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Altered ABA, proline and hydrogen peroxide in an Arabidopsis glutamate:glyoxylate aminotransferase mutant

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Abstract

Plant responses to abiotic stress are determined both by the severity of the stress as well as the metabolic status of the plant. Abscisic acid (ABA) is a key component in integrating these various signals and controlling downstream stress responses. By screening for plants with decreased RD29A:LUC expression, we isolated two alleles, glutamate:glyoxylate transferase1-1 (ggt1-1) and ggt1-2, of a mutant with altered ABA sensitivity. In addition to reduced ABA induction of RD29A, ggt1-1 was altered in ABA and stress regulation of Δ 1 -pyrroline-5-carboxylate synthase, proline dehydrogenase and 9-cis-epoxycarotenoid dioxygenase 3, which encode enzymes involved in Pro and ABA metabolsim, respectively. ggt1-1 also had altered ABA and Pro contents after stress or ABA treatments while root growth and leaf water loss were relatively unaffected. A light-dependent increase in H2O2 accumulation was observed in ggt1-1 consistent with the previously characterized role of GGT1 in photorespiration. Treatment with exogenous H2O2, as well as analysis of a mutant in nucleoside diphosphate kinase 2 which also had increased H2O2 content but is not involved in photorespiration or amino acid metabolism, demonstrated that the greater ABA stimulation of Pro accumulation in these mutants was caused by altered H2O2 content as opposed to other metabolic changes. The results suggest that metabolic changes that alter H2O2 levels can affect both ABA accumulation and ABA sensitivity.

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Abbreviations

ABA:

Abscisic acid

COR15 :

Cold responsive 15

GGT1:

Glutamate:glyoxylate transferase 1

NCED3 :

9-cis-Epoxycarotenoed dioxygenase 3

NDPK2 :

Nucleoside diphosphate kinase 2

P5CS1 :

Δ 1 -Pyrroline-5-carboxylate synthase 1

PEG:

Polyethylene glycol 8000

ProDH:

Proline dehydrogenase

QPCR:

Quantitative real-time reverse transcriptase PCR

RAB18:

Responsive to ABA18

RD29A:LUC:

RD29A (responsive to dessication29A) promoter controlling expression of the luciferase coding region

ROS:

Reactive oxygen species

SA:

Salicylic acid

SHMT1:

Serine-hydroxylmethyl transferase

References

  • Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396

    Article  PubMed  CAS  Google Scholar 

  • Ball L, Accotto G-P, Bechtold U, Creissen G, Funck D, Jimenez A, Kular B, Leyland N, Mejia-Carranza J, Reynolds H, Karpinski S, Mullineaux PM (2004) Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in Arabidopsis. Plant Cell 16:2448–2462

    Article  PubMed  CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline in water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Bray EA, Beachy RN (1985) Regulation by ABA of β-conglycinin expression in cultured developing soybean cotyledons. Plant Physiol 79:746–750

    PubMed  CAS  Google Scholar 

  • Bright J, Desikan R, Hancock JT, Weir IS, Neill SJ (2006) ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J 45:113–122

    Article  PubMed  CAS  Google Scholar 

  • Chang CCC, Ball L, Fryer MJ, Baker NR, Karpinski S, Mullineaux PM (2004) Induction of ASCORBATE PEROXIDASE 2 expression in wounded Arabidopsis leaves does not involve known wound-signaling pathways but is associated with changes in photosynthesis. Plant J 38:499–511

    Article  PubMed  CAS  Google Scholar 

  • Cho Y-H, Yoo S-D, Sheen J (2006) Regulatory function of nuclear hexokinase1 complex in glucose signaling. Cell 127:579–589

    Article  PubMed  CAS  Google Scholar 

  • del Rio LA, Sandalio LM, Corpas FJ, Palma JM, Barroso JB (2006) Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiol 141:330–335

    Article  PubMed  CAS  Google Scholar 

  • Fabro G, Kovács I, Pavet V, Szabados L, Alvarez ME (2004) Proline accumulation and AtP5CS2 gene activation are induced by plant-pathogen incompatible interactions in Arabidopsis. Mol Plant Microbe Interact 17:343–350

    PubMed  CAS  Google Scholar 

  • Finkelstein RR, Gampala SSL, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14:S15–S45

    PubMed  CAS  Google Scholar 

  • Foyer CH, Noctor G (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119:355–364

    Article  CAS  Google Scholar 

  • Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875

    Article  PubMed  CAS  Google Scholar 

  • Fryer MJ, Ball L, Oxborough K, Karpinski S, Mullineaux PM, Baker NR (2003) Control of Ascorbate Peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organisation of Arabidopsis leaves. Plant J 33:691–705

    Article  PubMed  CAS  Google Scholar 

  • Guan L, Scandalios JG (1995) Developmentally related responses of maize catalase genes to salicylic acid. Proc Natl Acad Sci USA 92:5930–5934

    Article  PubMed  CAS  Google Scholar 

  • Hare PD, Cress WA, Van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Env 21:535–553

    Article  CAS  Google Scholar 

  • Hu JF, Li GF, Gao ZH, Chen L, Ren HB, Jia WS (2005) Regulation of water deficit-induced abscisic acid accumulation by apoplastic ascorbic acid in maize seedlings. J Integr Plant Biol 47:1335–1344

    Article  CAS  Google Scholar 

  • Igarashi D, Miwa T, Seki M, Kobayashi M, Kato T, Tabata S, Shinozaki K, Ohsumi C (2003) Identification of photorespiratory glutamate:glyoxylate aminotransferase (GGAT) gene in Arabidopsis. Plant J 33:975–987

    Article  PubMed  CAS  Google Scholar 

  • Igarashi D, Tsuchida H, Miyao M, Ohsumi C (2006) Glutamate:glyoxylate aminotransferase (GGAT) modulates amino acid contents during photorespiration. Plant Physiol Preview. doi:10.1104/pp106.085514

  • Imai R, Moses MS, Bray EA (1995) Expression of an ABA-induced gene of tomato in transgenic tobacco during periods of water deficit. J Exp Bot 46:1077–1084

    Article  CAS  Google Scholar 

  • Ishitani M, Xiong L, Stevenson B, Zhu J (1997) Genetic analysis of osmotic and cold stress signal transduction in Arabidopsis: interactions and convergence of abscisic acid-dependent and abscisic acid-independent pathways. Plant Cell 9:1935–1949

    Article  PubMed  CAS  Google Scholar 

  • Jiang MY, Zhang JH (2002) Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J Exp Bot 53:2401–2410

    Article  PubMed  CAS  Google Scholar 

  • Kiyosue T, Yoshiba Y, Yamaguchi-Shinozaki K, Shinozaki K (1996) A nuclear gene encoding mitochondrial proline dehydrogenase, an enzyme involved in proline metabolism, is upregulated by proline but downregulated by dehydration in Arabidopsis. Plant Cell 8:1323–1335

    Article  PubMed  CAS  Google Scholar 

  • Kwak JM, Mori IC, Pei Z-M, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JDG, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623–2633

    Article  PubMed  CAS  Google Scholar 

  • Kwak JM, Nguyen V, Schroeder JI (2006) The role of reactive oxygen species in hormonal responses. Plant Physiol 141:323–329

    Article  PubMed  CAS  Google Scholar 

  • Liepman AH, Olsen LJ (2001) Peroxisomal alanine:glyoxylate aminotransferase (AGT1) is a photorespiratory enzyme with multiple substrates in Arabidopsis thaliana. Plant J 25:487–498

    Article  PubMed  CAS  Google Scholar 

  • Liepman AH, Olsen LJ (2003) Alanine aminotransferase homologs catalyze the glutamate:glyoxylate aminotransferase reaction in peroxisomes of Arabidopsis. Plant Physiol 131:215–227

    Article  PubMed  CAS  Google Scholar 

  • Liepman AH, Olsen LJ (2004) Genomic analysis of aminotransferases in Arabidopsis thaliana. Crit Rev Plant Sci 23:73–89

    Article  CAS  Google Scholar 

  • Milla MAR, Maurer A, Huete AR, Gustafson JP (2003) Glutathione peroxidase genes in Arabidopsis are ubiquitous and regulated by abiotic stresses through diverse signaling pathways. Plant J 36:602–615

    Article  CAS  Google Scholar 

  • Moon H, Lee B, Choi G, Shin S, Prasad DT, Lee O, Kwak SS, Kim DH, Nam J, Bahk J, Hong JC, Lee SY, Cho MJ, Lim CO, Yun DJ (2003) NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants. Proc Natl Acad Sci USA 100:358–363

    Article  PubMed  CAS  Google Scholar 

  • Moore B, Zhou L, Rolland F, Hall Q, Cheng WH, Liu YX, Hwang I, Jones T, Sheen J (2003) Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300:332–336

    Article  PubMed  CAS  Google Scholar 

  • Moreno JI, Martin R, Castresana C (2005) Arabidopsis SHMT1, a serine hydroxymethyltransferase that functions in the photorespiratory pathway influences resistance to biotic and abiotic stress. Plant J 41:451–463

    Article  PubMed  CAS  Google Scholar 

  • Mori IC, Schroeder JI (2004) Reactive oxygen species activation of plant Ca2+ channels. A signaling mechanism in polar growth, hormone transduction, stress signaling, and hypothetically mechanotransduction. Plant Physiol 135:702–708

    Article  PubMed  CAS  Google Scholar 

  • Mullineaux PM, Karpinski S, Baker NR (2006) Spatial dependence for hydrogen peroxide-directed signaling in light-stressed plants. Plant Physiol 141:346–350

    Article  PubMed  CAS  Google Scholar 

  • op den Camp RGL, Przybyla D, Ochsenbein C, Laloi C, Kim C, Danon A, Wagner D, Hideg E, Gobel C, Feussner I, Nater M, Apel K (2003) Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15:2320–2332

    Article  CAS  Google Scholar 

  • Pastori GM, Foyer CH (2002) Common components, networks, and pathways of cross-tolerance to stress. The central role of “redox” and abscisic acid-mediated controls. Plant Physiol 129

  • Pastori GM, Kiddle G, Antoniw J, Bernard S, Veljovic-Jovanovic S, Verrier PJ, Noctor G, Foyer CH (2003) Leaf vitamin C contents modulate plant defense transcripts and regulate genes that control development through hormone signaling. Plant Cell 15:939–951

    Article  PubMed  CAS  Google Scholar 

  • Pavet V, Olmos E, Kiddle G, Mowla S, Kumar S, Antoniw J, Alvarez ME, Foyer CH (2005) Ascorbic acid deficiency activates cell death and disease resistance responses in Arabidopsis. Plant Physiol 139:1291–1303

    Article  PubMed  CAS  Google Scholar 

  • Rai V, Sharma S, Sharma S (1986) Reversal of ABA-induced stomatal closure by phenolic compounds. J Exp Bot 37:129–134

    Article  CAS  Google Scholar 

  • Rhoads DM, Umbach AL, Subbaiah CC, Siedow JN (2006) Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling. Plant Physiol 141:357–366

    Article  PubMed  CAS  Google Scholar 

  • Rossel JB, Walter PB, Hendrickson L, Chow WS, Poole A, Mullineaux PM, Pogson BJ (2006) A mutation affecting ASCORBATE PEROXIDASE 2 gene expression reveals a link between responses to high light and drought tolerance. Plant Cell Environ 29:269–281

    Article  PubMed  CAS  Google Scholar 

  • Sagi M, Fluhr R (2006) Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol 141:336–340

    Article  PubMed  CAS  Google Scholar 

  • Sharp RE, Wu Y, Voetberg GS, Saab IN, LeNoble ME (1994) Confirmation that abscisic accumulation is required for maize primary root elongation at low water potentials. J Exp Bot 45:1743–1751

    CAS  Google Scholar 

  • Shen Y-Y, Wang X-F, Wu F-Q, Du S-Y, Cao Z, Shang Y, Wang X-L, Peng C-C, Yu X-C, Zhu S-Y, Fan R-C, Xu Y-H, Zhang D-P (2006) The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443:823–826

    Article  PubMed  CAS  Google Scholar 

  • Shin R, Schachtman DP (2004) Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proc Natl Acad Sci USA 101:8827–8832

    Article  PubMed  CAS  Google Scholar 

  • Tan BC, Joseph LM, Deng WT, Liu LJ, Li QB, Cline K, McCarty DR (2003) Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family. Plant J 35:44–56

    Article  PubMed  CAS  Google Scholar 

  • Van Breusegem F, Dat JF (2006) Reactive oxygen species in plant cell death. Plant Physiol 141:384–390

    Article  PubMed  CAS  Google Scholar 

  • Verslues PE, Bray EA (2006) Role of abscisic acid (ABA) and Arabidopsis thaliana ABA-insensitive loci in low water potential-induced ABA and proline accumulation. J Exp Bot 57:201–212

    Article  PubMed  CAS  Google Scholar 

  • Verslues PE, Agarwal M, Katiyar-Agarwal S, Zhu JH, Zhu JK (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J 45:523–539

    Article  PubMed  CAS  Google Scholar 

  • Wingler A, Lea PJ, Quick WP, Leegood RC (2000) Photorespiration: metabolic pathways and their role in stress protection. Philos Trans R Soc Lond B 355:1517–1529

    Article  CAS  Google Scholar 

  • Xiong L, Zhu J-K (2003) Regulation of abscisic acid biosynthesis. Plant Physiol 133:29–36

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Ishitani M, Zhu J-K (1999) Interaction of osmotic stress, temperature, and abscisic acid in the regulation of gene expression in Arabidopsis. Plant Physiol 119:205–211

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Lee H, Ishitani M, Zhu J (2002) Regulation of osmotic stress-responsive gene expression by the LOS6/ABA1 locus in Arabidopsis. J Biol Chem 277:8588–8596

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (1993) Characterization of the expression of a desiccation-responsive rd29 gene of Arabidopsis thaliana and analysis of its promoter in transgenic plants. Mol Gen Genet 236:331–340

    Article  PubMed  CAS  Google Scholar 

  • Zeevaart JAD (1999) Abscisic acid metabolism and its regulation. In: Hall M, Libbenga K (eds) Biochemistry and molecular biology of plant hormones. Elsevier Science B.V

  • Zhang CS, Lu Q, Verma DPS (1995) Removal of feedback inhibition of Δ1-pyrroline−5-carboxylate synthetase, a bifunctional enzyme catalyzing the first 2 steps of proline biosynthesis in plants. J Biol Chem 270:20491–20496

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Zhang L, Dong FC, Gao JF, Galbraith DW, Song CP (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126:1438–1448

    Article  PubMed  CAS  Google Scholar 

  • Zhu J-K (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  PubMed  CAS  Google Scholar 

  • Zhu JH, Gong Z, Zhang C, Song C-P, Damsz B, Inan G, Koiwa H, Zhu J-K, Hasegawa PM, Bressan RA (2002) OSM1/SYP61: a syntaxin protein in Arabidopsis controls abscisic acid-mediated and non-abscisic acid-mediated responses to abiotic stress. Plant Cell 14:3009–3028

    Article  PubMed  CAS  Google Scholar 

  • Zhu JH, Verslues PE, Zheng XW, Lee B, Zhan XQ, Manabe Y, Sokolchik I, Zhu YM, Dong CH, Zhu J-K, Hasegawa PM, Bressan RA (2005) HOS10 encodes an R2R3-type MYB transcription factor essential for cold acclimation in plants. Proc Natl Acad Sci USA 102:9966–9971

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This work was supported by NIH grant 5R01GM059138 to J.-K.Z., by NSF grant IBN-0420152 to J.-K.Z and by an NIH postdoctoral fellowship (1F32GM074445) to P.E.V. We thank Giltsu Choi and Pill-Soon Song (Kumho Life and Environmental Science Laboratory, Korea) for the gift of ndpk2 seed. We also thank the laboratory of Dr Robert Heath for use of equipment for the Pro measurements and Rebecca Stevenson for technical assistance.

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  1. Yong-Sig Kim

    Present address: Department of Plant Sciences, University of Arizona, Tucson, AZ , 85721, USA

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  1. Department of Botany and Plant Sciences, Institute for Integrative Genome Biology, University of California, Riverside, CA, 92521, USA

    Paul E. Verslues & Jian-Kang Zhu

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  1. Paul E. Verslues
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Correspondence to Jian-Kang Zhu.

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Verslues, P.E., Kim, YS. & Zhu, JK. Altered ABA, proline and hydrogen peroxide in an Arabidopsis glutamate:glyoxylate aminotransferase mutant. Plant Mol Biol 64, 205–217 (2007). https://doi.org/10.1007/s11103-007-9145-z

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