposite expression patterns for these genes. The negative impact of ANAC032 on the expression of DFR, ANS/LDOX and TT8 was found to be correlated with the altered expression of negative regulators of anthocyanin biosynthesis, AtMYBL2 and SPL9. In addition to this, ANAC032 also repressed the MeJA- and ABA-induced anthocyanin biosynthesis. As a result, transgenic lines overexpressing ANAC032 (35S:ANAC032) produced drastically reduced levels of anthocyanin pigment compared to wild-type when challenged with salinity stress. However, transgenic chimeric repressor lines (35S:ANAC032-SRDX) exhibited the opposite phenotype. Our results suggest that ANAC032 functions as a negative regulator of anthocyanin biosynthesis in Arabidopsis thaliana during stress conditions.

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Most cited references 51

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A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis.

Ruiqin Zhong, Chanhui Lee, Jianli Zhou … (2008)

SECONDARY WALL-ASSOCIATED NAC DOMAIN PROTEIN1 (SND1) is a master transcriptional switch activating the developmental program of secondary wall biosynthesis. Here, we demonstrate that a battery of SND1-regulated transcription factors is required for normal secondary wall biosynthesis in Arabidopsis thaliana. The expression of 11 SND1-regulated transcription factors, namely, SND2, SND3, MYB103, MYB85, MYB52, MYB54, MYB69, MYB42, MYB43, MYB20, and KNAT7 (a Knotted1-like homeodomain protein), was developmentally associated with cells undergoing secondary wall thickening. Of these, dominant repression of SND2, SND3, MYB103, MYB85, MYB52, MYB54, and KNAT7 significantly reduced secondary wall thickening in fiber cells. Overexpression of SND2, SND3, and MYB103 increased secondary wall thickening in fibers, and overexpression of MYB85 led to ectopic deposition of lignin in epidermal and cortical cells in stems. Furthermore, SND2, SND3, MYB103, MYB85, MYB52, and MYB54 were able to induce secondary wall biosynthetic genes. Direct target analysis using the estrogen-inducible system revealed that MYB46, SND3, MYB103, and KNAT7 were direct targets of SND1 and also of its close homologs, NST1, NST2, and vessel-specific VND6 and VND7. Together, these results demonstrate that a transcriptional network consisting of SND1 and its downstream targets is involved in regulating secondary wall biosynthesis in fibers and that NST1, NST2, VND6, and VND7 are functional homologs of SND1 that regulate the same downstream targets in different cell types.

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AtNAP, a NAC family transcription factor, has an important role in leaf senescence.

Yongfeng Guo, Susheng Gan (2006)

Leaf senescence is a unique developmental process that is characterized by massive programmed cell death and nutrient recycling. The underlying molecular regulatory mechanisms are not well understood. Here we report the functional analysis of AtNAP, a gene encoding a NAC family transcription factor. Expression of this gene is closely associated with the senescence process of Arabidopsis rosette leaves. Leaf senescence in two T-DNA insertion lines of this gene is significantly delayed. The T-DNA knockout plants are otherwise normal. The mutant phenotype can be restored to wild-type by the intact AtNAP, as well as by its homologs in rice and kidney bean plants that are also upregulated during leaf senescence. Furthermore, inducible overexpression of AtNAP causes precocious senescence. These data strongly suggest that AtNAP and its homologs play an important role in leaf senescence in Arabidopsis and possibly in other plant species.

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NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in woody tissues of Arabidopsis.

Nobutaka Mitsuda, Akira Iwase, Hiroyuki Yamamoto … (2007)

Wood is formed by the successive addition of secondary xylem, which consists of cells with a conspicuously thickened secondary wall composed mainly of lignin and cellulose. Several genes involved in lignin and cellulose biosynthesis have been characterized, but the factors that regulate the formation of secondary walls in woody tissues remain to be identified. In this study, we show that plant-specific transcription factors, designated NAC SECONDARY WALL THICKENING PROMOTING FACTOR1 (NST1) and NST3, are key regulators of the formation of secondary walls in woody tissues of Arabidopsis thaliana. In nst1-1 nst3-1 double knockout plants, the secondary wall thickenings in interfascicular fibers and secondary xylem, except for vascular vessels, were completely suppressed without affecting formation of cells destined to be woody tissues. Conversely, as shown previously for NST1, overexpression of NST3 induced ectopic secondary wall thickenings in various aboveground tissues. Furthermore, the expression of chimeric repressors derived from NST1 and NST3 suppressed secondary wall thickenings in the presumptive interfascicular fibers. Because putative orthologs of NST1 and NST3 are present in the genome of poplar, our results suggest that they are also key regulators of the formation of secondary walls in woody plants and could be used as a tool for the genetic engineering of wood and its derivatives.

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Author and article information

Contributors

Kashif Mahmood: URI : http://loop.frontiersin.org/people/268159/overview

Zhenhua Xu: URI : http://loop.frontiersin.org/people/362746/overview

Ashraf El-Kereamy: URI : http://loop.frontiersin.org/people/33713/overview

José A. Casaretto: URI : http://loop.frontiersin.org/people/289541/overview

Steven J. Rothstein: URI : http://loop.frontiersin.org/people/23646/overview

Journal

Journal ID (nlm-ta): Front Plant Sci

Journal ID (iso-abbrev): Front Plant Sci

Journal ID (publisher-id): Front. Plant Sci.

Title: Frontiers in Plant Science

Publisher: Frontiers Media S.A.

ISSN (Electronic): 1664-462X

Publication date (Electronic): 14 October 2016

Publication date Collection: 2016

Volume: 7

Electronic Location Identifier: 1548

Affiliations

[1]Department of Molecular and Cellular Biology, University of Guelph, Guelph ON, Canada

Author notes

Edited by: Jirong Huang,Shanghai Institutes for Biological Sciences (CAS), China

Reviewed by: Yongzhen Pang, Institute of Botany (CAS), China; Ai-Xia Cheng, Shandong University, China

*Correspondence: Steven J. Rothstein, rothstei@ 123456uoguelph.ca

^†Present address: Ashraf El-Kereamy, Division of Agriculture and Natural Resources, University of California, Cooperative Extension Kern County, Bakersfield, CA, USA

This article was submitted to Plant Physiology, a section of the journal Frontiers in Plant Science

Article

DOI: 10.3389/fpls.2016.01548

PMC ID: 5063858

PubMed ID: 27790239

SO-VID: 27a5d8fb-d92b-41fc-8a04-3a5536782cbf

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This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

History

Date received : 19 July 2016

Date accepted : 03 October 2016

Page count

Figures: 7, Tables: 0, Equations: 0, References: 72, Pages: 15, Words: 0

Funding

Funded by: Natural Sciences and Engineering Research Council of Canada 10.13039/501100000038

The Arabidopsis Transcription Factor ANAC032 Represses Anthocyanin Biosynthesis in Response to High Sucrose and Oxidative and Abiotic Stresses

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Arabidopsis genomics

Most cited references 51

A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis.

AtNAP, a NAC family transcription factor, has an important role in leaf senescence.

NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in woody tissues of Arabidopsis.

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