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Expression of a rice glutaredoxin in aleurone layers of developing and mature seeds: subcellular localization and possible functions in antioxidant defense

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Abstract

Main Conclusion

A rice glutaredoxin isoform (OsGrxC2;2) with antioxidant capacity is expressed abundantly in seed tissues and is localized to storage vacuoles in aleurone layers in developing and mature seeds.

Seed tissues undergo drastic water loss at the late stage of seed development, and thus need to tolerate oxidative injuries associated with desiccation. We previously found a rice glutaredoxin isoform, OsGrxC2;2, as a gene expressed abundantly in developing seeds. Since glutaredoxin is involved in antioxidant defense, in the present study we investigated the subcellular localization and expression profile of OsGrxC2;2 and whether OsGrxC2;2 has a role in the defense against reactive oxygen species. Western blotting and immunohistochemistry revealed that the OsGrxC2;2 protein accumulated at a high level in the embryo and aleurone layers of developing and mature seeds. The OsGrxC2;2 in developing seeds was particularly localized to aleurone grains, which are storage organelles derived from vacuoles. Overexpression of OsGrxC2;2 resulted in an enhanced tolerance to menadione in yeast and methyl viologen in green leaves of transgenic rice plants. These results suggest that OsGrxC2;2 participates in the defense against oxidative stress in developing and mature seeds.

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Abbreviations

AsA:

Ascorbate

CaMV:

Cauliflower mosaic virus

DAF:

Days after flowering

DAI:

Days after the onset of imbibition

DHAR:

Dehydroascorbate reductase

ER:

Endoplasmic reticulum

GFP:

Green fluorescent protein

Grx:

Glutaredoxin

GSH:

Glutathione

Prx:

Peroxiredoxin

PS:

Photosystem

RFP:

Red fluorescent protein

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

Trx:

Thioredoxin

References

  • Bailly C, Audigier C, Ladonne F, Wagner MH, Coste F, Corbineau F, Côme D (2001) Changes in oligosaccharide content and antioxidant enzyme activities in developing bean seeds as related to acquisition of drying tolerance and seed quality. J Exp Bot 52:701–708

    CAS  PubMed  Google Scholar 

  • Bailly C, Leymarie J, Lehner A, Rousseau S, Côme D, Corbineau F (2004) Catalase activity and expression in developing sunflower seeds as related to drying. J Exp Bot 55:475–483

    Article  CAS  PubMed  Google Scholar 

  • Bailly C, El-Maarouf-Bouteau H, Corbineau F (2008) From intracellular signaling networks to cell death: the dual role of reactive oxygen species in seed physiology. C R Biologies 331:806–814

    Article  CAS  PubMed  Google Scholar 

  • Bandyopadhyay S, Gama F, Molina-Navarro MM, Gualberto JM, Claxton R, Naik SG, Huynh BH, Herrero E, Jacquot JP, Johnson MK, Rouhier N (2008) Chloroplast monothiol glutaredoxins as scaffold proteins for the assembly and delivery of [2Fe-2S] clusters. EMBO J 27:1122–1133

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Butt AD, Ohlrogge JB (1991) Acyl carrier protein is conjugated to glutathione in spinach seed. Plant Physiol 96:937–942

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chatre L, Brandizzi F, Hocquellet A, Hawes C, Moreau P (2005) Sec22 and Memb11 are v-SNAREs of the anterograde endoplasmic reticulum-Golgi pathway in tobacco leaf epidermal cells. Plant Physiol 139:1244–1254

    Article  PubMed Central  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 

  • Chiu W, Niwa Y, Zeng W, Hirano T, Kobayashi H, Sheen J (1996) Engineered GFP as a vital reporter in plants. Curr Biol 6:325–330

    Article  CAS  PubMed  Google Scholar 

  • Colville L, Kranner I (2010) Desiccation tolerant plants as model systems to study redox regulation of protein thiols. Plant Growth Regul 62:241–255

    Article  CAS  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 

  • De Gara L, de Pinto MC, Moliterni VMC, D’Egidio MG (2003) Redox regulation and storage processes during maturation in kernels of Triticum durum. J Exp Bot 54:249–258

    Article  PubMed  Google Scholar 

  • Dietz K-J, Jacob S, Oelze M-L, Laxa M, Tognetti V, de Miranda SMN, Baier M, Finkemeier I (2006) The function of peroxiredoxins in plant organelle redox metabolism. J Exp Bot 57:1697–1709

    Article  CAS  PubMed  Google Scholar 

  • El-Maarouf-Bouteau H, Bailly C (2008) Oxidative signaling in seed germination and dormancy. Plant Signal Behav 3:175–182

    Article  PubMed Central  PubMed  Google Scholar 

  • Garg R, Jhanwar S, Tyagi AK, Jain M (2010) Genome-wide survey and expression analysis suggest diverse roles of glutaredoxin gene family members during development and response to various stimuli in rice. DNA Res 17:353–367

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Hossain MA, Asada K (1984) Purification of dehydroascorbate reductase from spinach and its characterization as a thiol enzyme. Plant Cell Physiol 25:85–92

    CAS  Google Scholar 

  • Laporte D, Olate E, Salinas P, Salazar M, Jordana X, Holuigue L (2012) Glutaredoxin GRXS13 plays a key role in protection against photooxidative stress in Arabidopsis. J Exp Bot 63:503–515

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lee KO, Lee JR, Yoo JY, Jang HH, Moon JC, Jung BG, Chi YH, Park SK, Lee SS, Lim CO, Yun DJ, Cho MJ, Lee SY (2002) GSH-dependent peroxidase activity of the rice (Oryza sativa) glutaredoxin, a thioltransferase. Biochem Biophys Res Commun 296:1152–1156

    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  PubMed Central  CAS  PubMed  Google Scholar 

  • Luikenhuis S, Perrone G, Dawes IW, Grant CM (1998) The yeast Saccharomyces cerevisiae contains two glutaredoxin genes that are required for protection against reactive oxygen species. Mol Biol Cell 9:1081–1091

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Marty F (1999) Plant vacuoles. Plant Cell 11:587–600

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Minakuchi K, Yabushita T, Masumura T, Ichihara K, Tanaka K (1994) Cloning and sequence analysis of a cDNA encoding rice glutaredoxin. FEBS Lett 337:157–160

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  CAS  PubMed  Google Scholar 

  • Morita S, Nakatani S, Koshiba T, Masumura T, Ogihara Y, Tanaka K (2011) Differential expression of two cytosolic ascorbate peroxidase and two superoxide dismutase genes in response to abiotic stresses in rice. Rice Sci 18:157–166

    Article  Google Scholar 

  • Morita S, Tsukamoto S, Sakamoto A, Makino H, Nakauji E, Kaminaka H, Masumura T, Ogihara Y, Satoh S, Tanaka K (2012) Differences in intron-mediated enhancement of gene expression by the first intron of cytosolic superoxide dismutase gene from rice in monocot and dicot plants. Plant Biotechnol 29:115–119

    Article  CAS  Google Scholar 

  • Ndamukong I, Abdallat AA, 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 

  • Ohta S, Mita S, Hattori T, Nakamura K (1990) Construction and expression in tobacco of a β-glucuronidase (GUS) reporter gene containing an intron within the coding sequence. Plant Cell Physiol 31:805–813

    CAS  Google Scholar 

  • Pulido P, Cazalis R, Cejudo FJ (2009) An antioxidant redox system in the nucleus of wheat seed cells suffering oxidative stress. Plant J 57:132–145

    Article  CAS  PubMed  Google Scholar 

  • Puntarulo S, Galleano M, Sanchez RA, Boveris A (1991) Superoxide anion and hydrogen peroxide metabolism in soybean embryonic axes during germination. Biochim Biophys Acta 1074:277–283

    Article  CAS  PubMed  Google Scholar 

  • Rhazi L, Cazalis R, Lemelin E, Aussenac T (2003) Changes in the glutathione thiol-disulfide status during wheat grain development. Plant Physiol Biochem 41:895–902

    Article  CAS  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

    PubMed Central  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, Sautiere PE, Brun A, Laurent P, Tagu D, Gerard J, de Fay E, Meyer Y, Jacquot JP (2001) Isolation and characterization of a new peroxiredoxin from poplar sieve tubes that uses either glutaredoxin or thioredoxin as a proton donor. Plant Physiol 127:1299–1309

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rouhier N, Couturier J, Jacquot JP (2006) Genome-wide analysis of plant glutaredoxin systems. J Exp Bot 57:1685–1696

    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 

  • Saito Y, Kishida K, Takata K, Takahashi H, Shimada T, Tanaka K, Morita S, Satoh S, Masumura T (2009) A green fluorescent protein fused to rice prolamin forms protein body-like structures in transgenic rice. J Exp Bot 60:615–627

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Serrato AJ, Cejudo FJ (2003) Type-h thioredoxins accumulate in the nucleus of developing wheat seed tissues suffering oxidative stress. Planta 217:392–399

    Article  CAS  PubMed  Google Scholar 

  • Sha S, Minakuchi K, Higaki N, Sato K, Ohtsuki K, Kurata A, Yoshikawa H, Kotaru M, Masumura T, Ichihara K, Tanaka K (1997) Purification and characterization of glutaredoxin (thioltransferase) from rice (Oryza sativa L.). J Biochem 121:842–848

    Article  CAS  PubMed  Google Scholar 

  • Stacy RA, Munthe E, Steinum T, Sharma B, Aalen RB (1996) A peroxiredoxin antioxidant is encoded by a dormancy-related gene, Per1, expressed during late development in the aleurone and embryo of barley grains. Plant Mol Biol 31:1205–1216

    Article  CAS  PubMed  Google Scholar 

  • Stacy RA, Nordeng TW, Culianez-Macia FA, Aalen RB (1999) The dormancy-related peroxiredoxin anti-oxidant, PER1, is localized to the nucleus of barley embryo and aleurone cells. Plant J 19:1–8

    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, 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 

  • Tanaka K, Kasai Z, Ogawa M (1995) Physiology of ripening. In: Matsuo T, Kumazawa K, Ishii R, Ishihara K, Hirata H (eds) Science of the rice plant. Physiology, vol 2. Food and Agriculture Policy Research Center, Tokyo, pp 97–118

    Google Scholar 

  • Tarrago L, Laugier E, Zaffagnini M, Marchand C, Le Marechal P, Rouhier N, Lemaire SD, Rey P (2009) Regeneration mechanisms of Arabidopsis thaliana methionine sulfoxide reductases B by glutaredoxins and thioredoxins. J Biol Chem 284:18963–18971

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Toki S (1997) Rapid and efficient Agrobacterium-mediated transformation in rice. Plant Mol Biol Rep 15:16–21

    Article  CAS  Google Scholar 

  • Tsukamoto S, Morita S, Hirano E, Yokoi H, Masumura T, Tanaka K (2005) A novel cis-element that is responsive to oxidative stress regulates three antioxidant defense genes in rice. Plant Physiol 137:317–327

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Uemura T, Ueda T, Ohniwa RL, Nakano A, Takeyasu K, Sato MH (2004) Systematic analysis of SNARE molecules in Arabidopsis: dissection of the post-Golgi network in plant cells. Cell Struct Funct 29:49–65

    Article  CAS  PubMed  Google Scholar 

  • Vitale A, Hinz G (2005) Sorting of proteins to storage vacuoles: how many mechanisms? Trends Plant Sci 10:316–323

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Xiao Y, Chen W, Tang K, Zhang L (2010) Increased vitamin C content accompanied by an enhanced recycling pathway confers oxidative stress tolerance in Arabidopsis. J Integr Plant Biol 52:400–409

    Article  CAS  PubMed  Google Scholar 

  • Wells WW, Xu DP, Yang Y, Rocque PA (1990) Mammalian thioltransferase (glutaredoxin) and protein disulfide isomerase have dehydroascorbate reductase activity. J Biol Chem 265:15361–15364

    CAS  PubMed  Google Scholar 

  • Xing S, 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 

  • Yin L, Wang S, Eltayeb A, Uddin MI, Yamamoto Y, Tsuji W, Takeuchi Y, Tanaka K (2010) Overexpression of dehydroascorbate reductase, but not monodehydroascorbate reductase, confers tolerance to aluminum stress in transgenic tobacco. Planta 231:609–621

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science (grant no. 18780078 to S.M.), and by a grant from The Tojuro Iijima Foundation for Food Science and Technology (to S.M).

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Correspondence to Shigeto Morita.

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Morita, S., Yamashita, Y., Fujiki, M. et al. Expression of a rice glutaredoxin in aleurone layers of developing and mature seeds: subcellular localization and possible functions in antioxidant defense. Planta 242, 1195–1206 (2015). https://doi.org/10.1007/s00425-015-2354-9

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