Desiccation tolerant plants as model systems to study redox regulation of protein thiols

Plant Growth Regulation

Volumn 62, Issue 3, 2010, Pages 241-255

  Colville, Louise ^a   Kranner, Ilse ^a  

^a ROYAL BOTANIC GARDENS   (United Kingdom)

Author keywords

Desiccation; Glutaredoxin; Glutathione; Glutathionylation; Thiol; Thioredoxin

Indexed keywords

ANIMALIA; BRYOPHYTA; BRYOPHYTES; MAGNOLIOPHYTA;

EID: 77958561000     PISSN: 01676903     EISSN: 15735087     Source Type: Journal    
DOI: 10.1007/s10725-010-9482-9     Document Type: Article

References (96)

1. Aalen RB (1999) Peroxiredoxin antioxidants in seed physiology. Seed Sci Res 9: 285-295.
2. Alkhalfioui F, Renard M, Vensel WH, Wong J, Tanaka CK, Hurkman WJ, Buchanan BB, Montrichard F (2007) Thioredoxin-linked proteins are reduced during germination of Medicago truncatula seeds. Plant Physiol 144: 1559-1579.
3. Alpert P (2005) The limits and frontiers of desiccation-tolerant life. Integr Comp Biol 45: 685-695.
4. Alpert P (2006) Constraints of tolerance: why are desiccation-tolerant organisms so small or rare? J Exp Bot 209: 1575-1584.
5. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55: 373-399.
6. Bailly C (2004) Active oxygen species and antioxidants in seed biology. Seed Sci Res 14: 93-107.
7. Bailly C, Audigier C, Ladonne F, Wagner MH, Coste F, Corbineau F, Come 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.
8. Beckett RP, Minibayeva FV, Lüthje S, Böttger M (2004) Reactive oxygen species metabolism in desiccation-stressed thalli of the liverwort Dumortiera hirsuta. Physiol Plant 122: 3-10.
9. Berjak P, Pammenter NW (2008) From Avicennia to Zizania: Seed recalcitrance in perspective. Annal Bot 101: 213-228.
10. Black M, Pritchard HW (2002) Desiccation and survival in plants: drying without dying. CAB International, Wallingford.
11. Broin M, Rey P (2003) Potato plants lacking the CDSP32 plastidic thioredoxin exhibit overoxidation of the BAS1 2-Cysteine peroxiredoxin and increased lipid peroxidation in thylakoids under photooxidative stress. Plant Physiol 132: 1335-1343.
12. Buitink J, Leprince O (2004) Glass formation in plant anhydrobiotes: survival in the dry state. Cryobiol 48: 215-228.
13. Butt AD, Ohlrogge JB (1991) Acyl carrier protein is conjugated to glutathione in spinach seed. Plant Physiol 96: 937-942.
14. Cazalis R, Pulido P, Aussenac T, Perez-Ruiz JM, Cejudo FJ (2006) Cloning and expression of three thioredoxin h isoforms from wheat showing differential expression in seeds. J Exp Bot 57: 2165-2172.
15. 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.
16. Cumming RC, Andon NL, Haynes PA, Park M, Fischer WH, Schubert D (2004) Protein disulfide bond formation in the cytoplasm during oxidative stress. J Biol Chem 279: 21749-21758.
17. Dalle-Donne I, Rossi R, Giustarini D, Colombo R, Milzani A (2007) S-glutathionylation in protein redox regulation. Free Radic Bio Med 43: 883-898.
18. Dalle-Donne I, Rossi R, Colombo G, Giustarini D, Milzani A (2009) Protein S-glutathionylation: a regulatory device from bacteria to humans. Trends Biochem Sci 34: 85-96.
19. 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.
20. De Tullio MC, Arrigoni O (2003) The ascorbic acid system in seeds: to protect and to serve. Seed Sci Res 13: 249-260.
21. Dhindsa R (1987) Glutathione status and protein synthesis during drought and subsequent rehydration in Tortula ruralis. Plant Physiol 83: 816-819.
22. Dhindsa R (1991) Drought stress, enzymes of glutathione metabolism, oxidation injury and protein synthesis in Tortula ruralis. Plant Physiol 95: 648-651.
23. Dietz KJ (2003) Plant peroxiredoxins. Annu Rev Plant Biol 54: 93-107.
24. Dietz KJ (2008) Redox signal integration: from stimulus to networks and genes. Physiol Plant 133: 459-468.
25. Dietz KJ, Jacob S, Oelze M, Laxa M, Tognetti V, Nunes de Miranda SM, Baier M, Finkemeier I (2006) The function of peroxiredoxins in plant organelle redox metabolism. J Exp Bot 57: 1697-1709.
26. Dixon DP, Skipsey M, Grundy NM, Edwards R (2005) Stress-induced protein S-glutathionylation in Arabidopsis. Plant Physiol 138: 2233-2244.
27. Dos Santos CV, Rey P (2006) Plant thioredoxins are key actors in the oxidative stress response. Trends Plant Sci 11: 329-334.
28. Fahey RC, Brody S, Mikolajczyk SD (1975) Changes in the glutathione thiol-disulphide status of Neurospora crassa conidia during germination and aging. J Bacteriol 135: 144-151.
29. Fahey RC, Di Stefano DL, Meier GP, Bryan RN (1980) Role of hydration state and thiol-disulfide status in the control of thermal stability and protein synthesis in wheat embryo. Plant Physiol 65: 1062-1066.
30. Fomenko DE, Xing W, Adair BM, Thomas DJ, Gladyshev VN (2007) High-throughput identification of catalytic redox-active cysteine residues. Science 315: 387-389.
31. Giustarini D, Rossi R, Milzani A, Colombo R, Dalle-Donne I (2004) S-Glutathionylation: from redox regulation of protein functions to human diseases. J Cell Mol Med 8: 201-212.
32. Hajheidari M, Eivazi A, Buchanan BB, Wong JH, Majidi I, Salekdeh GH (2007) Proteomics uncovers a role for redox in drought tolerance in wheat. J Proteome Res 6: 1451-1460.
33. Hancock J, Desikan R, Harrison J, Bright J, Hooley R, Neill S (2006) Doing the unexpected: proteins involved in hydrogen peroxide perception. J Exp Bot 57: 1711-1718.
34. Hansen RE, Roth D, Winther JR (2009) Quantifying the global cellular thiol-disulfide status. Proc Natl Acad Sci 106: 422-427.
35. Haslekas C, Viken MK, Grini PE, Nygaard V, Nordgard SH, Meza TJ, Aalen RB (2003) Seed 1-Cysteine peroxiredoxin antioxidants are not involved in dormancy, but contribute to inhibition of germination during stress. Plant Physiol 133: 1148-1157.
36. Hoekstra FA, Golovina EA, Buitink J (2001) Mechanisms of plant desiccation tolerance. Trends Plant Sci 6: 431-438.
37. Illing N, Denby KJ, Collett H, Shen A, Farrant JM (2005) The signature of seeds in resurrection plants: a molecular and physiological comparison of desiccation tolerance in seeds and vegetative tissues. Integr Comp Biol 45: 771-787.
38. Jacquot J, Eklund H, Rouhier N, Schurmann P (2009) Structural and evolutionary aspects of thioredoxin reductases in photosynthetic organisms. Trends Plant Sci 14: 336-343.
39. Jenks M, Wood A (2007) Plant desiccation tolerance. Iowa, Iowa State University Press.
40. Jiang G, Wang Z, Shang H, Yang W, Hu Z, Phillips J, Deng X (2007) Proteome analysis of leaves from the resurrection plant Boea hygrometrica in response to dehydration and rehydration. Planta 225: 1405-1420.
41. Kemp M, Go YM, Jones DP (2008) Nonequilibrium thermodynamics of thiol/disulfide redox systems: a perspective on redox systems biology. Free Radic Biol Med 44: 921-937.
42. Koster KL (1991) Glass formation and desiccation tolerance in seeds. Plant Physiol 96: 302-304.
43. Koster KL, Leopold AC (1988) Sugars and desiccation tolerance in seeds. Plant Physiol 88: 829-832.
44. Kranner I (2002) Glutathione status correlates with different degrees of desiccation tolerance in three lichens. New Phytol 154: 451-460.
45. Kranner I, Birtic S (2005) A modulating role for antioxidants in desiccation tolerance. Integr Comp Biol 45: 734-740.
46. Kranner I, Grill D (1993) Content of low-molecular-weight thiols during imbibition of pea seeds. Physiol Plant 88: 557-562.
47. Kranner I, Grill D (1996) Significance of thiol-disulfide exchange in resting stages of plant development. Bot Acta 109: 8-14.
48. Kranner I, Grill D (1997) Desiccation and the subsequent recovery of cryptogamics that are resistant to drought. Phyton 37 Special issue Oxygen. Free radic environ stress plants 37: 139-150.
49. Kranner I, Beckett RP, Wornik S, Zorn M, Pfeifhofer HW (2002) Revival of a resurrection plant correlates with its antioxidant status. Plant J 31: 13-24.
50. Kranner I, Birtić S, Anderson KM, Pritchard HW (2006) Glutathione half-cell reduction potential: A universal stress marker and modulator of programmed cell death? Free Radic Bio Med 40: 2155-2165.
51. Kranner I, Beckett RP, Hochman A, Nash T III (2008) Desiccation tolerance in lichens: a review. Bryologist 111: 576-593.
52. Kranner I, Roach BeckettRP, Whitaker C, Minibayeva FV (2010) Extracellular production of reactive oxygen species during seed germination and early seedling growth in Pisum sativum. J Plant Physioly 167(10): 805-811. doi: 10. 1016/j. jplph. 2010. 01. 019.
53. Leprince O, Harren FJM, Buitink J, Alberda M, Hoekstra FA (2000) Metabolic dysfunction and unabated respiration precede the loss of membrane integrity during dehydration of germinating radicles. Plant Physiol 122: 597-608.
54. Liu X, Wang Z, Wang L, Wu R, Phillips J, Deng X (2009) LEA 4 group genes from the resurrection plant Boea hygrometrica confer dehydration tolerance in transgenic tobacco. Plant Sci 176: 90-98.
55. Meyer AJ, Rüdiger H (2005) Glutathione homeostasis and redox-regulation by sulfhydryl groups. Photosynth Res 86: 435-457.
56. Meyer AJ, Brach T, Marty L, Kreye S, Rouhier N, Jacquot JP, Hell R (2007) Redox-sensitive GFP in Arabidopsis thaliana is a quantitative biosensor for the redox potential of the cellular glutathione redox buffer. Plant J 52: 973-986.
57. Minibayeva F, Beckett RP (2001) High rates of extracellular superoxide production in bryophytes and lichens, and an oxidative burst in response to rehydration following desiccation. New Phytol 152: 333-341.
58. Mittler R (2004) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7: 405-410.
59. Moore JP, Le NT, Brandt WF, Driouich A, Farrant JM (2009) Towards a systems-based understanding of plant desiccation tolerance. Trends Plant Sci 14: 110-117.
60. Mowla SB, Thomson JA, Farrant JM, Mundree SG (2002) A novel stress-inducible antioxidant enzyme identified from the resurrection plant Xerophyta viscosa Baker. Planta 215: 716-726.
61. Murthy UMN, Kumar PP, Sun WQ (2003) Mechanisms of seed ageing under different storage conditions for Vigna radiata (L.) Wilczek: lipid peroxidation, sugar hydrolyisis, Maillard reactions and their relationship to glass state transition. J Exp Bot 54: 1057-1067.
62. Navari-Izzo F, Quartacci MF, Pinzino C, Rascio N, Vazzana C, Sgherri CLM (2000) Protein dynamics in thylakoids of the desiccation-tolerant plant Boea hygroscopica during dehydration and rehydration. Plant Physiol 124: 1427-1436.
63. Navrot N, Collin V, Gualberto J, Gelhaye E, Hirasawa M, Rey P, Knaff DB, Issakidis E, Jacquot J, 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.
64. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49: 249-279.
65. Onda Y, Kumamaru T, Kawagoe Y (2009) ER membrane-localized oxidoreductase Ero1 is required for disulfide bond formation in the rice endosperm. Proc Natl Acad Sci 106: 14156-14161.
66. Paulsen CE, Carroll KS (2010) Orchestrating redox signalling networks through regulatory cyteine switches. ACS Chem Biol 5: 47-62.
67. Peltoniemi MJ, Karala A, Jurvansuu JK, Kinnula VL, Ruddock LW (2006) Insights into deglutathionylation reactions-different intermediates in the glutaredoxin and protein disulfide isomerase catalyzed reactions are defined by the γ-linkage present in glutathione. J Biol Chem 281: 33107-33114.
68. Potts M, Slaughter SM, Hunneke FU, Garst JF, Helm RF (2005) Desiccation tolerance of prokaryotes: Application of principles to human cells. Integr Comp Biol 45: 800-809.
69. Proctor MCF, Oliver MJ, Wood AJ, Alpert P, Stark LR, Cleavitt NL, Mishler BD (2007) Desiccation-tolerance in bryophytes: a review. Bryologist 110: 595-621.
70. Pukacka S, Ratajczak E (2006) Antioxidative response of ascorbate-glutathione pathway enzymes and metabolites to desiccation of recalcitrant Acer saccharinum seeds. J Plant Physiol 163: 1259-1266.
71. Pukacka S, Ratajczak E (2007) Ascorbate and glutathione metabolism during development and desiccation of orthodox and recalcitrant seeds of the genus Acer. Funct Plant Biol 34: 601-613.
72. Rhazi L, Cazalis R, Lemelin E, Aussenac T (2003) Changes in the thiol-disulfide status during wheat grain development. Plant Physiol Biochem 41: 895-902.
73. Rinalducci S, Murgiano L, Zolla L (2008) Redox proteomics: basic principles and future perspectives for the detection of protein oxidation in plants. J Exp Bot 59: 3781-3801.
74. Roach T, Beckett RP, Minibayeva FV, Colville L, Whitaker C, Chen HY, Bailly C, Kranner I (2010) Extracellular superoxide production, viability and redox poise in response to desiccation in recalcitrant Castanea sativa seeds. Plant Cell Environ 33: 59-75.
75. 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.
76. Schafer FQ, Buettner GR (2001) Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Bio Med 30: 1191-1212.
77. Schopfer P, Plachy C, Frahry G (2001) Release of reactive oxygen intermediates (superoxide radicals, hydrogen peroxide, and hydroxyl radicals) and peroxidase in germinating radish seeds controlled by light, gibberellin, and abscisic acid. Plant Physiol 125: 1591-1602.
78. Seel WE, Hendry GAF, Lee JA (1992) Effects of desiccation on some activated oxygen processing enzymes and anti-oxidants in mosses. J Ex Bot 43: 1031-1037.
79. Serrato AJ, Cejudo FJ (2003) Type-h thioredoxins accumulate in the nucleus of developing wheat seed tissues suffering oxidative stress. Planta 217: 392-399.
80. Serrato AJ, Perez-Ruiz JM, Spinola MC, Cejudo FJ (2004) A novel NADPH thioredoxin reductase, localized in the chloroplast, which deficiency causes hypersensitivity to abiotic stress in Arabidopsis thaliana. J Biol Chem 279: 43821-43827.
81. 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.
82. Shen-Miller J, Mudgett MB, Schopf JW, Clarke S, Berger R (1995) Exceptional seed longevity and robust growth: ancient sacred lotus from China. Am J Bot 82: 1367-1380.
83. Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 125: 27-58.
84. Smirnoff N, Wheeler GL (2000) Ascorbic acid in plants: biosynthesis and function. Crit Rev Plant Sci 19: 267-290.
85. Stacy RAP, 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.
86. Szalai G, Kellos T, Galiba G, Kocsy G (2009) Glutathione as an antioxidant and regulatory molecule in plants under abiotic stress conditions. J Plant Growth Regul 28: 66-80.
87. Tommasi F, Paciolla C, Arrigoni O (1999) The ascorbate system in recalcitrant and orthodox seeds. Physiol Plant 105: 193-198.
88. Tommasi F, Paciolla C, de Pinto MC, De Gara L (2001) A comparative study of glutathione and ascorbate metabolism during germination of Pinus pinea L. seeds. J Ex Bot 52: 1647-1654.
89. 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.
90. Wang XQ, Yang PF, Liu Z, Liu WZ, Hu Y, Chen H, Kuang TY, Pei ZM, Shen SH, He YK (2009) Exploring the mechanism of Physcomitrella patens desiccation tolerance through a proteomic strategy. Plant Physiol 149: 1739-1750.
91. Wettlaufer SH, Leopold AC (1991) Relevance of Amadori and Maillard products to seed deterioration. Plant Physiol 97: 165-169.
92. Wise MJ, Tunnacliffe A (2004) POPP the question: what do LEA proteins do? Trends Plant Sci 9: 13-17.
93. 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.
94. 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. Phytochem 65: 1629-1640.
95. Woo HA, Jeong W, Chang T, Park KJ, Park SJ, Yang JS, Rhee SG (2005) Sulfiredoxin is specific to 2-Cys peroxiredoxins. J Biol Chem 280: 3125-3128.
96. Ying J, Clavreul N, Sethuraman M, Adachi T, Cohen RA (2007) Thiol oxidation in signalling and response to stress: detection and quantification of physiological and pathophysiological thiol modifications. Free Radic Biol Med 43: 1099-1108.