Arabidopsis poly(ADP-ribose) glycohydrolase 1 is required for drought, osmotic and oxidative stress responses
Research highlights
▶ Loss of PARG1 function resulted in reduced tolerance to drought, osmotic and oxidative stress. ▶ Overexpression of PARG1 does not improve tolerance to drought, osmotic and oxidative stress. ▶ Function of PARG1 is required for abiotic stress response in Arabidopsis.
Introduction
During their lifespan, plants encounter many unfavorable environmental conditions, such as drought, salinity, and oxidative stress, which can adversely affect their growth and development [1]. To cope with abiotic stress, plants invoke multiple complicated and precisely regulated physiological and molecular networks, which are only now becoming understood through a combination of physiological, biochemical, molecular, genetic and genomics studies [2], [3], [4], [5], [6]. These responses of plants to environmental stress are now recognized to occur through altered expression of many abiotic stress-related genes, many of which have great potential for crop improvement [7], [8], [9], [10], [11].
Recent studies have demonstrated that post-translational modifications of some regulatory proteins can modulate plant responses to abiotic stresses [12], [13], [14], [15]. Poly(ADP-ribosyl)ation is an immediate, but transient, post-translational protein modification. This reaction is achieved by poly(ADP-ribose) polymerases (PARPs), which catalyze the transfer of ADP-ribose moieties from the substrate nicotinamide adenine dinucleotide (NAD+) to target proteins to form poly(ADP-ribose) polymers [16], [17]. By contrast, poly(ADP-ribose) glycohydrolases (PARGs) degrade poly(ADP-ribose) polymers [16], [17]. Proteins modified by poly(ADP-ribosyl)ation are involved in a wide range of cellular processes in animal systems, including chromatin decondensation, centrosome duplication, and telomere integrity, as well as cell division, transcription, DNA repair, cell survival, and death [17], [18], [19], [20], [21], [22], [23].
Increasing evidence now indicates that poly(ADP-ribosyl)ation is also one of the important regulatory mechanisms that modulate plant responses to various abiotic stresses. The first line of evidence came from experiments with cultured soybean and tobacco suspension cells that were protected from programmed cell death triggered by H2O2 or heat shock by the addition of PARP inhibitors [24], [25]. Later studies showed that DNA damage induced by ionizing radiation activates a rapid and massive expression of PARP1 and PARP2 genes in all Arabidopsis tissues, whereas the accumulation of PARP2 transcripts is preferentially induced by dehydration and cadmium stress [26]. Further functional analysis revealed an inhibition of cell death and conferral of more tolerance to a broad range of abiotic stresses, such as high light intensity, drought, and heat stress, when PARP activity was reduced by means of chemical inhibitors or by gene silencing [27]. Similarly, reduction of PARP2 levels by RNAi-mediated downregulation in transgenic Arabidopsis and oilseed rape plants resulted in greater resistance to various abiotic stresses, including drought stress, in laboratory and greenhouse experiments, but had no significant effect on growth, development, and seed production [28]. This increased stress tolerance was initially attributed to maintenance of energy homeostasis due to reduced NAD+ consumption or increased levels of cyclic ADP-ribose, but microarray-based gene expression profiling revealed an up-regulation of a large set of abscisic acid (ABA)-responsive genes in PARP2-deficient plants [27], [28], [29]. Recent studies have also implicated PARP in plant responses to pathogen infection, as the induction of innate immune responses (e.g., callose deposition, lignin deposition, and phenylalanine ammonia lyase activity) by treatment with two well-known microbe-associated molecular patterns, flg22 and elf18, which can be blocked by PARP inhibitors [30], [31].
In contrast, little is known about the functions of PARGs in plants. Recently, PARG1 (or At2g31870, also known as TEJ) was implicated as a regulator of the circadian oscillator because mutation of PARG1 in Arabidopsis affected the clock-controlled transcription of genes and altered the timing of photoperiod-dependent transition from vegetative growth to flowering [32]. Expression of putative PARG genes including PARG1 was also up-regulated in response to oxidative stress caused by methyl viologen (MV) [33]. Functional analysis using T-DNA insertion lines indicated that mutations in both PARG1 and another putative PARG gene (At2g31865) accelerated the onset of disease symptoms caused by infection with Botrytis cinerea [31]. Therefore, like PARPs, PARGs also appear to have diverse functions in plant biotic and abiotic stress responses.
In our study on the function of PARG1 in disease resistance response, we occasionally observed that plants of a parg1 mutant line suffered drought stress while the wild type plants grew normally in an accident that all Arabidopsis plants grown in a growth room were not watered for a period of 4-days. In the present study, we thus examined in detail the possible function of PARG1 in abiotic stress tolerance in Arabidopsis using genetic mutant parg1-3 and transgenic PARG1-overexpressing plants. Our results indicate that PARG1 is required for tolerance to drought, osmotic and oxidative stress in Arabidopsis and thus suggest an important role for PARGs in abiotic stress response in plants.
Section snippets
Plant materials and growth conditions
Seeds of wild type (ecotypes Col-0 and Ws-0) and a T-DNA insertion line (FLAG315E11) were obtained from the Arabidopsis thaliana Resource Centre at Ohio State University, USA, and the Arabidopsis thaliana Resource Centre for Genomics at the Versailles Genetics and Plant Breeding Laboratory, France, respectively. All Arabidopsis plants were grown in soil or grown on a 1/2 Murashige and Skoog (MS) medium containing 1% sucrose and 0.8% agar in a growth room under fluorescent lighting (150 μE m2 s−1)
Characterization of parg1-3 mutant and transgenic overexpression lines
The Arabidopsis PARG1 gene (At2g31870) consists of 11 exons and 10 introns (Fig. 1a) and this annotation for exon/intron organization of the PARG1 gene is confirmed by two full-length cDNAs (AF394690 and AK222165) in the GenBank database. Two T-DNA insertion lines, SALK_147805 and SALK_116086, were previously identified and designated parg1-1 and parg1-2, respectively (Fig. 1a) [31]. The parg1-1 and parg1-2 lines contain T-DNA insertions in the eighth and ninth introns, respectively, which are
Discussion
Poly(ADP-ribosyl)ation is a unique posttranslational protein modification involved in plant responses to biotic and abiotic stresses, as shown through detailed functional analyses of PARPs and PARGs [27], [28], [30], [31]. In the present study, use of genetic mutant and transgenic overexpression lines allowed us to examine the role of PARG1 in tolerance to various abiotic stresses. The normal function of PARG1 is required for tolerance of Arabidopsis to drought, osmotic and MV-induced oxidative
Acknowledgement
We thank the Arabidopsis thaliana Resource Centre for Genomics at the Versailles Genetics and Plant Breeding Laboratory, France, for the T-DNA insertion line seeds. This work was supported in part by the Natural Science Foundation of China (Grant No. 30771399), the National Basic Research Program of China (2009CB119005) and the National Key Project for Research on Transgenic Plant (2009ZX08001-017B).
References (50)
Abiotic stress, the field environment and stress combination
Trends Plant Sci.
(2006)- et al.
The reactive oxygen gene network of plants
Trends Plant Sci.
(2004) - et al.
Regulatory metabolic networks in drought stress responses
Curr. Opin. Plant Biol.
(2007) - et al.
Developing salt-tolerant crop plants: challenges and opportunities
Trends Plant Sci.
(2005) - et al.
Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future
Curr. Opin. Biotechnol.
(2006) Inducing drought tolerance in plants: recent advances
Biotechnol. Adv.
(2010)- et al.
Poly(ADP-ribose) makes a date with death
Curr. Opin. Chem. Biol.
(2007) - et al.
The expanding role of poly(ADP-ribose) metabolism: current challenges and new perspectives
Curr. Opin. Cell. Biol.
(2006) - et al.
The involvement of poly(ADP-ribose) polymerase in the oxidative stress responses in plants
FEBS Lett.
(1998) - et al.
Involvement of poly(ADP-ribose) polymerase and activation of caspase-3-like protease in heat shock-induced apoptosis in tobacco suspension cells
FEBS Lett.
(2000)
tej defines a role for poly(ADP-ribosyl)ation in establishing period length of the Arabidopsis circadian oscillator
Dev. Cell
Low concentration of arsenite exacerbates UVR-induced DNA strand breaks by inhibiting PARP-1 activity
Toxicol. Appl. Pharmacol.
The MutT proteins or ‘Nudix’ hydrolases, a family of versatile, widely distributed, ‘housecleaning’ enzymes
J. Biol. Chem.
Identification and characterization of the Nudix hydrolase from the Archaeon, Methanococcus jannaschii, as a highly specific ADP-ribose pyrophosphatase
J. Biol. Chem.
Salt and drought stress signal transduction in plants
Ann. Rev. Plant Biol.
Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses
Annu. Rev. Plant Biol.
Gene networks involved in drought stress response and tolerance
J. Exp. Bot.
Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance
Planta
Transgenic approaches for abiotic stress tolerance in plants: retrospect and prospects
Plant Cell Rep.
Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis
PLoS Biol.
Distinctive core histone post-translational modification patterns in Arabidopsis thaliana
PLoS ONE
Up-regulation of stress-inducible genes in tobacco and Arabidopsis cells in response to abiotic stresses and ABA treatment correlates with dynamic changes in histone H3 and H4 modifications
Planta
Alterations of lysine modifications on the histone H3 N-tail under drought stress conditions in Arabidopsis thaliana
Plant Cell Physiol.
Regulation of poly(ADP-ribose) metabolism by poly(ADP-ribose) glycohydrolase: where and when?
Cell Mol. Life Sci.
Poly(ADP-ribose): novel functions for an old molecule
Nat. Rev. Mol. Cell Biol.
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