Glutathione and plant response to the biotic environment

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    nepoli

    Microbe

    GlutathioneRedox

    . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 724actionsplants. . . . . .. . . . . .

    another ATP-dependent reaction. The primary sequence of GS differs

    found in both thelates to millimolarologs have beenserved is homo-ddition to GSH in5,6]. Its synthesis

    redox reactions of the cysteine sulfur group, resulting in the

    Contents lists available at ScienceDirect

    vie

    Free Radical Biolog

    Free Radical Biology and Medicine 65 (2013) 724730which uses NADPH to supply reducing power. GSH can also reactE-mail address: frendo@unice.fr (P. Frendo).coexistence of a reduced state (GSH) and an oxidized state (GSSG),in which two GSH molecules are linked via a disulde bound. Thecellular GSH pool is mostly reduced under optimal conditions. Theredox status of GSH is kept high by glutathione reductase (GR),

    0891-5849/$ - see front matter & 2013 Elsevier Inc. All rights reserved.http://dx.doi.org/10.1016/j.freeradbiomed.2013.07.035

    n Corresponding author at: Institut Sophia Agrobiotech, 400 Route des Chappes,F-06903 Sophia Antipolis Cedex, France.sequence of GSH1 is not conserved in these different groups oforganisms [1]. In the second step, glutathione synthetase (GS orGSH2) catalyzes the formation of GSH from GC and glycine, in

    requires a specic homoglutathione synthetase, encoded by a genederived from the GS gene by gene duplication [7].

    The biological functions of GSH relate principally to reversibleGlutathione (GSH) is a tripeptide (-glutamylcysteinylglycine)present in a broad range of organisms, from bacteria to humans. It issynthesized in a two-step process. In the rst step, -glutamylcysteinesynthetase or -glutamylcysteine ligase (-GCL, GSH1) catalyzes theformation of -glutamylcysteine (GC) from glutamate and cysteine, inan ATP-dependent reaction. Surprisingly, although GSH is present inmany organisms, including bacteria, plants, and animals, the primary

    encoded by a nuclear gene (GSH1) and is targetedGS is also encoded by a nuclear gene (GSH2) and isplastids and the cytosol [3,4]. In plants, GSH accumuconcentrations within cells. Multiple GSH homdetected in plants. One of the most frequently obglutathione (hGSH), which replaces or is present in athe large and diverse plant family Leguminosae [Introduction between eukaryotes and prokaryotes [1]. In plants, the GSH synthesispathway takes place in the plastid and cytosol (Fig. 1). -GCL is

    to plastids [2,3].Contents

    Introduction. . . . . . . . . . . . . . . . . . . . .Glutathione and plantpathogen interGlutathione and interactions betweenConclusion and perspectives. . . . . . . .References . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 725and benecial microbes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 726. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 727. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 728PathogenesisSymbiosisReceived in revised form22 July 2013Accepted 23 July 2013Available online 1 August 2013

    Keywords:Plant

    have claried the molecular processes involving GSH in plantmicrobe interactions. In this review, wesummarize recent studies, highlighting the roles of GSH in interactions between plants and microbes,whether pathogenic or benecial to plants.

    & 2013 Elsevier Inc. All rights reserved.Received 31 January 2013 development and respons

    Article history: Glutathione (GSH) is a major antioxidant molecule in plants. It is involved in regulating plant

    es to the abiotic and biotic environment. In recent years, numerous reportsReview Article

    Glutathione and plant response to the b

    Pierre Frendo a,b,c,n, Fabien Baldacci-Cresp a,b,c, Soaa Universit de NiceSophia Antipolis, Institut Sophia Agrobiotech, F-06903 Sophia Antib INRA UMR 1355, Institut Sophia Agrobiotech, F-06903 Sophia Antipolis Cedex, Francec CNRS UMR 7254, Institut Sophia Agrobiotech, F-06903 Sophia Antipolis Cedex, France

    a r t i c l e i n f o a b s t r a c t

    journal homepage: www.elsetic environment

    M. Benyamina a,b,c, Alain Puppo a,b,c

    s Cedex, France

    r.com/locate/freeradbiomed

    y and Medicine

  • with protein cysteine residues to form mixed disuldes via aglutathionylation process. Protein glutathionylation has beenextensively investigated in animals [811], but much less is knownabout this process in plants [12,13]. Glutaredoxins (GRXs), whichcouple GSH redox potential to changes in protein thioldisuldestatus, are involved in the deglutathionylation process and in theregeneration of multiple enzymes, such as peroxiredoxins andmethionine sulfoxide reductases [14,15]. GSH may also reactwith numerous endogenous and xenobiotic electrophilic com-pounds, via glutathione S-transferases [16,17]. Finally, GSHalso protects plants against heavy metals, through the formationof phytochelatins (PCs), which are GSH polymers. PCs are

    metabolism and plant defense mechanisms [28]. This associationbetween GSH content and plant defense has also been demon-

    Fig. 1. Synthesis and transport of glutathione in a plant cell. Glutathione (GSH) issynthesized in a two-step biosynthetic pathway involving -glutamylcysteine ligase(GSH1) and glutathione synthetase (GSH2). The redox state of GSH is regulated byglutathione reductase (GR).

    P. Frendo et al. / Free Radical Biology and Medicine 65 (2013) 724730 725Fig. 2. General roles of glutathione in plants. Glutathione (GSH) is used as asubstrate by glutaredoxins (GRX) and glutathione S-transferases (GST); it is alsoinvolved in protein glutathionylation. In plants GSH is involved in development,abiotic and abiotic stress responses, and protection against heavy metals and

    xenobiotics.strated with other GSH1-decient mutants, cad2-1 and rax1-1,which are less resistant than the wild type to avirulent strains of P.syringae [23].

    Thioldisulde redox status is clearly involved in the regulationof a major regulatory protein, NPR1 (nonexpressor of PR gene 1)[36]. NPR1 must be converted from its oligomeric form to amonomer for translocation from the cytosol to the nucleus, andthis requires the reduction of the disulde bonds of the oligomericform [31]. It has also been shown that the disulde bonds can bereduced in vitro in vitro with a GSH:GSSG buffer at physiologicalconcentration [31]. Furthermore, NPR1 can also be reduced bythioredoxins (Trxs) [37]. However, NPR1 oligomerization may alsobe in vitro regulated in vitro by nitrosylation, with S-nitrosoglu-tathione (GSNO) [37]. Moreover, the SA-induced monomerization ofNPR1 and its nuclear translocation are inhibited in the atgsnor1-3mutant, which lacks the GSNO reductase and has high levels of S-nitrosylation activity [37,38]. The resistance of atgsnor1-3 mutantsto pathogens is severely compromised [38], and atgsnor1-3mutantssynthesized by phytochelatin synthase, which uses GSH as asubstrate [18].

    GSH plays a crucial role in plant development (Fig. 2). Analysesof the phenotypes of Arabidopsis thaliana GSH-decient mutantshave shown that GSH is involved in embryo and meristemdevelopment [19,20]. Abiotic and biotic stresses play a crucial rolein the regulation of development and the adaptation of plants totheir environment [21,22]. In this context, GSH has been shown tobe involved in light signaling, in studies of the Arabidopsis rax1mutant, which has only half the normal level of GSH in its leavesand displays constitutive expression of the photo-oxidative stress-inducible ascorbate peroxidase 2 [23]. However, the role of GSH isnot restricted to the regulation of the plant growth and adaptationto the abiotic environment. This molecule is also involved in theresponse of the plant to its biotic environment. In this review, weanalyze the links between glutathione metabolism and the adap-tation of the plant to its biotic environment.

    Glutathione and plantpathogen interactions

    Studies in the late 1980s showed that the treatment of culturedplant cells with exogenous GSH induced the accumulation of plantdefense-related transcripts for proteins such as phenylpropanoidbiosynthetic enzymes, phenylalanine ammonia-lyase, and chal-cone synthase, which is involved in lignin and phytoalexinproduction [24,25]. Treatment with pathogen-derived elicitorswas then shown to induce GSH accumulation in cell cultures[26] or in plants, during defense induction [27,28]. The plantdefense response to pathogens also modies the redox state ofGSH [29]. Moreover, GSH levels increase after treatment withthe defense-related plant hormone salicylic acid (SA), and theredox state of this molecule shifts toward a more reduced state[3032].

    The rst genetic evidence of a role for GSH in defense reactionswas provided by the isolation of Arabidopsis phytoalexin-decient(pad) mutants [33]. The pad2 mutant line displays impairedproduction of the phytoalexin camalexin and enhanced suscept-ibility to the pathogenic bacterium Pseudomonas syringae. Thismutant line has also been shown to be susceptible to thepathogenic oomycetes Phytophthora porri and Botrytis cinerea[34,35]. Levels of pathogenesis-related protein 1 and of SA arevery low in the pad2mutant line [34]. The identication of PAD2 asGSH1 demonstrated the existence of a clear link between GSHalso display alterations to SA metabolism, with lower levels of SA

  • knot nematodes (RKNs) and Medicago truncatula [58]. RKNs are

    P. Frendo et al. / Free Radical Biology and Medicine 65 (2013) 724730726accumulation and a weaker response to exogenous SA treatment.Thus, GSH may also play an important role in regulating plantdefense mechanisms, by acting as a nitric oxide (NO) reservoir [39].Interestingly, GSH metabolism seems to be regulated by NOaccumulation, at least after exogenous treatment [40,41].

    The ratio of GSH to GSSG was also clearly shown to play a rolein plant defense by a genetic approach based on the conditionalcatalase-decient Arabidopsis mutant cat2 [42]. Photorespiration isa light-dependent process generating hydrogen peroxide (H2O2) inthe peroxisome within the plant cell. The concentrations of thissignaling molecule are regulated by catalase. The growth ofArabidopsis catalase 2 (CAT2)-knockout mutants in ambient airresults in changes to intracellular redox balance, the activation ofoxidative signaling pathways, and an induction of defense geneexpression, linked to the development of hypersensitive response(HR)-like lesions [42]. This phenotype is dependent on long-dayirradiation and CO2 level (high CO2 levels inhibit photorespirationand the stress-related phenotype) [42]. The Arabidopsis cat2mutant may be seen as a model mimicking inducible stress [43].The role of GSH redox state in the cat2 phenotype has beenanalyzed by introducing the gr1 mutation into the cat2 mutantbackground [44]. GR1 is a cytosolic GR that regulates GSH redoxstate. An analysis of gr1 and cat2 transcriptomes led to theidentication of genes displaying a similar pattern of regulation,including phytohormone-associated genes, such as those regulat-ing jasmonic acid signaling [43]. Jasmonic acid and methyljasmonate, collectively referred to as jasmonate (JA), are planthormones involved in the plant response to pathogens [4547].Growth rates for virulent P. syringae are higher in gr1mutants thanin the control background, and this stronger bacterial growth iscorrelated with the lower SA content of gr1mutants. An analysis ofcat2 gr1 double mutants demonstrated that GR1-dependent GSHstatus controls multiple responses to increases in the availability ofH2O2, including the limitation of lesion formation, SA accumula-tion, the induction of pathogenesis-related genes and signaling viathe jasmonic acid pathways [43]. A similar approach was used todetermine the role of GSH level in H2O2 signaling; this approachinvolved the introduction of the cad2 mutation, which reducesGSH content, into the cat2 line [48]. In addition to the responsesalready observed in the gr1 and npr1 mutant lines, the cad2mutation altered the H2O2 signaling pathway by compromisingthe induction of the isochorismate synthase 1 (ICS1) gene, whichregulates SA synthesis [49]. Thus, in addition to acting as anantioxidant, GSH regulates SA by modulating ICS1 expressionindependent of NPR1 [48].

    Unlike SA, which is involved in plant defense against biotrophicpathogens, JA seems to be more involved in plant defense againstnecrotrophic pathogens and insects [46]. Exogenous treatmentwith JA activates the GSH metabolism pathway [50,51]. Resistanceto the generalist insect Spodoptera littoralis is compromised in theArabidopsis mutant pad2, because the two major indole andaliphatic glucosinolates of Arabidopsis produced in response toinsect feedingindolyl-3-methylglucosinolate and 4-methylsul-nylbutylglucosinolateaccumulate to a much lesser extent in thismutant than in the wild type. This effect was not reversed bytreatment with the strong reducing agent dithiothreitol, suggest-ing that it is not mediated by redox changes [52]. Cross talkbetween the SA and the JA signaling pathways plays an importantrole in the regulation and ne-tuning of induced defenses againstpathogens and insect attack. The expression of JA-regulated genesis decreased by SA [32,53,54]. The suppressive effect of SA on theexpression of the JA-responsive defensin gene PDF1.2 is correlatedwith a transient increase in GSH levels. Treatment with buthioninesulfoximine, a GSH biosynthesis inhibitor, strongly decreases thissuppressive effect of SA, suggesting that GSH plays an important

    role in the SA-mediated reduction of JA-regulated gene expressionobligate parasites of plants. These worms induce the redifferentia-tion of root cells into multinucleate, hypertrophied giant cellsessential for nematode growth and reproduction. These metabo-lically active feeding cells constitute the sole source of nutrientsfor the nematode [59]. The depletion of GSH and hGSH impairsnematode egg mass formation and modies the sex ratio, demon-strating the importance of these molecules in the M. truncatulaRKN interaction [58]. The changes to this interaction are correlatedwith specic modications of carbon metabolism in (h)GSH (GSH+hGSH)-depleted galls, suggesting that (h)GSH plays a key role inregulating giant cell metabolism [58]. An analysis of the potentialeffectors present in the Meloidogyne incognita secretome revealedthe presence of a putative GS, suggesting that the nematode maymodify giant cell GSH metabolism [60].

    In conclusion, GSH plays a key role in the regulation ofinteractions between plants and pathogens, whether these patho-gens are prokaryotic, such as bacteria, or euk...

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