Thiol synthetases of legumes: Immunogold localization and differential gene regulation by phytohormones

Journal of Experimental Botany

Volumn 63, Issue 10, 2012, Pages 3923-3934

  Clemente, Maria R ^a   Bustos Sanmamed, Pilar ^a   Loscos, Jorge ^a   James, Euan K ^b   Pérez Rontomé, Carmen ^a   Navascués, Joaquín ^a   Gay, Marina ^c   Becana, Manuel ^a  

^a CSIC   (Spain)

^b SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^c INST D INVESTIGACIONS B   (Spain)

Author keywords

Glutamylcysteine synthetase; (homo)glutathione synthetase; immunogold localization; legumes; phytohormones; plant stress

Indexed keywords

LIGASE; PHYTOHORMONE; THIOL DERIVATIVE; VEGETABLE PROTEIN;

ARTICLE; CHEMISTRY; ENZYMOLOGY; FABACEAE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; PLANT ROOT; PROTEIN TRANSPORT;

FABACEAE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; IMMUNOHISTOCHEMISTRY; LIGASES; PLANT GROWTH REGULATORS; PLANT PROTEINS; PLANT ROOTS; PROTEIN TRANSPORT; SULFHYDRYL COMPOUNDS;

LOTUS CORNICULATUS VAR. JAPONICUS;

EID: 84863664222     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ers083     Document Type: Article

References (49)

1. Balbi V, Devoto A. 2008. Jasmonate signalling network in Arabidopsis thaliana: crucial regulatory nodes and new physiological scenarios. The New Phytologist 177, 301-318.
2. Balmer Y, Vensel WH, DuPont FM, Buchanan BB, Hurkman WJ. 2006. Proteome of amyloplasts isolated from developing wheat endosperm presents evidence of broad metabolic capability. Journal of Experimental Botany 57, 1591-1602.
3. Beckers GJM, Spoel SH. 2006. Fine-tuning plant defence signalling: salicylate versus jasmonate. Plant Biology 8, 1-10.
4. Bergmann L, Rennenberg H. 1993. Glutathione metabolism in plants. In: LJ De Kok, I Stulen, H Rennenberg, C Brunold, WE Rauser, eds, Sulfur nutrition and assimilation in higher plants. The Netherlands: SPB Academic Publishing, 109-123.
5. Boisson-Dernier A, Chabaud M, Garcia F, Bé card G, Rosenberg C, Barker DG. 2001. Hairy roots of Medicago truncatula as tools for studying nitrogen-fixing and endomycorrhizal symbioses. Molecular Plant-Microbe Interactions 14, 693-700.
6. Bouchereau A, Aziz A, Larher F, Martin-Tanguy J. 1999. Polyamines and environmental challenges: recent development. Plant Science 140, 103-125.
7. Broughton WJ, Dilworth MJ. 1971. Control of leghaemoglobin synthesis in snake beans. The Biochemical Journal 125, 1075-1080.
8. Dello Ioio R, Scaglia Linhares F, Sabatini S. 2008. Emerging role of cytokinin as a regulator of cellular differentiation. Current Opinion in Plant Biology 11, 23-27.
9. Ding Y, Kalo P, Yendrek C, Sun J, Liang Y, Marsh JF, Harris JM, Oldroyd GED. 2008. Abscisic acid coordinates Nod factor and cytokinin signaling during the regulation of nodulation in Medicago truncatula. The Plant Cell 20, 2681-2695.
10. Foyer CH, Noctor G. 2011. Ascorbate and glutathione: the heart of the redox hub. Plant Physiology 155, 2-18.
11. Frendo P, Hernández-Jimé nez MJ, Mathieu C, Duret L, Gallesi D, Van de Sype G, Hé rouart D, Puppo A. 2001. A Medicago truncatula homoglutathione synthetase is derived from glutathione synthetase by gene duplication. Plant Physiology 126, 1706-1715.
12. Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K. 2006. Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signalling networks. Current Opinion in Plant Biology 9, 436-442.
13. González-Rizzo S, Crespi M, Frugier F. 2006. The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. The Plant Cell 18, 2680-2693.
14. Gromes R, Hothorn M, Lenherr ED, Rybin V, Scheffzek K, Rausch T. 2008. The redox switch of c-glutamylcysteine ligase via a reversible monomer-dimer transition is a mechanism unique to plants. The Plant Journal 54, 1063-1075.
15. Hell R, Bergmann L. 1988. Glutathione synthetase in tobacco suspension cultures: catalytic properties and localization. Physiologia Plantarum 72, 70-76.
16. Hell R, Bergmann L. 1990. c-Glutamylcysteine synthetase in higher plants: catalytic properties and subcellular localization. Planta 180, 603-612.
17. Hicks LM, Cahoon RE, Bonner ER, Rivard RS, Sheffield J, Jez JM. 2007. Thiol-based regulation of redox-active glutamate-cysteine ligase from Arabidopsis thaliana. The Plant Cell 19, 2653-2661.
18. Innocenti G, Pucciariello C, Le Gleuher M, Hopkins J, de Stefano M, Delledonne M, Puppo A, Baudouin E, Frendo P. 2007. Glutathione synthesis is regulated by nitric oxide in Medicago truncatula roots. Planta 225, 1597-1602.
19. Iturbe-Ormaexte I, Heras B, Matamoros MA, Ramos J, Moran JF, Becana M. 2002. Cloning and functional characterization of a homoglutathione synthetase from pea nodules. Physiologia Plantarum 115, 69-73.
20. James EK, Iannetta PPM, Nixon PJ, Whiston AJ, Peat L, Crawford RMM, Sprent JI, Brewin NJ. 1996. Photosystem II and oxygen regulation in Sesbania rostrata stem nodules. Plant, Cell and Environment 19, 895-910.
21. Jez JM, Cahoon RE. 2004. Kinetic mechanism of glutathione synthetase from Arabidopsis thaliana. Journal of Biological Chemistry 279, 42726-42731.
22. Klapheck S, Zopes H, Levels HG, Bergmann L. 1988. Properties and localization of the homoglutathione synthetase from Phaseolus coccineus leaves. Physiologia Plantarum 74, 733-739.
23. Loscos J, Matamoros MA, Becana M. 2008. Ascorbate and homoglutathione metabolism in common bean nodules under stress conditions and during natural senescence. Plant Physiology 146, 1282-1292.
24. Macnicol PM. 1987. Homoglutathione and glutathione synthetases of legume seedlings: partial purification and substrate specificity. Plant Science 53, 229-235.
25. Matamoros MA, Moran JF, Iturbe-Ormaetxe I, Rubio MC, Becana M. 1999. Glutathione and homoglutathione synthesis in legume root nodules. Plant Physiology 121, 879-888.
26. Matamoros MA, Clemente MR, Sato S, Asamizu E, Tabata S, Ramos J, Moran JF, Stiller J, Gresshoff PM, Becana M. 2003. Molecular analysis of the pathway for the synthesis of thiol tripeptides in the model legume Lotus japonicus. Molecular Plant-Microbe Interactions 16, 1039-1046.
27. Maughan S, Foyer CH. 2006. Engineering and genetic approaches to modulating glutathione network in plants. Physiologia Plantarum 126, 382-397.
28. May MJ, Vernoux T, Sánchez-Fernández R, Van Montagu M, Inzé D. 1998. Evidence for posttranscriptional activation of c-glutamylcysteine synthetase during plant stress responses. Proceedings of the National Academy of Sciences, USA 95, 12049-12054.
29. Meister A. 1994. Glutathione-ascorbic acid antioxidant system in animals. Journal of Biological Chemistry 269, 9397-9400.
30. Moran JF, Iturbe-Ormaetxe I, Matamoros MA, Rubio MC, Clemente MR, Brewin NJ, Becana M. 2000. Glutathione and homoglutathione synthetases of legume nodules. Cloning, expression, and subcellular localization. Plant Physiology 124, 1381-1392.
31. Naya L, Ladrera R, Ramos J, González EM, Arrese-Igor C, Minchin FR, Becana M. 2007. The response of carbon metabolism and antioxidant defenses of alfalfa nodules to drought stress and to the subsequent recovery of plants. Plant Physiology 144, 1104-1114.
32. Neill SJ, Desikan R, Hancock JT. 2003. Nitric oxide signalling in plants. The New Phytologist 159, 11-35.
33. Pasternak M, Lim B, Wirtz M, Hell R, Cobbett CS, Meyer AJ. 2008. Restricting glutathione biosynthesis to the cytosol is sufficient for normal plant development. The Plant Journal 53, 999-1012.
34. Pucciariello C, Innocenti G, Van de Velde W, et al. 2009. (Homo)glutathione depletion modulates host gene expression during the symbiotic interaction between Medicago truncatula and Sinorhizobium meliloti. Plant Physiology 151, 1186-1196.
35. Ramos J, Matamoros MA, Naya L, James EK, Rouhier N, Sato S, Tabata S, Becana M. 2009. The glutathione peroxidase gene family of Lotus japonicus: characterization of genomic clones, expression analyses and immunolocalization in legumes. The New Phytologist 181, 103-114.
36. Riggs P. 2000. Expression and purification of recombinant proteins by fusion to maltose-binding protein. Molecular Biotechnology 15, 51-63.
37. Rubio MC, Becana M, Kanematsu S, Ushimaru T, James EK. 2009. Immunolocalization of antioxidant enzymes in high-pressure frozen root and stem nodules of Sesbania rostrata. The New Phytologist 183, 395-407.
38. Schäfer HJ, Haag-Kerwer A, Rausch T. 1998. cDNA cloning and expression analysis of genes encoding GSH synthesis in roots of the heavy-metal accumulator Brassica juncea L.: evidence for Cdinduction of a putative mitochondrial c-glutamylcysteine synthetase isoform. Plant Molecular Biology 37, 87-97.
39. Stacey G, McAlvin CB, Kim SY, Olivares J, Soto MJ. 2006. Effects of endogenous salicylic acid on nodulation in the model legumes Lotus japonicus and Medicago truncatula. Plant Physiology 141, 1473-1481.
40. Sun J, Cardoza V, Mitchell DM, Bright L, Oldroyd G, Harris JM. 2006. Crosstalk between jasmonic acid, ethylene and Nod factor signalling allows integration of diverse inputs for regulation of nodulation. The Plant Journal 46, 961-970.
41. Theiss C, Bohley P, Voigt J. 2002. Regulation by polyamines of ornithine decarboxylase activity and cell division in the unicellular green alga Chlamydomonas reinhardtii. Plant Physiology 128, 1470-1479.
42. Tirichine L, Sandal N, Madsen LH, Radutoiu S, Albrektsen AS, Sato S, Asamizu E, Tabata S, Stougaard J. 2007. A gain-offunction mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 315, 104-107.
43. Tominaga A, Nagata M, Futsuki K, et al. 2009. Enhanced nodulation and nitrogen fixation in the abscisic acid low-sensitive mutant enhanced nitrogen fixation1 of Lotus japonicus. Plant Physiology 151, 1965-1976.
44. Tun NN, Santa-Catarina C, Begum T, Silveira V, Handro W, Segal Floh EI, Scherer GFE. 2006. Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant and Cell Physiology 47, 346-354.
45. Wachter A, Wolf S, Steininger H, Bogs J, Rausch T. 2005. Differential targeting of GSH1 and GSH2 is achieved by multiple transcription initiation: implications for the compartmentation of glutathione biosynthesis in the Brassicaceae. The Plant Journal 41, 15-30.
46. Wild AC, Mulcahy RT. 2000. Regulation of c-glutamylcysteine synthetase subunit gene expression: insights into transcriptional control of antioxidant defenses. Free Radical Research 32, 281-301.
47. Wingate VPM, Lawton MA, Lamb CJ. 1988. Glutathione causes a massive and selective induction of plant defense genes. Plant Physiology 87, 206-210.
48. Xiang C, Oliver DJ. 1998. Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. The Plant Cell 10, 1539-1550.
49. Yamasaki H, Cohen MF. 2006. NO signal at the crossroads: polyamine-induced nitric oxide synthesis in plants? Trends in Plant Science 11, 522-524.