Proteome-wide characterization of seed aging in Arabidopsis: A comparison between artificial and natural aging protocols

Plant Physiology

Volumn 148, Issue 1, 2008, Pages 620-641

  Rajjou, Loïc ^a,b   Lovigny, Yoann ^c   Groot, Steven P C ^d   Belghazi, Maya ^e   Job, Claudette ^c   Job, Dominique ^c  

^a AGROPARISTECH   (France)

^b INSTITUT JEAN PIERRE BOURGIN   (France)

^c UNIVERSITÉ DE LYON   (France)

^d WAGENINGEN UNIVERSITY   (Netherlands)

^e Institut Federatif de Recherche Jean Roche   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

3 MERCAPTOPYRUVATE SULPHURTRANSFERASE; 3-MERCAPTOPYRUVATE SULPHURTRANSFERASE; AMINO ACID; ARABIDOPSIS PROTEIN; DEHYDRIN PROTEINS, PLANT; MESSENGER RNA; PROTEOME; SULFURTRANSFERASE; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; COMPARATIVE STUDY; GERMINATION; GLYCOLYSIS; METABOLISM; OXIDATION REDUCTION REACTION; PLANT SEED; PROTEIN CARBONYLATION; PROTEIN SYNTHESIS; TIME;

AMINO ACIDS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; GERMINATION; GLYCOLYSIS; OXIDATION-REDUCTION; PLANT PROTEINS; PROTEIN BIOSYNTHESIS; PROTEIN CARBONYLATION; PROTEOME; RNA, MESSENGER; SEEDS; SULFURTRANSFERASES; TIME FACTORS;

EID: 53049084651     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.108.123141     Document Type: Article

References (137)

1. Abdalla FH, Roberts EH (1968) The effects of temperature and moisture on the induction of chromosome damage in seeds of barley, broad bean and pea during storage. Ann Bot (Lond) 32: 119-136
2. Adams DO, Yang SF (1981) Ethylene, the gaseous plant hormone: mechanism and regulation of biosynthesis. Trends Biochem Sci 6: 161-164
3. Agrawal GK, Yonekura M, Iwahashi Y, Iwahashi H, Rakwal R (2005a) Systems, trends and perspectives of proteomics in dicot plants Part I: Technologies in proteome establishment. J Chromatogr B Analyt Technol Biomed Life Sci 815: 109-123
4. Agrawal GK, Yonekura M, Iwahashi Y, Iwahashi H, Rakwal R (2005b) Systems, trends and perspectives of proteomics in dicot plants Part II: Proteomes of the complex developmental stages. J Chromatogr B Analyt Technol Biomed Life Sci 815: 125-136
5. Agrawal GK, Yonekura M, Iwahashi Y, Iwahashi H, Rakwal R (2005c) Systems, trends and perspectives of proteomics in dicot plants Part III: Unraveling the proteomes influenced by the environment, and at the levels of functions and genetic relationships. J Chromatogr B Analyt Technol Biomed Life Sci 815: 137-145
6. Alban C, Job D, Douce R (2000) Biotin metabolism in plant. Annu Rev Plant Physiol Plant Mol Biol 51: 17-47
7. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815
8. Aspart L, Meyer Y, Laroche M, Penon P (1984) Developmental regulation of the synthesis of proteins encoded by stored mRNA in radish embryos. Plant Physiol 76: 664-673
9. Bailly C (2004) Active oxygen species and antioxidants in seed biology. Seed Sci Res 14: 93-107
10. Bartoli CG, Pastori GM, Foyer CH (2000) Ascorbate biosynthesis in mitochondria is linked to the electron transport chain between complexes III and IV. Plant Physiol 123: 335-344
11. Baxter CJ, Redestig H, Schauer N, Repsilber D, Patil KR, Nielsen J, Selbig J, Liu J, Fernie AR, Sweetlove LJ (2007) The metabolic response of heterotrophic Arabidopsis cells to oxidative stress. Plant Physiol 143: 312-325
12. Bentsink L, Alonso-Blanco C, Vreugdenhil D, Tesnier K, Groot SPC, Koornneef M (2000) Genetic analysis of seed-soluble oligosaccharides in relation to seed storability of Arabidopsis. Plant Physiol 124: 1595-1604
13. Bentsink L, Jowett J, Hanhart CJ, Koornneef M (2006) Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis. Proc Natl Acad Sci USA 103: 17042-17047
14. Berlett BS, Stadtman ER (1997) Protein oxidation in aging, disease, and oxidative stress. J Biol Chem 272: 20313-20316
15. Bethke PC, Libourel IG, Reinohl V, Jones RL (2006) Sodium nitroprusside, cyanide, nitrite, and nitrate break Arabidopsis seed dormancy in a nitric oxide-dependent manner. Planta 223: 805-812
16. Bewley JD, Black M (1994) Seeds: Physiology of Development and Germination. Plenum Press, New York
17. Bies-Ethève N, Gaubier-Comella P, Debures A, Lasserre E, Jobet E, Raynal M, Cooke R, Delseny M (2008) Inventory, evolution and expression profiling diversity of the LEA (late embryogenesis abundant) protein gene family in Arabidopsis thaliana. Plant Mol Biol 67: 107-124
18. Blum H, Beier H, Gross HJ (1987) Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 8: 93-99
19. Bonomi F, Pagani S, Kurtz DM Jr (1985) Enzymic synthesis of the 4Fe-4S clusters of Clostridium pasteurianum ferredoxin. Eur J Biochem 148: 67-73
20. Borovskii GB, Stupnikova IV, Antipina AI, Vladimirova SV, Voinikov VK (2002) Accumulation of dehydrin-like proteins in the mitochondria of cereals in response to cold, freezing, drought and ABA treatment. BMC Plant Biol 2: 5
21. Boudet J, Buitink J, Hoekstra FA, Rogniaux H, Larré C, Satour P, Leprince O (2006) Comparative analysis of the heat stable proteome of radicles of Medicago truncatula seeds during germination identifies late embryogenesis abundant proteins associated with desiccation tolerance. Plant Physiol 140: 1418-1436
22. Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein using the principle of protein-dye binding. Anal Biochem 72: 248-254
23. Brown PD, Tokuhisa JG, Reichelt M, Gershenzon J (2003) Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. Phytochemistry 62: 471-481
24. Busk PK, Møller BL (2002) Dhurrin synthesis in sorghum is regulated at the transcriptional level and induced by nitrogen fertilization in older plants. Plant Physiol 129: 1222-1231
25. Cabiscol E, Piulats E, Echave P, Herrero E, Ros J (2000) Oxidative stress promotes specific protein damage in Saccharomyces cerevisiae. J Biol Chem 275: 27393-27398
26. Cánovas FM, Dumas-Gaudot E, Recorbet G, Jorrín J, Mock HP, Rossignol M (2004) Plant proteome analysis. Proteomics 4: 285-298
27. Cipollini D, Gruner B (2007) Cyanide in the chemical arsenal of garlic mustard, Alliaria petiolata. J Chem Ecol 33: 85-94
28. Cipollone R, Ascenzi P, Visca P (2007) Common themes and variations in the rhodanese superfamily. IUBMB Life 59: 51-59
29. Clarke S (2003) Aging as war between chemical and biochemical processes: protein methylation and the recognition of age-damaged proteins for repair. Ageing Res Rev 2: 263-285
30. Clerkx EJ, Blankestijn-De Vries H, Ruys GJ, Groot SPC, Koornneef M (2004a) Genetic differences in seed longevity of various Arabidopsis mutants. Physiol Plant 121: 448-461
31. Clerkx EJ, El-Lithy ME, Vierling E, Ruys GJ, Blankestijn-De Vries H, Groot SPC, Vreugdenhil D, Koornneef M (2004b) Analysis of natural allelic variation of Arabidopsis seed germination and seed longevity traits between the accessions Landsberg erecta and Shakdara, using a new recombinant inbred line population. Plant Physiol 135: 432-443
32. Close TJ (1996) Dehydrins: emergence of a biochemical role of a family of plant dehydration proteins. Physiol Plant 97: 795-803
33. Close TJ (1997) Dehydrins: a commonality in the response of plants to dehydration and low temperature. Physiol Plant 100: 291-296
34. Cuming AC (1999) LEA proteins. In PR Shewry, R Casey, eds, Seed Proteins. Kluwer Academic Press, Dordrecht, The Netherlands, pp 753-780
35. Davies MJ (2005) The oxidative environment and protein damage. Biochim Biophys Acta 1703: 93-109
36. Debeaujon I, Léon-Kloosterziel KM, Koornneef M (2000) Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiol 122: 403-414
37. de los Reyes BG, Myers SJ, McGrath JM (2003) Differential induction of glyoxylate cycle enzymes by stress as a marker for seedling vigor in sugar beet (Beta vulgaris). Mol Genet Genomics 269: 692-698
38. Delouche JC, Baskin CC (1973) Accelerated aging techniques for predicting the relative storability of seed lots. Seed Sci Technol 1: 427-452
39. Devaiah SP, Pan X, Hong Y, Roth M, Welti R, Wang X (2007) Enhancing seed quality and viability by suppressing phospholipase D in Arabidopsis. Plant J 50: 950-957
40. Donadio S, Shafiee A, Hutchinson CR (1990) Disruption of a rhodanese like gene results in cysteine auxotrophy in Saccharopolyspora erythraea. J Bacteriol 172: 350-360
41. Droux M, Ruffet ML, Douce R, Job D (1998) Interactions between serine acetyltransferase and O-acetylserine (thiol) lyase in higher plants: structural and kinetic properties of the free and bound enzymes. Eur J Biochem 255: 235-245
42. Dure L III (1993) Structural motifs in LEA proteins of higher plants. In TJ Close, EA Bray, eds, Response of Plants to Cellular Dehydration during Environmental Stress. American Society of Plant Physiologists, Rockville, MD, pp 91-103
43. Duval M, DeRose RT, Job C, Faucher D, Douce R, Job D (1994a) The major biotinyl protein from Pisum sativum seeds covalently binds biotin at a novel site. Plant Mol Biol 26: 265-273
44. Duval M, Job C, Alban C, Douce R, Job D (1994b) Developmental patterns of free and protein-bound biotin during maturation and germination of seeds of Pisum sativum: characterization of a novel seed-specific biotinylated protein. Biochem J 299: 141-150
45. Eastmond PJ, Graham IA (2001) Re-examining the role of the glyoxylate cycle in oilseeds. Trends Plant Sci 6: 72-78
46. Ellis WD, Dunford HB (1968) The kinetics of cyanide and fluoride binding by ferric horseradish peroxidase. Biochemistry 7: 2054-2062
47. Feller U, Fischer A (1994) Nitrogen metabolism in senescing leaves. Crit Rev Plant Sci 13: 241-273
48. Finkelstein RR (1993) Abscisic acid-insensitive mutations provide evidence for stage-specific signal pathways regulating expression of an Arabidopsis late embryogenesis-abundant (lea) gene. Mol Gen Genet 238: 401-408
49. Franca Neto JB, Shatters RG, West SH (1997) Developmental pattern of biotinylated proteins during embryogenesis and maturation of soybean seed. Seed Sci Res 7: 377-384
50. Freedman RB, Dunn AD, Ruddock LW (1998) Protein folding: a missing redox link in the endoplasmic reticulum. Curr Biol 8: R468-R470
51. Gallardo K, Job C, Groot SPC, Puype M, Demol H, Vandekerckhove J, Job D (2001) Proteomic analysis of Arabidopsis seed germination and priming. Plant Physiol 126: 835-848
52. Gallardo K, Job C, Groot SPC, Puype M, Demol H, Vandekerckhove J, Job D (2002a) Proteomics analysis of Arabidopsis seed germination: a comparative study of wild-type and GA-deficient seeds. Plant Physiol 129: 823-837
53. Gallardo K, Job C, Groot SPC, Puype M, Demol H, Vandekerckhove J, Job D (2002b) Importance of methionine biosynthesis for Arabidopsis seed germination and seedling growth. Physiol Plant 116: 238-247
54. Goel A, Goel AK, Sheoran IS (2003) Changes in oxidative stress enzymes during artificial ageing in cotton (Gossypium hirsutum L.) seeds. J Plant Physiol 160: 1093-1100
55. Goldberg RB, Barker SJ, Perez-Grau L (1989) Regulation of gene expression during plant embryogenesis. Cell 56: 149-160
56. Görg A, Postel W, Weser J, Günther S, Strahler JR, Hanash SM, Somerlot L (1987) Elimination of point streaking on silver stained two-dimensional gels by addition of iodoacetamide to the equilibration buffer. Electrophoresis 8: 122-124
57. Graham IA (2008) Seed storage oil mobilization. Annu Rev Plant Biol 59: 115-142
58. Halmer P (2000) Commercial seed treatment technology. In M Black, JD Bewley, eds, Seed Technology and Its Biological Basis. Sheffield Academic Press, Sheffield, England, pp 257-286
59. Harder A, Wildgruber R, Nawrocki A, Fey SJ, Larsen PM, Görg A (1999) Comparison of yeast cell protein solubilization procedures for two-dimensional electrophoresis. Electrophoresis 20: 826-829
60. Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J Gerontol 11: 298-300
61. Heydecker W, Higgins J, Gulliver RL (1973) Accelerated germination by osmotic seed treatment. Nature 246: 42-44
62. Höfgen R, Kreft O, Willmitzer L, Hesse H (2001) Manipulation of thiol contents in plants. Amino Acids 20: 291-299
63. Holdsworth MJ, Finch-Savage WE, Grappin P, Job D (2008) Post-genomics dissection of seed dormancy and germination. Trends Plant Sci 13: 7-13
64. Hsing YC, Tsou CH, Hsu TF, Chen ZY, Hsieh KL, Hsieh JS, Chow TY (1998) Tissue- and stage-specific expression of a soybean (Glycine max L.) seed-maturation, biotinylated protein. Plant Mol Biol 38: 481-490
65. Ingrosso D, Cimmino A, D'Angelo S, Alfinito F, Zappia V, Galletti P (2002) Protein methylation as a marker of aspartate damage in glucose-6-phosphate dehydrogenase-deficient erythrocytes: role of oxidative stress. Eur J Biochem 269: 2032-2039
66. Ismail AM, Hall AE, Close TJ (1999) Purification and partial characterization of a dehydrin involved in chilling tolerance during seedling emergence of cowpea. Plant Physiol 120: 237-244
67. Job C, Laugel S, Duval M, Gallardo K, Job D (2001) Biochemical characterization of atypical biotinylation domains in seed proteins. Seed Sci Res 11: 149-161
68. Job C, Rajjou L, Lovigny Y, Belghazi M, Job D (2005) Patterns of protein oxidation in Arabidopsis seeds and during germination. Plant Physiol 138: 790-802
69. Job D, Ricard J (1975) Kinetic and equilibrium studies of cyanide and fluoride binding to turnip peroxidases. Arch Biochem Biophys 170: 427-437
70. Johansson E, Olsson O, Nyström T (2004) Progression and specificity of protein oxidation in the life cycle of Arabidopsis thaliana. J Biol Chem 279: 22204-22208
71. Jorrín JV, Maldonado AM, Castillejo MA (2007) Plant proteome analysis: a 2006 update. Proteomics 7: 2947-2962
72. Kibinza S, Vinel D, Côme D, Bailly C, Corbineau F (2006) Sunflower seed deterioration as related to moisture content during ageing, energy metabolism and active oxygen species scavenging. Physiol Plant 128: 496-506
73. Korolainen MA, Goldsteins G, Alafuzoff I, Koistinaho J, Pirttila T (2002) Proteomic analysis of protein oxidation in Alzheimer's disease brain. Electrophoresis 23: 3428-3433
74. Laboissière MC, Sturley SL, Raines RT (1997) Protein disulfide isomerase in spore germination and cell division. Biol Chem 378: 431-437
75. Lane BG (1991) Cellular desiccation and hydration: developmentally regulated proteins, and the maturation and germination of seed embryos. FASEB J 5: 2893-2901
76. Lång V, Palva ET (1992) The expression of a rab-related gene, rab18, is induced by abscisic acid during the cold acclimation process of Arabidopsis thaliana (L.) Heynh. Plant Mol Biol 20: 951-962
77. Lanteri S, Nada E, Belletti P, Quagliotti L, Bino RJ (1996) Effects of controlled deterioration and osmoconditioning on germination and nuclear replication in seeds of pepper (Capsicum annuum L.). Ann Bot (Lond) 77: 591-597
78. Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, Ahn BW, Shaltiel S, Stadtman ER (1990) Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186: 464-478
79. Levine RL, Stadtman ER (2001) Oxidative modification of proteins during aging. Exp Gerontol 36: 1495-1502
80. Lopez-Martin MC, Becana M, Romero LC, Gotor C (2008) Knocking out cytosolic cysteine synthesis compromises the antioxidant capacity of the cytosol to maintain discrete concentrations of hydrogen peroxide in Arabidopsis. Plant Physiol 147: 562-572
81. Lopez-Molina L, Mongrand S, McLachlin DT, Chait BT, Chua NH (2002) ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J 32: 317-328
82. Mano J, Belles-Boix E, Babiychuk E, Inzè D, Torii Y, Hiraoka E, Takimoto K, Slooten L, Asada K, Kushnir S (2005) Protection against photooxidative injury of tobacco leaves by 2-alkenal reductase: detoxication of lipid peroxide-derived reactive carbonyls. Plant Physiol 139: 1773-1783
83. March TJ, Able JA, Schultz CJ, Able AJ (2007) A novel late embryogenesis abundant protein and peroxidase associated with black point in barley grains. Proteomics 7: 3800-3808
84. McDonald MB (1999) Seed deterioration: physiology, repair and assessment. Seed Sci Technol 27: 177-237
85. Miura K, Lin Y, Yano M, Nagamine T (2002) Mapping quantitative trait loci controlling seed longevity in rice (Oryza sativa L.). Theor Appl Genet 104: 981-986
86. Møller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58: 459-481
87. Nagahara N, Katayama A (2005) Post-translational regulation of mercaptopyruvate sulfurtransferase via a low redox potential cysteine-sulfenate in the maintenance of redox homeostasis. J Biol Chem 280: 34569-34576
88. Nakabayashi K, Okamoto M, Koshiba T, Kamiya Y, Nambara E (2005) Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. Plant J 41: 697-709
89. Nikolau BJ, Ohlrogge JB, Wurtele ES (2003) Plant biotin-containing carboxylases. Arch Biochem Biophys 414: 211-222
90. Nyström T (2005) Role of oxidative carbonylation in protein quality control and senescence. EMBO J 24: 1311-1317
91. Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15: 1591-1604
92. Oracz K, El-Maarouf-Bouteau H, Bogatek R, Corbineau F, Bailly C (2008) Release of sunflower seed dormancy by cyanide: cross-talk with ethylene signalling pathway. J Exp Bot 59: 2241-2251
93. Osborne DJ, Sharon R, Ben-Ishai R (1980/1981) DNA integrity and repair. Isr J Bot 29: 259-272
94. Pagani S, Bonomi F, Cerletti P (1984) Enzymic synthesis of the iron-sulfur cluster of spinach ferredoxin. Eur J Biochem 142: 361-366
95. Papdi C, Abraham E, Joseph MP, Popescu C, Koncz C, Szabados L (2008) Functional identification of Arabidopsis stress regulatory genes using the controlled cDNA overexpression system. Plant Physiol 147: 528-542
96. Papenbrock J, Schmidt A (2000a) Characterization of a sulfurtransferase from Arabidopsis thaliana. Eur J Biochem 267: 145-154
97. Papenbrock J, Schmidt A (2000b) Characterization of two sulfurtransferase isozymes from Arabidopsis thaliana. Eur J Biochem 267: 5571-5579
98. Parcy F, Valon C, Raynal M, Gaubier-Comella P, Delseny M, Giraudat J (1994) Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell 6: 1567-1582
99. Park OK (2004) Proteomic studies in plants. J Biochem Mol Biol 37: 133-138
100. Patton DA, Schetter AL, Franzmann LH, Nelson K, Ward ER, Meinke DW (1998) An embryo-defective mutant of Arabidopsis disrupted in the final step of biotin synthesis. Plant Physiol 116: 935-946
101. Peiser GD, Wang TT, Hoffman NE, Yang SF, Liu HW, Walsh CT (1984) Formation of cyanide from carbon 1 of 1-aminocyclopropane-1-carboxylic acid during its conversion to ethylene. Proc Natl Acad Sci USA 81: 3059-3063
102. Pell EJ, Schlagnhaufer CD, Arteca RN (1997) Ozone-induced oxidative stress: mechanisms of action and reaction. Physiol Plant 100: 264-273
103. Pillay DTN (1977) Protein synthesis in aging soybean cotyledons: loss in translational capacity. Biochem Biophys Res Commun 79: 796-804
104. Poulton JE (1990) Cyanogenesis in plants. Plant Physiol 94: 401-405
105. Powell AA (1995) The controlled deterioration test. In HA van de Venter, ed, Seed Vigour Testing Seminar. International Seed Testing Association, Zurich, pp 73-87
106. Prieto-Dapena P, Castaño R, Almoguera C, Jordano J (2006) Improved resistance to controlled deterioration in transgenic seeds. Plant Physiol 142: 1102-1112
107. Rajjou L, Belghazi M, Huguet R, Robin C, Moreau A, Job C, Job D (2006a) Proteomic investigation of the effect of salicylic acid on Arabidopsis seed germination and establishment of early defense mechanisms. Plant Physiol 141: 910-923
108. Rajjou L, Gallardo K, Debeaujon I, Vandekerckhove J, Job C, Job D (2004) The effect of alpha-amanitin on the Arabidopsis seed proteome high-lights the distinct roles of stored and neosynthesized mRNAs during germination. Plant Physiol 134: 1598-1613
109. Rajjou L, Gallardo K, Job C, Job D (2006b) Proteome analysis for the study of developmental processes in plants. In C Finnie, ed, Plant Proteomics. Annual Plant Reviews 28. Blackwell Publishing, Oxford, pp 151-184
110. Rajjou L, Lovigny Y, Job C, Belghazi M, Groot S, Job D (2007a) Seed quality and germination. In S Navie, S Adkins, S Ashmore, eds, Seeds: Biology, Development and Ecology. CAB International Publishing, Cambridge, MA, pp 324-332
111. Rajjou L, Miché L, Huguet R, Job C, Job D (2007b) Proteome and transcriptome profiling to understand seed germination and identify intrinsic markers determining seed quality, germination efficiency and early seedling vigor. In S Navie, S Adkins, S Ashmore, eds, Seeds: Biology, Development and Ecology. CAB International Publishing, Cambridge, MA, pp 149-158
112. Ravanel S, Gakière B, Job D, Douce R (1998) The specific features of methionine biosynthesis and metabolism in plants. Proc Natl Acad Sci USA 95: 7805-7812
113. Rossignol M, Peltier JB, Mock HP, Matros A, Maldonado AM, Jorrín JV (2006) Plant proteome analysis: a 2004-2006 update. Proteomics 6: 5529-5548
114. Sattler SE, Gilliland LU, Magallanes-Lundback M, Pollard M, DellaPenna D (2004) Vitamin E is essential for seed longevity and for preventing lipid peroxidation during germination. Plant Cell 16: 1419-1432
115. Shatters RG, Boo SP, Franca Neto JB, West SH (1997) Identification of biotinylated proteins in soybean [Glycine max (L.) Merrill] seeds and their characterization during germination and seedling growth. Seed Sci Res 7: 373-376
116. Shen-Miller J (2002) Sacred lotus, the long-living fruits of China Antique. Seed Sci Res 12: 131-143
117. 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
118. Skriver K, Mundy J (1990) Gene expression in response to abscisic acid and osmotic stress. Plant Cell 2: 503-512
119. Soeda Y, Konings MCJM, Vorst O, van Houwelingen AMML, Stoopen GM, Maliepaard CA, Kodde J, Bino RJ, Groot SPC, van der Geest AHM (2005) Gene expression programs during Brassica oleracea seed maturation, osmopriming and germination are indicators of progression of the germination process and the stress tolerance level. Plant Physiol 137: 354-368
120. Somerville C, Koornneef M (2002) A fortunate choice: the history of Arabidopsis as a model plant. Nat Rev Genet 3: 883-889
121. Söti C, Csermely P (2007) Protein stress and stress proteins: implications in aging and disease. J Biosci 32: 511-515
122. Stadtman ER (2001) Protein oxidation in aging and age-related diseases. Ann N Y Acad Sci 928: 22-38
123. Stadtman ER (2004) Role of oxidant species in aging. Curr Med Chem 11: 1105-1112
124. Tamarit J, Cabiscol E, Ros J (1998) Identification of the major oxidatively damaged proteins in Escherichia coli cells exposed to oxidative stress. J Biol Chem 273: 3027-3032
125. Taylorson RB, Hendricks SB (1973) Promotion of seed germination by cyanide. Plant Physiol 52: 23-27
126. Tejera García NA, Iribarne C, Palma F, Lluch C (2007) Inhibition of the catalase activity from Phaseolus vulgaris and Medicago sativa by sodium chloride. Plant Physiol Biochem 45: 535-541
127. TeKrony DM (1995) Accelerated aging. In HA van de Venter, ed, Seed Vigour Testing Seminar. International Seed Testing Association, Zurich, pp 53-73
128. Terskikh VV, Zeng Y, Feurtado JA, Giblin M, Abrams SR, Kermode AR (2008) Deterioration of western redcedar (Thuja plicata Donn ex D. Don) seeds: protein oxidation and in vivo NMR monitoring of storage oils. J Exp Bot 59: 765-777
129. Tesnier K, Strookman-Donkers HM, van Pijlen JG, van der Geest AHM, Bino RJ, Groot SPC (2002) A controlled deterioration test of Arabidopsis thaliana reveals genetic variation in seed quality. Seed Sci Technol 30: 149-165
130. Walters C (2004) Temperature dependency of molecular mobility in preserved seeds. Biophys J 86: 1253-1258
131. Walters C, Wheeler LM, Grotenhuis JM (2005) Longevity of seeds stored in a genebank: species characteristics. Seed Sci Res 15: 1-20
132. Walters C, Wheeler LM, Stanwood PC (2004) Longevity of cryogenically stored seeds. Cryobiology 48: 229-244
133. Wan CY, Wilkins TA (1994) A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.). Anal Biochem 223: 7-12
134. Wechsberg GE, Probert RJ, Bray CM (1994) The relationship between "dehydrin-like" proteins and seed longevity in Ranunculus sceleratus L. J Exp Bot 45: 1027-1030
135. Wilkinson B, Gilbert HF (2004) Protein disulfide isomerase. Biochim Biophys Acta 1699: 35-44
136. Xu Q, Belcastro MP, Villa ST, Dinkins RD, Clarke SG, Downie AB (2004) A second protein L-isoaspartyl methyltransferase gene in Arabidopsis produces two transcripts whose products are sequestered in the nucleus. Plant Physiol 136: 2652-2664
137. Yoshida H (2007) ER stress and diseases. FEBS J 274: 630-658