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A tomato glutaredoxin gene SlGRX1 regulates plant responses to oxidative, drought and salt stresses

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Abstract

Glutaredoxins (Grxs) are ubiquitous small heat-stable disulfide oxidoreductases that play a crucial role in plant development and response to oxidative stress. Here, a novel cDNA fragment (SlGRX1) from tomato encoding a protein containing the consensus Grx family domain with a CGFS active site was isolated and characterized. Southern blot analysis indicated that SlGRX1 gene had a single copy in tomato genome. Quantitative real-time RT-PCR analysis revealed that SlGRX1 was expressed ubiquitously in tomato including leaf, root, stem and flower, and its expression could be induced by oxidative, drought, and salt stresses. Virus-induced gene silencing mediated silencing of SlGRX1 in tomato led to increased sensitivity to oxidative and salt stresses with decreased relative chlorophyll content, and reduced tolerance to drought stress with decreased relative water content. In contrast, over-expression of SlGRX1 in Arabidopsis plants significantly increased resistance of plants to oxidative, drought, and salt stresses. Furthermore, expression levels of oxidative, drought and salt stress related genes Apx2, Apx6, and RD22 were up-regulated in SlGRX1-overexpressed Arabidopsis plants when analyzed by quantitative real-time PCR. Our results suggest that the Grx gene SlGRX1 plays an important role in regulating abiotic tolerance against oxidative, drought, and salt stresses.

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Abbreviations

MS-medium:

Murashige and Skoog medium

NCBI:

National center for biotechnology information

PCR:

Polymerase chain reaction

RT-PCR:

Reverse transcription PCR

VIGS:

Virus-induced gene silencing

TYLCCNV:

Tomato yellow leaf curl China virus

Grx:

Glutaredoxin

TMV:

Tobacco mosaic virus

CaMV:

Cauliflower mosaic virus

qRT-PCR:

Quantitative real-time RT-PCR

References

  • Alonso JM, Stepanova AN, Leisse TJ et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657

    Article  PubMed  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Ardie SW, Xie LN, Takahashi R, Liu SK, Takano T (2009) Cloning of a high-affinity K+ transporter gene PutHKT2;1 from Puccinellia tenuiflora and its functional comparison with OsHKT2;1 from rice in yeast and Arabidopsis. J Exp Bot 60:3491–3502

    Article  CAS  PubMed  Google Scholar 

  • Bandyopadhyay S, Gama F, Molina-Navarro MM et al (2008) Chloroplast monothiol glutaredoxins as scaffold proteins for the assembly and delivery of [2Fe-2S] clusters. EMBO J 27:1122–1133

    Article  CAS  PubMed  Google Scholar 

  • Cheng NH (2008) AtGRX4, an Arabidopsis chloroplastic monothiol glutaredoxin, is able to suppress yeast grx5 mutant phenotypes and respond to oxidative stress. FEBS Lett 582:848–854

    Article  CAS  PubMed  Google Scholar 

  • Cheng NH, Liu JZ, Brock A, Nelson RS, Hirschi KD (2006) AtGRXcp, an Arabidopsis chloroplastic glutaredoxin, is critical for protection against protein oxidative damage. J Biol Chem 281:26280–26288

    Article  CAS  PubMed  Google Scholar 

  • Claude P, Rob G, Mike T, Philippe S (1999) In Silico cloning of a new protein kinase, Aik2, related to Drosophila aurora using the new tool: EST blast. In Silico Biol 1:123–128

    Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Couturier J, Jacquot JP, Rouhier N (2009) Evolution and diversity of glutaredoxins in photosynthetic organisms. Cell Mol Life Sci 66:2539–2557

    Article  CAS  PubMed  Google Scholar 

  • Cui XF, Li G, Wang D, Hu D, Zhou XP (2005) A begomovirus DNAbeta-encoded protein binds DNA, functions as a suppressor of RNA silencing, and targets the cell nucleus. J Virol 79:10764–10775

    Article  CAS  PubMed  Google Scholar 

  • Ding XS, Schneider WL, Chaluvadi SR, Mian MAR, Nelson RS (2006) Characterization of a brome mosaic virus strain and its use as a vector for gene silencing in monocotyledonous hosts. Mol Plant Microbe Interact 19:1229–1239

    Article  CAS  PubMed  Google Scholar 

  • Fernandes AP, Holmgren A (2004) Glutaredoxins: glutathione-dependent redox enzymes with functions far beyond a simple thioredoxin backup system. Antioxid Redox Sign 6:63–74

    Article  CAS  Google Scholar 

  • Fernandez-Falcon M, Hernandez M, Alvarez CE, Borges AA (2006) Variation in nutrition along time and relative chlorophyll content of Leucospermum cordifolium cv. ‘High Gold’, and their relationship with chlorotic sypmptoms. Sci Hortic 107:373–379

    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  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Holmgren A (1979) Glutathione-dependent synthesis of deoxyribonucleotides—purification and characterization of glutaredoxin from Escherichia coli. J Biol Chem 254:3664–3671

    CAS  PubMed  Google Scholar 

  • Holmgren A (1989) Thioredoxin and glutaredoxin systems. J Biol Chem 264:13963–13966

    CAS  PubMed  Google Scholar 

  • Huang CJ, Xie Y, Zhou XP (2009) Efficient virus-induced gene silencing in plants using a modified geminivirus DNA1 component. Plant Biotechnol J 7:254–265

    Article  CAS  PubMed  Google Scholar 

  • Jami SK, Clark GB, Turlapati SA, Handley C, Roux SJ, Kirti PB (2008) Ectopic expression of an annexin from Brassica juncea confers tolerance to abiotic and biotic stress treatments in transgenic tobacco. Plant Physiol Biochem 46:1019–1030

    Article  CAS  PubMed  Google Scholar 

  • Kang JY, Choi HI, Im MY, Kim SY (2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14:343–357

    Article  CAS  PubMed  Google Scholar 

  • Kumagai MH, Donson J, Dellacioppa G, Harvey D, Hanley K, Grill LK (1995) Cytoplasmic inhibition of carotenoid biosynthesis with virus-derived RNA. Proc Natl Acad Sci USA 92:1679–1683

    Article  CAS  PubMed  Google Scholar 

  • Li S, Lauri A, Ziemann M, Busch A, Bhave M, Zachgo S (2009) Nuclear activity of ROXY1, a glutaredoxin interacting with TGA factors, is required for petal development in Arabidopsis thaliana. Plant Cell 21:429–441

    Article  CAS  PubMed  Google Scholar 

  • Liu YL, Schiff M, Dinesh-Kumar SP (2002a) Virus-induced gene silencing in tomato. Plant J 31:777–786

    Article  CAS  PubMed  Google Scholar 

  • Liu YL, Schiff M, Marathe R, Dinesh-Kumar SP (2002b) Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus. Plant J 30:415–429

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–Δ ΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Luo HL, Song FM, Zheng Z (2005) Overexpression in transgenic tobacco reveals different roles for the rice homeodomain gene OsBIHD1 in biotic and abiotic stress responses. J Exp Bot 56:2673–2682

    Article  CAS  PubMed  Google Scholar 

  • Matsumoto T, Wu JZ, Kanamori H et al (2005) The map-based sequence of the rice genome. Nature 436:793–800

    Article  Google Scholar 

  • Meyer Y, Buchanan BB, Vignols F, Reichheld JP (2009) Thioredoxins and glutaredoxins: unifying elements in redox biology. Annu Rev Genet 43:335–367

    Article  CAS  PubMed  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2009) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  PubMed  Google Scholar 

  • Narendra S, Venkataramani S, Shen G, Wang J, Pasapula V, Lin Y, Kornyeyev D, Holaday AS, Zhang H (2006) The Arabidopsis ascorbate peroxidase 3 is a peroxisomal membrane-bound antioxidant enzyme and is dispensable for Arabidopsis growth and development. J Exp Bot 57:3033–3042

    Article  CAS  PubMed  Google Scholar 

  • Ndamukong I, Al Abdallat A, Thurow C, Fode B, Zander M, Weigel R, Gatz C (2007) SA-inducible Arabidopsis glutaredoxin interacts with TGA factors and suppresses JA-responsive PDF1.2 transcription. Plant J 50:128–139

    Article  CAS  PubMed  Google Scholar 

  • Panchuk II, Zentgraf U, Volkov RA (2005) Expression of the Apx gene family during leaf senescence of Arabidopsis thaliana. Planta 222:926–932

    Article  CAS  PubMed  Google Scholar 

  • Peele C, Jordan CV, Muangsan N, Turnage M, Egelkrout E, Eagle P, Hanley-Bowdoin L, Robertson D (2001) Silencing of a meristematic gene using geminivirus-derived vectors. Plant J 27:357–366

    Article  CAS  PubMed  Google Scholar 

  • Pitzschke A, Forzani C, Hirt H (2006) Reactive oxygen species signaling in plants. Antioxid Redox Sign 8:1757–1764

    Article  CAS  Google Scholar 

  • Purkayastha A, Dasgupta I (2009) Virus-induced gene silencing: a versatile tool for discovery of gene functions in plants. Plant Physiol Biochem 47:967–976

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Manzaneque MT, Ros J, Cabiscol E, Sorribas A, Herrero E (1999) Grx5 glutaredoxin plays a central role in protection against protein oxidative damage in Saccharomyces cerevisiae. Mol Cell Biol 19:8180–8190

    CAS  PubMed  Google Scholar 

  • Rouhier N (2010) Plant glutaredoxins: pivotal players in redox biology and iron-sulphur centre assembly. New Phytol 186:365–372

    Article  CAS  PubMed  Google Scholar 

  • Rouhier N, Gelhaye E, Jacquot JP (2004) Plant glutaredoxins: still mysterious reducing systems. Cell Mol Life Sci 61:1266–1277

    Article  CAS  PubMed  Google Scholar 

  • Rouhier N, Unno H, Bandyopadhyay S et al (2007) Functional, structural, and spectroscopic characterization of a glutathione-ligated [2Fe-2S] cluster in poplar glutaredoxin C1. Proc Natl Acad Sci USA 104:7379–7384

    Article  CAS  PubMed  Google Scholar 

  • Rouhier N, Lemaire SD, Jacquot JP (2008) The role of glutathione in photosynthetic organisms: emerging functions for glutaredoxins and glutathionylation. Annu Rev Plant Biol 59:143–166

    Article  CAS  PubMed  Google Scholar 

  • Scandalios JG (2002) The rise of ROS. Trends Biochem Sci 27:483–486

    Article  CAS  PubMed  Google Scholar 

  • Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319

    Article  CAS  PubMed  Google Scholar 

  • Sundaram S, Rathinasabapathi B (2010) Transgenic expression of fern Pteris vittata glutaredoxin PvGrx5 in Arabidopsis thaliana increases plant tolerance to high temperature stress and reduces oxidative damage to proteins. Planta 231:361–369

    Article  CAS  PubMed  Google Scholar 

  • Sundaram S, Rathinasabapathi B, Ma LQ, Rosen BP (2008) An arsenate-activated glutaredoxin from the arsenic hyperaccumulator fern Pteris vittata L regulates intracellular arsenite. J Biol Chem 283:6095–6101

    Article  CAS  PubMed  Google Scholar 

  • Sundaram S, Wu S, Ma LQ, Rathinasabapathi B (2009) Expression of a Pteris vittata glutaredoxin PvGRX5 in transgenic Arabidopsis thaliana increases plant arsenic tolerance and decreases arsenic accumulation in the leaves. Plant Cell Environ 32:851–858

    Article  CAS  PubMed  Google Scholar 

  • Tao XR, Zhou XP (2004) A modified viral satellite DNA that suppresses gene expression in plants. Plant J 38:850–860

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) Clustal-W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  Google Scholar 

  • Turner NC (1981) Techniques and experimental approaches for the measurement of plant water status. Plant Soil 58:339–366

    Article  Google Scholar 

  • Vranová E, Inzé D, Van Breusegem F (2002) Signal transduction during oxidative stress. J Exp Bot 53:1227–1236

    Article  PubMed  Google Scholar 

  • Wang Z, Xing SP, Birkenbihl RP, Zachgo S (2009) Conserved functions of Arabidopsis and rice CC-type glutaredoxins in flower development and pathogen response. Mol Plant 2:323–335

    Article  CAS  PubMed  Google Scholar 

  • Xing SP, Zachgo S (2008) ROXY1 and ROXY2, two Arabidopsis glutaredoxin genes, are required for anther development. Plant J 53:790–801

    Article  CAS  PubMed  Google Scholar 

  • Xing SP, Rosso MG, Zachgo S (2005) ROXY1, a member of the plant glutaredoxin family, is required for petal development in Arabidopsis thaliana. Development 132:1555–1565

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the Important National Science & Technology Specific Projects of China (2009ZX08009-026B), the National Key Basic Research and Development Program of China (2006CB101903) and the National High Technology Research and Development program of China (863 Program) (2007AA10Z413).

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Correspondence to Xueping Zhou.

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Guo, Y., Huang, C., Xie, Y. et al. A tomato glutaredoxin gene SlGRX1 regulates plant responses to oxidative, drought and salt stresses. Planta 232, 1499–1509 (2010). https://doi.org/10.1007/s00425-010-1271-1

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  • DOI: https://doi.org/10.1007/s00425-010-1271-1

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