Identification and characterization of thioredoxin h isoforms differentially expressed in germinating seeds of the model legume Medicago truncatula

Plant Physiology

Volumn 155, Issue 3, 2011, Pages 1113-1126

  Renard, Michelle ^a   Alkhalfioui, Fatima ^a,b   Schmitt Keichinger, Corinne ^b   Ritzenthaler, Christophe ^b   Montrichard, Françoise ^a  

^a CEMAGREF   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MEDICAGO TRUNCATULA;

EID: 79952290450     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.110.170712     Document Type: Article

References (81)

1. Alkhalfioui F, Renard M, Frendo P, Keichinger C, Meyer Y, Gelhaye E, Hirasawa M, Knaff DB, Ritzenthaler C, Montrichard F (2008) A novel type of thioredoxin dedicated to symbiosis in legumes. Plant Physiol 148: 424-435.
2. Alkhalfioui F, Renard M, Montrichard F (2007a) Unique properties of NADP-thioredoxin reductase C in legumes. J Exp Bot 58: 969-978.
3. Alkhalfioui F, Renard M, Vensel WH, Wong JH, Tanaka CK, Hurkman WJ, Buchanan BB, Montrichard F (2007b) Thioredoxin-linked proteins are reduced during germination of Medicago truncatula seeds. Plant Physiol 144: 1559-1579.
4. Arsova B, Hoja U, Wimmelbacher M, Greiner E, Ustün S, Melzer M, Petersen K, Lein W, Börnke F (2010) Plastidial thioredoxin z interacts with two fructokinase-like proteins in a thiol-dependent manner: evidence for an essential role in chloroplast development in Arabidopsis and Nicotiana benthamiana. Plant Cell 22: 1498-1515.
5. Bailly C (2004) Active oxygen species and antioxidants in seed biology. Seed Sci Res 14: 93-107.
6. Balmer Y, Vensel WH, Cai N, Manieri W, Schürmann P, Hurkman WJ, Buchanan BB (2006) A complete ferredoxin/thioredoxin system regulates fundamental processes in amyloplasts. Proc Natl Acad Sci USA 103: 2988-2993.
7. Besse I, Wong JH, Kobrehel K, Buchanan BB (1996) Thiocalsin: a thioredoxin- linked, substrate-specific protease dependent on calcium. Proc Natl Acad Sci USA 93: 3169-3175.
8. Bønsager BC, Finnie C, Roepstorff P, Svensson B (2007) Spatio-temporal changes in germination and radical elongation of barley seeds tracked by proteome analysis of dissected embryo, aleurone layer, and endosperm tissues. Proteomics 7: 4528-4540.
9. Boursiac Y, Chen S, Luu DT, Sorieul M, van den Dries N,Maurel C (2005) Early effects of salinity on water transport in Arabidopsis roots: molecular and cellular features of aquaporin expression. Plant Physiol 139: 790-805.
10. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
11. Buchanan BB (1991) Regulation of CO2 assimilation in oxygenic photosynthesis: the ferredoxin/thioredoxin system. Perspective on its discovery, present status, and future development. Arch Biochem Biophys 288: 1-9.
12. Buchanan BB, Balmer Y (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol 56: 187-220.
13. Cazalis R, Pulido P, Aussenac T, Pérez-Ruiz JM, Cejudo FJ (2006) Cloning and characterization of three thioredoxin h isoforms from wheat showing differential expression in seeds. J Exp Bot 57: 2165-2172.
14. Cho MJ, Wong JH, Marx C, Jiang W, Lemaux PG, Buchanan BB (1999) Overexpression of thioredoxin h leads to enhanced activity of starch debranching enzyme (pullulanase) in barley grain. Proc Natl Acad Sci USA 96: 14641-14646.
15. Collin V, Issakidis-Bourguet E, Marchand C, Hirasawa M, Lancelin JM, Knaff DB, Miginiac-Maslow M (2003) The Arabidopsis plastidial thioredoxins: new functions and new insights into specificity. J Biol Chem 278: 23747-23752.
16. Collin V, Lamkemeyer P, Miginiac-Maslow M, Hirasawa M, Knaff DB, Dietz KJ, Issakidis-Bourguet E (2004) Characterization of plastidial thioredoxins from Arabidopsis belonging to the new y-type. Plant Physiol 136: 4088-4095.
17. de Dios Barajas-López J, Serrato AJ, Olmedilla A, Chueca A, Sahrawy M, (2007) Localization in roots and flowers of pea chloroplastic thioredoxin f and thioredoxin m proteins reveals new roles in nonphotosynthetic organs. Plant Physiol 145: 946-960.
18. Duval FD, Renard M, Jaquinod M, Biou V, Montrichard F, Macherel D (2002) Differential expression and functional analysis of three calmodulin isoforms in germinating pea (Pisum sativum L.) seeds. Plant J 32: 481-493.
19. Gautier MF, Lullien-Pellerin V, de Lamotte-Guéry F, Guirao A, Joudrier P, (1998) Characterization of wheat thioredoxin h cDNA and production of an active Triticum aestivum protein in Escherichia coli. Eur J Biochem 252: 314-324.
20. Gelhaye E, Rouhier N, Gérard J, Jolivet Y, Gualberto J, Navrot N, Ohlsson PI, Wingsle G, Hirasawa M, Knaff DB, et al (2004a) A specific form of thioredoxin h occurs in plant mitochondria and regulates the alternative oxidase. Proc Natl Acad Sci USA 101: 14545-14550.
21. Gelhaye E, Rouhier N, Jacquot JP (2004b) The thioredoxin h system of higher plants. Plant Physiol Biochem 42: 265-271.
22. Gelhaye E, Rouhier N, Jacquot JP (2003a) Evidence for a subgroup of thioredoxin h that requires GSH/Grx for its reduction. FEBS Lett 555: 443-448.
23. Gelhaye E, Rouhier N, Laurent P, Sautiére PE, Martin F, Jacquot JP, (2002) Isolation and characterization of an extended thioredoxin h from poplar. Physiol Plant 114: 165-171.
24. Gelhaye E, Rouhier N, Vlamis-Gardikas A, Girardet JM, Sautiere PE, Sayzet M, Martin F, Jacquot JP (2003b) Identification and characterization of a third thioredoxin h in poplar. Plant Physiol Biochem 41: 629-635.
25. Guo HX, Yin J, Ren JP, Wang ZY, Chen HL (2007) Changes in proteinswithin germinating seeds of transgenic wheat with an antisense construct directed against the thioredoxin. Zhi Wu Sheng Li Yu Fen Zi Sheng Wu Xue Xue Bao 33: 18-24.
26. Hägglund P, Bunkenborg J, Maeda K, Svensson B, (2008) Identification of thioredoxin disulfide targets using a quantitative proteomics approach based on isotope-coded affinity tags. J Proteome Res 7: 5270-5276.
27. Holmgren A (1979) Thioredoxin catalyzes the reduction of insulin disulfides by dithiothreitol and dihydrolipoamide. J Biol Chem 254: 9627-9632.
28. Holmgren A (1985) Thioredoxin. Annu Rev Biochem 54: 237-271.
29. Ishiwatari Y, Fujiwara T, McFarland KC, Nemoto K, Hayashi H, Chino M, Lucas WJ (1998) Rice phloem thioredoxin h has the capacity to mediate its own cell-to-cell transport through plasmodesmata. Planta 205: 12-22.
30. Ishiwatari Y, Honda C, Kawashima I, Nakamura S, Hirano H, Mori S, Fujiwara T, Hayashi H, Chino M (1995) Thioredoxin h is one of the major proteins in rice phloem sap. Planta 195: 456-463.
31. Jacquot JP, Issakidis E, Decottignies P, Lemaire M, Miginiac-Maslow M (1995) Analysis and manipulation of target enzymes for thioredoxin control. Methods Enzymol 252: 240-252.
32. Jiao J, Yee BC, Wong JH, Kobrehel K, Buchanan BB (1993) Thioredoxinlinked changes in regulatory properties of barley a-amylase/subtilisin inhibitor protein. Plant Physiol Biochem 31: 799-804.
33. Jiao JA, Yee BC, Kobrehel K, Buchanan BB (1992) Effect of thioredoxinlinked reduction on the activity and stability of the Kunitz and Bowman- Birk soybean inhibitor proteins. J Agric Food Chem 40: 2333-2336.
34. Juárez-Diáz JA, McClure B, Vázquez-Santana S, Guevara-Garciá A, León-Mejiá P, Márquez-Guzmán J, Cruz-Garciá F, (2006) A novel thioredoxin h is secreted in Nicotiana alata and reduces S-RNase in vitro. J Biol Chem 281: 3418-3424.
35. Juttner J, Olde D, Langridge P, Baumann U (2000) Cloning and expression of a distinct subclass of plant thioredoxins. Eur J Biochem267: 7109-7117.
36. Kobrehel K, Wong JH, Balogh A, Kiss F, Yee BC, Buchanan BB (1992) Specific reduction of wheat storage proteins by thioredoxin h. Plant Physiol 99: 919-924.
37. Kobrehel K, Yee BC, Buchanan BB (1991) Role of the NADP/thioredoxin system in the reduction of a-amylase and trypsin inhibitor proteins. J Biol Chem 266: 16135-16140.
38. Koh CS, Navrot N, Didierjean C, Rouhier N, Hirasawa M, Knaff DB, Wingsle G, Samian R, Jacquot JP, Corbier C, et al (2008) An atypical catalytic mechanism involving three cysteines of thioredoxin. J Biol Chem 283: 23062-23072.
39. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
40. Laloi C, Mestres-Ortega D, Marco Y, Meyer Y, Reichheld JP (2004) The Arabidopsis cytosolic thioredoxin h5 gene induction by oxidative stress and its W-box-mediated response to pathogen elicitor. Plant Physiol 134: 1006-1016.
41. Laurent TC, Moore EC, Reichard P (1964) Enzymatic synthesis of deoxyribonucleotides: isolation and characterization of thioredoxin, the hydrogen donor from Escherichia coli B. J Biol Chem 239: 3436-3444.
42. Lee MY, Shin KH, Kim YK, Suh JY, Gu YY, Kim MR, Hur YS, Son O, Kim JS, Song E, et al (2005) Induction of thioredoxin is required for nodule development to reduce reactive oxygen species levels in soybean roots. Plant Physiol 139: 1881-1889.
43. Lemaire SD, Collin V, Keryer E, Issakidis-Bourguet E, Lavergne D, Miginiac-Maslow M (2003a) Chlamydomonas reinhardtii: amodel organism for the study of the thioredoxin family. Plant Physiol Biochem 41: 513-521.
44. Lemaire SD, Collin V, Keryer E, Quesada A, Miginiac-Maslow M (2003b) Characterization of thioredoxin y, a new type of thioredoxin identified in the genome of Chlamydomonas reinhardtii. FEBS Lett 543: 87-92.
45. Li YC, Ren JP, Cho MJ, Zhou SM, Kim YB, Guo HX, Wong JH, Niu HB, Kim HK, Morigasaki S, et al (2009) The level of expression of thioredoxin is linked to fundamental properties and applications of wheat seeds. Mol Plant 2: 430-441.
46. Lozano RM,Wong JH, Yee BC, Peters A, Kobrehel K, Buchanan BB (1996) New evidence for a role for thioredoxin h in germination and seedling development. Planta 200: 100-106.
47. Maeda K, Finnie C, ØStergaard O, Svensson B (2003) Identification, cloning and characterization of two thioredoxin h isoforms, HvTrxh1 and HvTrxh2, from the barley seed proteome. Eur J Biochem 270: 2633-2643.
48. Maeda K, Finnie C, Svensson B (2004) Cy5 maleimide labelling for sensitive detection of free thiols in native protein extracts: identification of seed proteins targeted by barley thioredoxin h isoforms. Biochem J 378: 497-507.
49. Marx C, Wong JH, Buchanan BB (2003) Thioredoxin and germinating barley: targets and protein redox changes. Planta 216: 454-460.
50. Meng L, Wong JH, Feldman LJ, Lemaux PG, Buchanan BB (2010) A membrane-associated thioredoxin required for plant growth moves from cell to cell, suggestive of a role in intercellular communication. Proc Natl Acad Sci USA 107: 3900-3905.
51. Mestres-Ortega D, Meyer Y (1999) The Arabidopsis thaliana genome encodes at least four thioredoxins m and a new prokaryotic-like thioredoxin. Gene 240: 307-316.
52. Meyer Y, Reichheld JP, Vignols F (2005) Thioredoxins in Arabidopsis and other plants. Photosynth Res 86: 419-433.
53. Meyer Y, Riondet CC, Constans L, Abdelgawwad MR, Reichheld JP, Vignols F (2006) Evolution of redoxin genes in the green lineage. Photosynth Res 89: 179-192.
54. Meyer Y, Vignols F, Reichheld JP (2002) Classification of plant thioredoxins by sequence similarity and intron position. Methods Enzymol 347: 394-402.
55. Montrichard F, Alkhalfioui F, Yano H, Vensel WH, Hurkman WJ, Buchanan BB (2009) Thioredoxin targets in plants: the first 30 years. J Proteomics 72: 452-474.
56. Montrichard F, Renard M, Alkhalfioui F, Duval FD, Macherel D (2003) Identification and differential expression of two thioredoxin h isoforms in germinating seeds from pea. Plant Physiol 132: 1707-1715.
57. Mouaheb N, Thomas D, Verdoucq L, Monfort P, Meyer Y (1998) In vivo functional discrimination between plant thioredoxins by heterologous expression in the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci USA 95: 3312-3317.
58. Navrot N, Collin V, Gualberto J, Gelhaye E, Hirasawa M, Rey P, Knaff DB, Issakidis E, Jacquot JP, Rouhier N (2006) Plant glutathione peroxidases are functional peroxiredoxins distributed in several subcellular compartments and regulated during biotic and abiotic stresses. Plant Physiol 142: 1364-1379.
59. 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.
60. Reichheld JP, Khafif M, Riondet C, Droux M, Bonnard G, Meyer Y (2007) Inactivation of thioredoxin reductases reveals a complex interplay between thioredoxin and glutathione pathways in Arabidopsis development. Plant Cell 19: 1851-1865.
61. Reichheld JP, Meyer E, Khafif M, Bonnard G, Meyer Y (2005) AtNTRB is the major mitochondrial thioredoxin reductase in Arabidopsis thaliana. FEBS Lett 579: 337-342.
62. Rivas S, Rougon-Cardoso A, Smoker M, Schauser L, Yoshioka H, Jones JD (2004) CITRX thioredoxin interacts with the tomato Cf-9 resistance protein and negatively regulates defence. EMBO J 23: 2156-2165.
63. Rivera-Madrid R, Mestres D, Marinho P, Jacquot JP, Decottignies P, Miginiac-Maslow M, Meyer Y (1995) Evidence for five divergent thioredoxin h sequences in Arabidopsis thaliana. Proc Natl Acad Sci USA 92: 5620-5624.
64. Schobert C, Baker L, Szederkenyi J, Grossmann P, Komor E, Hayashi H, Chino M, Lucas WJ (1998) Identification of immunologically related proteins in sieve-tube exudate collected from monocotyledonous and dicotyledonous plants. Planta 206: 245-252.
65. Serrato AJ, Cejudo FJ (2003) Type-h thioredoxins accumulate in the nucleus of developing wheat seed tissues suffering oxidative stress. Planta 217: 392-399.
66. Serrato AJ, Crespo JL, Florencio FJ, Cejudo FJ (2001) Characterization of two thioredoxins h with predominant localization in the nucleus of aleurone and scutellum cells of germinating wheat seeds. PlantMol Biol 46: 361-371.
67. Serrato AJ, Guilleminot J, Meyer Y, Vignols F (2008) AtCXXS: atypical members of the Arabidopsis thaliana thioredoxin h family with a remarkably high disulfide isomerase activity. Physiol Plant 133: 611-622.
68. Serrato AJ, Préz-Ruiz JM, Cejudo FJ (2002) Cloning of thioredoxin h reductase and characterization of the thioredoxin reductase-thioredoxin h system from wheat. Biochem J 367: 491-497.
69. Shahpiri A, Svensson B, Finnie C (2008) The NADPH-dependent thioredoxin reductase/thioredoxin system in germinating barley seeds: gene expression, protein profiles, and interactions between isoforms of thioredoxin h and thioredoxin reductase. Plant Physiol 146: 789-799.
70. Shi J, Bhattacharyya MK (1996) A novel plasma membrane-bound thioredoxin from soybean. Plant Mol Biol 32: 653-662.
71. Traverso JA, Vignols F, Cazalis R, Pulido A, Sahrawy M, Cejudo FJ, Meyer Y, Chueca A (2007) PsTRXh1 and PsTRXh2 are both pea h-type thioredoxins with antagonistic behavior in redox imbalances. Plant Physiol 143: 300-311.
72. Vignols F, Bréhélin C, Surdin-Kerjan Y, Thomas D, Meyer Y, (2005) Ayeast two-hybrid knockout strain to explore thioredoxin-interacting proteins in vivo. Proc Natl Acad Sci USA 102: 16729-16734.
73. Wong J, Jiao JA, Kobrehel K, Buchanan B (1995) Thioredoxin-dependent deinhibition of pullulanase of barley malt by inactivation of a specific inhibitor protein. Plant Physiol 108: 67
74. Wong JH, Balmer Y, Cai N, Tanaka CK, Vensel WH, Hurkman WJ, Buchanan BB (2003) Unraveling thioredoxin-linked metabolic processes of cereal starchy endosperm using proteomics. FEBS Lett 547: 151-156.
75. Wong JH, Cai N, Balmer Y, Tanaka CK, Vensel WH, Hurkman WJ, Buchanan BB (2004) Thioredoxin targets of developing wheat seeds identified by complementary proteomic approaches. Phytochemistry 65: 1629-1640.
76. Wong JH, Kim YB, Ren PH, Cai N, Cho MJ, Hedden P, Lemaux PG, Buchanan BB (2002) Transgenic barley grain overexpressing thioredoxin shows evidence that the starchy endosperm communicates with the embryo and the aleurone. Proc Natl Acad Sci USA 99: 16325-16330.
77. Xie G, Kato H, Sasaki K, Imai R (2009) A cold-induced thioredoxin h of rice, OsTrx23, negatively regulates kinase activities of OsMPK3 and OsMPK6 in vitro. FEBS Lett 583: 2734-2738.
78. Yano H, Kuroda M (2006) Disulfide proteome yields a detailed understanding of redox regulations: a model study of thioredoxin-linked reactions in seed germination. Proteomics 6: 294-300.
79. Yano H, Wong JH, Cho MJ, Buchanan BB (2001a) Redox changes accompanying the degradation of seed storage proteins in germinating rice. Plant Cell Physiol 42: 879-883.
80. Yano H, Wong JH, Lee YM, Cho MJ, Buchanan BB (2001b) A strategy for the identification of proteins targeted by thioredoxin. Proc Natl Acad Sci USA 98: 4794-4799.
81. Zhang L, Tian LH, Zhao JF, Song Y, Zhang CJ, Guo Y (2009) Identification of an apoplastic protein involved in the initial phase of salt stress response in rice root by two-dimensional electrophoresis. Plant Physiol 149: 916-928.