Elsevier

Plant Science

Volumes 188–189, June 2012, Pages 48-59
Plant Science

Transcriptional response of abscisic acid (ABA) metabolism and transport to cold and heat stress applied at the reproductive stage of development in Arabidopsis thaliana

https://doi.org/10.1016/j.plantsci.2012.03.001Get rights and content

Abstract

The phytohormone abscisic acid (ABA) plays an important role in developmental processes in addition to mediating plant adaptation to stress. In the current study, transcriptional response of 17 genes involved in ABA metabolism and transport has been examined in vegetative and reproductive organs exposed to cold and heat stress. Temperature stress activated numerous genes involved in ABA biosynthesis, catabolism and transport; however, several ABA biosynthesis genes (ABA1, ABA2, ABA4, AAO3, NCED3) were differentially expressed (up- or down-regulated) in an organ-specific manner. Key genes (CYP707As) involved in ABA catabolism responded differentially to temperature stress. Cold stress strongly activated ABA catabolism in all organs examined, whereas heat stress triggered more subtle activation and repression of select CYP707A genes. Genes involved in conjugation (UGT71B6), hydrolysis (AtBG1), and transport (ABCG25, ABCG40) of ABA or ABA glucose ester responded to temperature stress and displayed unique organ-specific expression patterns. Comparing the transcriptional response of vegetative and reproductive organs revealed ABA homeostasis is differentially regulated at the whole plant level. Taken together our findings indicate organs in close physical proximity undergo vastly different transcriptional programs in response to abiotic stress and developmental cues.

Highlights

Cold stress modify ABA biosynthesis and catabolism in Arabidopsis. ► Temperature stress also affects ABA transport and homeostasis. ► ABA metabolism and homeostasis differ between vegetative and reproductive organs. ► ABA metabolism and homeostasis are dynamically regulated during plant development.

Introduction

In plants the hormone abscisic acid (ABA) is often associated with inhibition of growth during abiotic or biotic stress conditions and also functions as a mediator of key phase transitions throughout the plant lifecycle [1], [2]. However, several lines of evidence indicate basal levels of ABA metabolism and signaling exert a promotive effect on plant growth, development and physiology. For example, ABA-deficient mutants of Arabidopsis thaliana and tobacco (Nicotiana plumbaginifolia) display vegetative and reproductive phenotypes (e.g. impaired shoot growth, unfertilized ovules, aborted embryos) that can be rescued through exogenous applications of ABA [3], [4], [5], [6]. Low concentrations of ABA also stimulate root growth and promote maintenance of stem cells [7], [8]. ABA accumulates within inflorescence and floral meristems at the reproductive stage of development and may function in regulating assimilate distribution within reproductive organs [9], [10]. Hormone profiling studies further revealed reproductive structures (flowers, siliques) accumulate substantial quantities of ABA and related metabolites [11], [12]. At present, very little is known as to how ABA promotes the growth of vegetative and reproductive organs in the absence of stress.

For economically important crop species ABA holds a key role in directing physiological processes that improve the stress tolerance of reproductive structures exposed to cold, heat and drought [13], [14], [15]. Molecular studies in rice (Oryza sativa) and wheat (Triticum aestivum) also revealed unique cellular and organ-level aspects of ABA homeostasis that distinguish stress-tolerant and stress-sensitive germplasm at the reproductive stage of development [16], [17]. From these studies, excessive ABA accumulation within reproductive structures was proposed to negatively correlate with abiotic stress tolerance. However, existing studies also provide evidence the beneficial or detrimental role(s) assigned to ABA accumulation during reproductive development are heavily dependent upon plant phenology and physiological context [9], [13], [18], [19].

During the course of studying reproductive phenotypes associated with ABA- and stress-responsive GRAM (for glucosyltransferases, Rab-like GTPase activators, and myotubularins) genes in Arabidopsis thaliana, we sought to determine whether rapidly growing reproductive organs (inflorescence meristems, developing siliques) displayed unique features with respect to ABA metabolism and transport when compared with adjacent vegetative tissues (cauline leaves) [20]. A large proportion of transcriptional studies examining ABA biosynthesis and catabolism have been conducted utilizing tissues associated with classical ABA responses such as seed dormancy and germination, seed maturation, developmental arrest of seedlings, or the response of vegetative tissues to abiotic stress [21]. However, the molecular understanding of ABA metabolism and transport at the whole plant level remains incomplete in spite of abundant physiological evidence indicating ABA is a mobile signaling molecule capable of facilitating communication at the cellular, organ, whole-plant and community levels [2], [22], [23].

Recent studies of ABA metabolism and homeostasis in the model plant Arabidopsis thaliana have led to identification of several novel proteins (UGT71B6, AtBG1, ABCG25, ABCG40) which modify endogenous ABA levels or mediate the active transport of ABA between plant cells (Fig. 1) [11], [24], [25], [26]. However, there is currently little or no molecular information describing how established pathways responsible for de novo ABA biosynthesis or catabolism are integrated with pathways mediating ABA transport or homeostasis. Understanding how ABA metabolism and transport are regulated at the whole plant level serves to enhance the understanding of ABA action in plant physiology [21]. In the present study, we analyzed the expression profile of Arabidopsis genes involved in ABA metabolism, transport and homeostasis in vegetative and reproductive organs at normal temperature and following cold and heat stress. Our results indicate key genes involved in ABA metabolism, transport and homeostasis are subject to a substantial degree of developmental regulation. Moreover, our findings provide evidence reproductive organs undergo contrasting transcriptional programs regulating ABA homeostasis in response to abiotic stress. Preceding studies revealed floral organs and early reproductive structures are particularly vulnerable to environmental stress (cold, heat, drought) and play a key role in the determination of crop yields [13], [14], [15]. In this regard, the current study offers new insight into how ABA metabolism and response operate during plant development and in response to abiotic stress. This information can in turn be utilized towards enhancing the abiotic stress tolerance of plant reproductive development.

Section snippets

Plant material and growth conditions

Arabidopsis thaliana (Columbia ecotype) seeds were surface sterilized (70% EtOH, 0.5% Triton) and placed on sterile agar plates containing half strength MS medium. Plates were stratified for 2 d at 4 °C in the darkness after which plates were placed under a light bar at a constant temperature of 22 ± 1.5 °C and providing 140 ± 20 μmol m−2 s−1 from cool white fluorescent lamps. Following germination, seedlings (4 true leaf stage) were transplanted in 8.5 cm2 square pots containing media (LA4 mix, aggregate

Cold and heat stress negatively impact reproductive development

In the current work Arabidopsis thaliana plants (Col-0) were gradually exposed to severe temperature extremes with the intention of negatively impacting reproductive development [28], [29]. At a macroscopic level cold and heat stress treatments caused visible changes in the pigmentation of inflorescence meristems, flowers and developing siliques (Fig. 2A–C). For plants exposed to heat stress, growth of stamen filaments was severely impaired preventing stamens from pollinating the stigma. At a

Discussion

In plants cellular ABA levels and ABA homeostasis are regulated through the coordinated action of numerous genes involved in ABA biosynthesis, catabolism and transport, alongside loci mediating the conjugation or hydrolysis of ABA and ABA-GE [2], [11], [21], [24]. In the current study, we examined how vegetative and reproductive organs of Arabidopsis thaliana differ with respect to transcriptional regulation of ABA metabolism and homeostasis in response to abiotic stress. To our knowledge this

Acknowledgements

This research was supported by Natural Sciences and Engineering Research Council (NSERC) grants awarded to CS and DS in addition to Canadian Wheat Board (CWB) and University of Manitoba (UMGF) scholarships awarded to KB. The authors would also like to thank Doug Durnin, Shiling Jiang and Sravan Kumar Jami for technical assistance and critical reading of the manuscript.

References (67)

  • A. Frey et al.

    Maternal synthesis of abscisic acid controls seed development and yield in Nicotiana plumbaginifolia

    Planta

    (2004)
  • M.E. LeNoble et al.

    Maintenance of shoot growth by endogenous ABA: genetic assessment of the involvement of ethylene suppression

    J. Exp. Bot.

    (2004)
  • J.M. Barrero et al.

    A mutational analysis of the ABA1 gene of Arabidopsis thaliana highlights the involvement of ABA in vegetative development

    J. Exp. Bot.

    (2005)
  • H.M. Zhang et al.

    ABA promotes quiescence of the quiescent centre and suppresses stem cell differentiation in the Arabidopsis primary root meristem

    Plant J.

    (2010)
  • G.L. Yarrow et al.

    Effect of shading individual soybean reproductive structures on their abscisic acid content, metabolism, and partitioning

    Plant Physiol.

    (1988)
  • Y.B. Peng et al.

    Preferential localization of abscisic acid in primordial and nursing cells of reproductive organs of Arabidopsis and cucumber

    New Phytol.

    (2006)
  • D.M. Priest et al.

    Use of the glucosyltransferase UGT71B6 to disturb abscisic acid homeostasis in Arabidopsis thaliana

    Plant J.

    (2006)
  • Y. Kanno et al.

    Comprehensive hormone profiling in developing Arabidopsis seeds: examination of the site of ABA biosynthesis, ABA transport and hormone interactions

    Plant Cell Physiol.

    (2010)
  • F. Liu et al.

    A review of drought adaptation in crop plants: changes in vegetative and reproductive physiology induced by ABA-based chemical signals

    Aust. J. Agric. Res.

    (2005)
  • B. Barnabás et al.

    The effect of drought and heat stress on reproductive processes in cereals

    Plant Cell Environ.

    (2008)
  • S.N. Oliver et al.

    ABA regulates apoplastic sugar transport and is a potential for cold-induced pollen sterility in rice

    Plant Cell Physiol.

    (2007)
  • X.M. Ji et al.

    Control of abscisic acid catabolism and abscisic acid homeostasis is important for reproductive stage stress tolerance in cereals

    Plant Physiol.

    (2011)
  • J.C. Yang et al.

    Involvement of abscisic acid and ethylene in the responses of rice grains to water stress during filling

    Plant Cell Environ.

    (2004)
  • L.M.C. Nitsch et al.

    Abscisic acid levels in tomato ovaries are regulated by LeNCED1 and SlCYP707A1

    Planta

    (2009)
  • E. Nambara et al.

    Abscisic acid biosynthesis and catabolism

    Annu. Rev. Plant Physiol. Mol. Biol.

    (2005)
  • J.A.D. Zeevaart et al.

    Metabolism and physiology of abscisic acid

    Annu. Rev. Plant Physiol. Mol. Biol.

    (1988)
  • S. Wilkinson et al.

    Drought, ozone, ABA and ethylene: new insights from cell to plant to community

    Plant Cell Environ.

    (2010)
  • J. Kang et al.

    PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid

    Proc. Natl. Acad. Sci. USA

    (2010)
  • T. Kuromori et al.

    ABC transporter AtABCG25 is involved in abscisic acid transport and responses

    Proc. Natl. Acad. Sci. USA

    (2010)
  • D.C. Boyes et al.

    Growth stage-based phenotypic analysis of Arabidopsis: A model for high throughput functional genomics in plants

    Plant Cell

    (2001)
  • J.Y. Lee et al.

    Use of serial analysis of gene expression technology to reveal changes in gene expression in Arabidopsis pollen undergoing cold stress

    Plant Physiol.

    (2003)
  • R.M. Warner et al.

    Naturally occurring variation in high temperature induced floral bud abortion across Arabidopsis thaliana accessions

    Plant Cell Environ.

    (2005)
  • T. Czechowski et al.

    Genome-wide identification and testing of superior reference genes for transcripts normalization in Arabidopsis

    Plant Physiol.

    (2005)
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