Glutathione and plant response to the biotic environment

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ionepoliMicrobeGlutathioneRedox. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 724actionsplants. . . . . .. . . . . .another ATP-dependent reaction. The primary sequence of GS differsfound in both thelates to millimolarologs have beenserved is homo-ddition to GSH in5,6]. Its synthesisredox reactions of the cysteine sulfur group, resulting in theContents lists available at ScienceDirectvieFree Radical BiologFree 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.2013.07.035n 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, inrequires 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 primaryencoded 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 isto plastids [2,3].ContentsIntroduction. . . . . . . . . . . . . . . . . . . . .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 2013Keywords:Planthave 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 responsArticle history: Glutathione (GSH) is a major antioxidant molecule in plants. It is involved in regulating plantes to the abiotic and biotic environment. In recent years, numerous reportsReview ArticleGlutathione and plant response to the bPierre 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, Francea r t i c l e i n f o a b s t r a c tjournal homepage: www.elsetic environmentM. Benyamina a,b,c, Alain Puppo a,b,cs Cedex, Francer.com/locate/freeradbiomedy and Medicinewith 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 aremetabolism 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 andxenobiotics.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 interactionsStudies 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 SAknot nematodes (RKNs) and Medicago truncatula [58]. RKNs areP. 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 importantrole 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 eukaryotic, such as fungi,oomycetes, nematodes, and insects.Glutathione and interactions between plants and benecialmicrobesGSH also plays an important role during interactions betweenthe plant and benecial microbes. The most studied such interac-tion is nitrogen-xing symbiosis (NFS). Legumes interact symbio-tically with bacteria of the Rhizobiaceae to form nitrogen-xingroot nodules. During this process, an exchange of recognitionsignals between the plant and the bacterial partners allows thebacteria to penetrate into the host plant root and triggers thedevelopment of a new nitrogen-xing organ, the root nodule. Therhizobia then develop into intracellular symbionts, the bacteroids,which modify their metabolism to x atmospheric nitrogen[61,62]. Redox signaling has been shown to play a role in theestablishment and functioning of NFS [6365].A rst indication of the importance of GSH in NFS was providedby analysis of the ascorbateGSH pathway in soybean root nodules[66]. Early in nodule development, ascorbate peroxidase anddehydroascorbate reductase activities increase markedly, as doesthe total glutathione content of nodule extracts, and theseincreases are positively correlated with nitrogen xation efciency(NFE), suggesting an important role for glutathione. High concen-[32]. The role of GSH redox state in JA/SA cross talk was conrmedby analysis of the cat2 and gr1 mutant lines [44]. The cat2mutation induces the accumulation of SA during long days. ThisSA accumulation is correlated with the repression of JA-associatedgenes. A similar repression of JA-associated genes is observed inthe gr1 mutant line, suggesting that an optimum GSH redox stateis required for induction of the JA-regulated genes [44]. Finally, theexpression of JA-related genes is correlated with leaf GSH contentand the induction of these genes in a cat2 mutant background ispartially dependent on cellular GSH content [48,55]. Takentogether, these results show that GSH content and redox statemay regulate JA-associated genes.GSH also seems to be involved in the plant response to obligateparasites. The obligate biotrophic pathogen Plasmodiophora bras-sicae induces clubroot disease in all members of the Brassicaceae[56]. The development of galls on the root system is associatedwith the establishment of a new carbon metabolic sink, allowingthe parasite to complete its life cycle. An analysis of the metabolicresponse to the infection in 18 rapeseed genotypes displayingdifferent degrees of symptom severity showed that GSH accumu-lation in roots was a positive marker of disease development [57].Similarly, GSH content increases during interactions between roottrations of GSH and of hGSH, a GSH analog present in legumes,have been found not only in soybean nodules, but also in thenodules of other legumes, such as pea and M. truncatula [67,68].These high GSH and hGSH concentrations are associated with NFE[69]. A correlation between GSH concentration and NFE has alsobeen reported during the natural and stress-induced senescence ofroot nodules [67,7073].The importance of (h)GSH during the early stages of nitrogen-xing symbiosis was demonstrated by studies of the interactionbetween M. truncatula and Sinorhizobium meliloti [74]. The deple-tion of (h)GSH by pharmacological and genetic approaches inhibitsroot nodule formation. Plants depleted of (h)GSH during thenodulation process have far fewer nascent nodules and lower(SmgshA) has been shown not to grow under free-living conditions,precluding nodulation. By contrast, an S. meliloti GS-mutant strain(SmgshB) grows under such conditions, indicating that -glutamylcys-teine, the dipeptide intermediate, may be able to substitute for GSH.However, the SmgshB strain forms nodules later than the wild type, itsNFE is 75% lower, and its nodules senesce early [84]. Delayednodulation and early nodule senescence have also been reported forPhaseolus vulgaris (common bean) inoculated with the Rhizobiumtropici gshB mutant strain [85]. By contrast, the deletion of -GLC fromthe Bradyrhizobium sp. SEMIA 6144 strain has no effect on thesymbiotic efcacy of the bacterium [86].The importance of S. meliloti GRXs during NFS has beenthe scaffold to acceptor apoproteins [89]. This iron-associatedomoiruleassicicicongaeralisognieliloP. Frendo et al. / Free Radical Biology and Medicine 65 (2013) 724730 727levels of expression of the early nodulin genes MtENOD12 andMtENOD40 than control plants [74]. Lower root nodule numberand dry weight have also been reported for GSH-depleted peanutroots [75]. Transcriptomic analysis of the response of (h)GSH-depleted M. truncatula roots to S. meliloti infection has shown that(h)GSH depletion increases the expression of SA-regulated genesafter S. meliloti infection to levels higher than those in inoculatedcontrol roots [76]. The expression of SA-regulated genes inresponse to exogenous SA treatment is enhanced by (h)GSHdeciency, suggesting changes to SA perception [76]. SA has beenshown to inhibit the nodulation process, by both pharmacologicaland genetic approaches [7779]. Its effects during the infectionprocess may be mediated by NPR1 [80].(H)GSH is also involved in regulating NFE in mature nodules[81]. Genetic approaches based on the use of the nodule nitrogen-xing zone-specic nodule cysteine-rich (NCR001) promoter havebeen used to deplete (h)GSH or to cause its overaccumulation inthe nitrogen-xing zone. Downregulation of the -GCL gene byRNA interference results in a signicantly lower NFE, associatedwith signicantly lower levels of expression of the leghemoglobinMtlb1 gene and smaller nodules [81]. Conversely, -GCL over-expression results in higher GSH levels, which are correlated witha higher NFE and signicantly higher levels of expression of thesucrose synthase-1 and leghemoglobin genes, two molecular mar-kers of the symbiotic process. Thus, NFE is correlated to the plant(h)GSH content of the nodule nitrogen-xing zone. Nodule GSHcontent declines in parallel with NFE as nodules age, but theresultant decrease in redox buffering capacity does not necessarilylead to enhanced reactive oxygen species or oxidative stress [82].It has been proposed that a high level of GSH and ascorbatesignaling is commensurate with meristem activity and symbiosis;a decline in nodule GSH with age (together with a decline inascorbate content) will slow mitosis contributing to the agingprocess in indeterminate nodules where there is a persistentmeristem but not in determinate nodules where meristematicactivity ceases early in development [82].The importance of GSH in NFS has also been studied from theviewpoint of the microbial partner. Unlike Escherichia coli, mutantS. meliloti strains lacking -GCL and GS grow less well in the absencethan in the presence of stress [83,84]. An S. meliloti -GLCmutant strainTable 1Studies showing the importance of GSH in plantmicrobe interactions.Plant MicrobeArabidopsis rax1-1 and cad2-1 mutants Avirulent PseudArabidopsis pad2 mutant Virulent and avArabidopsis pad2 mutant Phytophthora brArabidopsis pad2 mutant Botrytis cinereaArabidopsis pad2 mutant Alternaria brassArabidopsis gr1 mutant Virulent Ps. syriArabidopsis pad2 mutant Spodoptera littoM. truncatula -GCL RNAi line Meloidogyne incM. truncatula -GCL RNAi line Sinorhizobium mbiological activity is mediated by GRXs with a cysteine-glycine-phenylalanine-serine protein motif (CGFS) in their catalytic site.SmGRX1 (CGYC active site) displays deglutathionylation activityand the deletion of SmGRX1 leads to nodule abortion and anabsence of bacteroid differentiation [87]. SmGRX2 (CGFS activesite) is involved in regulating iron metabolism. The Smgrx2 mutantstrain has signicantly lower levels of activity than the wild typefor two ironsulfur-containing enzymes, aconitase and succinatedehydrogenase; it also displays a deregulation of the transcrip-tional activity of the RirA iron regulator and has a higherintracellular iron content [87]. These phenotypes are associatedwith a signicantly lower NFE. Thus, two S. meliloti GRXs areessential for symbiotic nitrogen xation, playing independentroles in bacterial differentiation and the regulation of iron meta-bolism. As these phenotypes are distinct and less severe than thatobserved with the GSH-depleted mutant strain, its seems likelythat GSH is involved in other rhizobial metabolic processes.The role of GSH in other interactions between plants and benecialmicrobes is not well dened. However, rice associated with thearbuscular mycorrhizal fungus Glomus intraradices has a signicantlyhigher shoot GSH content than control plants [90], suggesting thatGSH may also be involved in mycorrhizal symbiosis.Conclusion and perspectivesThe studies summarized in this review show that GSH is stronglyinvolved in plantmicrobe interactions (Table 1). For rhizobial andmycorrhizal symbioses in particular, characterization of the putativeinvolvement of GSH in the Nod and Myc factor signaling cascade is akey issue. In general, analyses of mutant and transgenic organismsRef.nas syringae pv tomato DC3000avrRpm1 [23]nt Ps. syringae pv tomato and maculicol [33]ae (Phytophthora porri) [34][35]la [97]pv tomato DC3000 [44][52]ta [58]ti [74,81]analyzed [87]. Glutaredoxins are small ubiquitous oxidoreductasesof the Trx superfamily that preferentially reduce the disuldebonds formed between cysteine residues of proteins and GSH[14,88]. The deglutathionylation reaction mostly concerns Grx'swith a cysteine-X-X-cysteine motif in their catalytic site. However,it has also been suggested that GRXs act as scaffold proteins for thede novo synthesis of ironsulfur clusters (ISCs) or as carrierproteins or chaperones for the transfer and delivery of ISCs fromtion is that of the glutathione S-transferases (GSTs). This name isP. Frendo et al. / Free Radical Biology and Medicine 65 (2013) 724730728misleading, as the members of this protein family not only transferGSH to multiple substrates, but also are involved in deglutathio-nylation. Thus, the large numbers of GSTs present in plants mayreect multiple functions, some of which may be linked to plantmicrobe interactions [91]. However, the possible links betweenglutathionylation, nitrosylation, and sulfenylation further highlightthe core role of GSH, as sulfenylated and nitrosylated proteins havebeen detected during legumerhizobium symbiosis [94,95] andplantpathogen interactions [96]. The possible buffering role ofGSNO thus requires further investigation.Finally, the results obtained with rhizobia show that GSH is alsoimportant for the microbial partner in plantmicrobe interactionsand highlight the crucial role of this tripeptide in the coevolutionprocess leading to symbiosis. In this context, an analysis of theimportance and roles of GSH in microbial partners might provideinteresting insights into the role of this molecule in microbialinteractions with the plant. Further analyses of the importance ofGSH in interactions between plants and plant growth-promotingrhizobacteria and mycorrhiza are also required to obtain a holisticview of the role of GSH in plantmicrobe interactions.References[1] Copley, S. 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