Elucidating hormonal/ROS networks during seed germination: Insights and perspectives

Plant Cell Reports

Volumn 32, Issue 10, 2013, Pages 1491-1502

  Diaz Vivancos, Pedro ^a   Barba Espín, Gregorio ^a,b   Hernández, José Antonio ^a  

^a RESEARCH GROUP ON QUALITY   (Spain)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

Antioxidative metabolism; Germination; Plant hormones; ROS signaling; Seed proteome

Indexed keywords

PHYTOHORMONE; PROTEOME; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; TRANSCRIPTOME;

GENE EXPRESSION REGULATION; GERMINATION; METABOLISM; PHYSIOLOGY; PLANT PHYSIOLOGY; PLANT SEED; PROTEIN PROCESSING; REVIEW; SIGNAL TRANSDUCTION;

GENE EXPRESSION REGULATION, PLANT; GERMINATION; MAP KINASE SIGNALING SYSTEM; PLANT GROWTH REGULATORS; PLANT PHYSIOLOGICAL PHENOMENA; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; SEEDS; TRANSCRIPTOME;

EID: 84884206149     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-013-1473-7     Document Type: Review

References (105)

1. Bahin E, Bailly C, Sotta B, Kranner I, Corbineau F, Leymarie J (2011) Crosstalk between reactive oxygen species and hormonal signalling pathway regulates grain dormancy in barley. Plant Cell Environ 34: 980-993.
2. Bailly C (2004) Active oxygen species and antioxidants in seed biology. Seed Sci Res 14: 93-107.
3. 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. CR Biol 331: 806-814.
4. Bajji M, M'Hamdi M, Gastiny F, Rojas-Beltran JA, du Jardin P (2007) Catalase inhibition accelerates dormancy release and sprouting in potato (Solanum tuberosum L.) tubers. Biotechnol Agron Soc Environ 11: 121-131.
5. Barba-Espín G, Diaz-Vivancos P, Clemente-Moreno MJ, Albacete A, Faize L, Faize M, Pérez-Alfocea F, Hernández JA (2010) Interaction between hydrogen peroxide and plant hormones during germination and the early growth of pea seedlings. Plant Cell Environ 33: 981-994.
6. 2 during pea seed germination: a combined proteomic and hormone profiling approach. Plant Cell Environ 34: 1907-1919.
7. Barba-Espín G, Clemente-M MJ, Nicolas E, Almansa MS, Cantero E, Albacete A, Hernandez JA, Diaz-Vivancos P (2012) Role of thioproline on seed germination: interaction ROS-ABA and effects on antioxidative metabolism. Plant Physiol Biochem 59: 30-36.
8. Beligni MV, Lamattina L (2001) Nitric oxide: a non-traditional regulator of plant growth. Trends Plant Sci 6: 508-509.
9. Bethke PC, Libourel IG, Aoyama N, Chung YY, Still DW, Jones RL (2007) The Arabidopsis aleurone layer responds to nitric oxide, gibberellin, and abscisic acid and is sufficient and necessary for seed dormancy. Plant Physiol 143: 1173-1188.
10. Bewley D (1997) Seed germination and dormancy. Plant Cell 9: 1055-1066.
11. Bray CM, West CE (2005) DNA repair mechanisms in plants: crucial sensors and effectors for the maintenance of genome integrity. New Phytol 168: 511-528.
12. Buchanan BB, Gruissem W, Jones RL (2000) Biochemistry and molecular biology of plants. Monona Drive, American Society of Plant Physiologist, Rockville.
13. Chen Z, Silva H, Klessing DF (1993) Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262: 1883-1886.
14. 2-induced lateral root formation in apocynin-treated rice. Plant Cell Rep 32: 219-226.
15. Chiu KY, Chen CL, Sung JM (2002) Effect of priming temperature on storability of primed sh-2-sweet corn seed. Crop Sci 42: 1993-2003.
16. De Gara L, de Pinto MC, Arrigoni O (1997) Ascorbate synthesis and ascorbate peroxidase activity during the early stage of wheat germination. Physiol Plant 100: 894-900.
17. de Pinto MC, De Gara L (2004) Changes in the ascorbate metabolism of apoplastic and symplastic spaces are associated with cell differentiation. J Exp Bot 55: 2559-2569.
18. de Tullio MC, Arrigoni O (2003) The ascorbic acid system in seeds: to protect and to serve. Seed Sci Res 13: 249-260.
19. Demidchik V (2012) Reactive oxygen species and oxidative stress in plants. In: Shabala S (ed) Plant stress physiology. CAB International, Oxfordshire, pp 24-58.
20. El-Maarouf-Bouteau H, Bailly C (2008) Oxidative signaling in seed germination and dormancy. Plant Signal Behav 3: 332-341.
21. Feng Y, Liu D, Yao H, Wang J (2007) Solution structure and mapping of a very weak calcium-binding site of human translationally controlled tumor protein by NMR. Arch Biochem Biophys 467: 48-57.
22. Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171: 501-523.
23. Finkelstein R, Reeves W, Ariizumi T, Steber C (2008) Molecular aspect of seed dormancy. Ann Rev Plant Biol 59: 387-415.
24. Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signalling: a metabolic interface between the stress perception and physiological responses. Plant Cell 17: 1866-1875.
25. Fulgosi H, Soll J, Maraschin SF, Korthout HAAJ, Wang M, Testerink C (2002) 14-3-3 proteins and plant development. Plant Mol Biol 50: 1019-1029.
26. 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.
27. Gallardo K, Job C, Groot SPC, Puype M, Demol H et al (2002a) Importance of methionine biosynthesis for Arabidopsis seed germination and priming. Plant Physiol 126: 835-848.
28. Gallardo K, Job C, Groot SPC, Puype M, Demol H et al (2002b) Proteomics of Arabidopsis seeds germination: a comparative study of wild-type and gibberellin-deficient seeds. Plant Physiol 129: 823-837.
29. Gidrol X, Lin WS, Degousee N, Yip SF, Kush A (1994) Accumulation of reactive oxygen species and oxidation of cytokinin in germinating soybean seeds. Eur J Biochem 224: 21-28.
30. Gniazdowska A, Krasuska U, Debska K, Andryka P, Bogatek R (2010a) The beneficial effect of small toxic molecules on dormancy alleviation and germination of apple embryos is due to NO formation. Planta 232: 999-1005.
31. Gniazdowska A, Krasuska U, Czajkowska K, Bogatek R (2010b) Nitric oxide, hydrogen cyanide and ethylene are required in the control of germination and undisturbed development of young apple seedlings. Plant Growth Regul 61: 75-84.
32. Guan L, Scandalios JG (1995) Developmentally related responses of maize catalase genes to salicylic acid. Proc Natl Acad Sci USA 92: 5930-5934.
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 M, Chae HS, Kieber JJ (2009) Regulation of ACS protein stabilization by cytokinin and brassinosteroid. Plant J 57: 606-614.
35. Howell KA, Narsai R, Carroll A, Ivanova A, Lohse M, Usadel B, Millar AH, Whelan J (2009) Mapping metabolic and transcript temporal switches during germination in rice highlights specific transcription factors and the role of RNA instability in the germination process. Plant Physiol 149: 961-980.
36. Ichimura K, Mizoguchi T, Yoshida R, Yuasa T, Shinozaki K (2000) Various abiotic stresses rapidly activate Arabidopsis MAP kinase ATMPK4 and ATMPK6. Plant J 24: 655-665.
37. Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Ann Rev Plant Physiol Plant Mol Biol 47: 377-403.
38. Ishibashi Y, Koda Y, Zheng SH, Yuasa T, Iwaya-Inoue M (2013) Regulation of soybean seed germination through ethylene production in response to reactive oxygen species. Ann Bot 111: 95-102.
39. Ito N, Tomizawa K, Tanaka K, Matsui M, Kendrick RE, Sato T, Nakagawa H (1997) Characterization of 26S proteasome α- and β-type and ATPase subunits from spinach and their expression during early stages of seedling development. Plant Mol Biol 34: 307-316.
40. Jiang Y, Huang B (2002) Protein alterations in tall fescue in response to drought stress and abscisic acid. Crop Sci 42: 202-207.
41. 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.
42. Kandasamy MK, Burgos-Rivera B, McKinney EC, Ruzicka DR (2007) Class-specific interaction of profilin and ADF isovariants with actin in the regulation of plant development. Plant Cell 19: 3111-3126.
43. Kende H (1993) Ethylene biosynthesis. Ann Rev Plant Physiol Plant Mol Biol 44: 283-307.
44. Kepczynski J, Kepczynska E (1997) Ethylene in seed dormancy and germination. Physiol Plant 101: 720-726.
45. Kimura M, Nambara E (2010) Stored and neosynthesized mRNA in Arabidopsis seeds: effects of cycloheximide and controlled deterioration treatment on the resumption of transcription during imbibition. Plant Mol Biol 73: 119-129.
46. Kobayashi M, Ohura I, Kawakita K, Yokota N, Fujiwara M, Shimamoto K, Doke N, Yoshioka H (2007) Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19: 1065-1080.
47. Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci USA 97: 2940-2945.
48. Kranner I, Minibayeva FV, Beckett RP, Seal CE (2010) What is stress? Concepts, definitions and applications in seed science. New Phytol 188: 655-673.
49. Kwak JM, Nguyen V, Schoeder JL (2006) The role of reactive oxygen species in hormonal responses. Plant Physiol 141: 323-329.
50. Liu X, Xing D, Li L, Zhang L (2007) Rapid determination of seed vigor based on the level of superoxide generation during early imbibitions. Photochem Photobiol Sci 6: 767-774.
51. Liu Y, Shi L, Ye N, Liu R, Jia W, Zhang J (2009) Nitric oxide-induced rapid decrease of abscisic acid concentration is required in breaking seed dormancy in Arabidopsis. New Phytol 183: 1030-1042.
52. 2 mediates the regulation of ABA catabolism and GA biosynthesis in Arabidopsis seed dormancy and germination. J Exp Bot 61: 2979-2990.
53. Lozano RM, Wong JH, Yee BC, Peters A, Kobrehel K, Buchanan BB (1996) New evidence for a role of thioredoxin h in germination and seedling development. Planta 200: 100-106.
54. Lu C, Han MH, Guevara-García A, Fedoroff NV (2002) Mitogen-activated protein kinase signaling in postgermination arrest of development by abscisic acid. Proc Natl Acad Sci USA 99: 15812-15817.
55. Maris AF, Kern AL, Picada JN, Boccardi F, Brendel M, Henriques JA (2000) Glutathione, but not transcription factor Yap1, is required for carbon source-dependent resistance to oxidative stress in Saccharomyces cerevisiae. Curr Genet 37: 175-182.
56. Matakiadis T, Alboresi A, Jikumaru Y, Tatematsu K, Pichon O, Renou JP, Kamiya Y, Nambara E, Truong HN (2009) The Arabidopsis abscisic acid catabolic gene CYP707A2 plays a key role in nitrate control of seed dormancy. Plant Physiol 149: 949-960.
57. Matilla AJ (2000) Ethylene in seed formation and germination. Seed Sci Res 10: 111-126.
58. Matilla AJ, Matilla-Vazquez MA (2008) Involvement of ethylene in seed physiology. Plant Sci 175: 87-97.
59. Meinhard M, Grill E (2001) Hydrogen peroxide is a regulator of ABAI1, a protein phosphatase 2C from Arabidopsis. FEBS Lett 508: 443-446.
60. Meinhard M, Rodriguez PL, Grill E (2002) The sensitivity of ABI2 to hydrogen peroxide links abscisic acid-response regulator to redox signalling. Planta 214: 775-782.
61. Miller G, Coutu J, Shulaev V, Mittler R (2008) Reactive oxygen signalling in plants. In: Yang Z (ed) Annual plant reviews, intracellular signaling in plants, vol 33. Wiley-Blackwell, Oxford, pp 189-201.
62. Mishra NS, Tuteja R, Tuteja N (2006) Signaling through MAP kinase networks in plants. Arch Biochem Biophys 452: 55-68.
63. Mittler R, Poulos TL (2008) Ascorbate peroxidase. In: Smirnoff N (ed) Antioxidant and reactive oxygen species in plants. Blackwell Publishing, Oxford, pp 87-100.
64. Mori IC, Murata Y, Uraji M (2009) Integration of ROS and hormole signalling. In: del Río LA, Puppo A (eds) Reactive oxygen species in plant signalling. Springer, Dordrech, pp 25-42.
65. Müller K, Linkies A, Vreeburg RAM, Fry SC (2009) In vivo cell wall loosening by hydroxyl radicals during cross seed germination and elongation growth. Plant Physiol 150: 1855-1865.
66. Munemasa S, Hossain MA, Nakamura Y, Mori IC, Murata Y (2011) The Arabidopsis calcium dependent protein kinase, CPK6, functions as a positive regulator of methyl jasmonate signaling in guard cells. Plant Physiol 155: 553-561.
67. 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.
68. Nambara E, Okamoto M, Tatematsu K, Yano R, Seo M, Kamiya Y (2010) Abscisic acid and the control of seed dormancy and germination. Seed Sci Res 20: 675-689.
69. Nanogaki H, Basel GW, Bewley JD (2010) Germination-still a mystery. Plant Sci 179: 574-581.
70. Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot 53: 1237-1247.
71. 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.
72. Okamoto M, Kuwahara A, Seo M, Kushiro T, Asami T, Hirai N, Kamiya Y, Koshiba T, Nambara E (2006) CYP707A1 and CYP707A2, which encode ABA 8′-hydroxylases, are indispensable for a proper control of seed dormancy and germination in Arabidopsis. Plant Physiol 141: 97-107.
73. Oracz K, El Maarouf-Bouteau H, Farrant JM, Cooper K, Belghazi M, Job C, Job D, Corbineau F, Bailly C (2007) ROS production and protein oxidation as a novel mechanism for seed dormancy alleviation. Plant J 50: 452-465.
74. Oracz K, El Maarouf-Bouteau H, Kranner I, Bogatek R, Corbineau F, Bailly C (2009) The mechanisms involved in seed dormancy alleviation by hydrogen cyanide unravel the role of reactive oxygen species as key factors of cellular signalling during germination. Plant Physiol 150: 494-505.
75. Ortiz-Masia D, Perez-Amador MA, Carbonell P, Aniento F, Carbonell J, Marcote MJ (2008) Characterization of PsMPK2, the first C1 subgroup MAP kinase from pea (Pisum sativum L.). Planta 227: 1333-1342.
76. Palma JM, Sandalio LM, Corpas FJ, Romero-Puertas MC, McCarthy I, del Río LA (2002) Plant proteases, protein degradation, and oxidative stress: role of peroxisomes. Plant Physiol Biochem 40: 521-530.
77. Pandey H, Nandi SK, Nadeem M, Palni LMS (2000) Chemical stimulation of seed germination in Aconitum heterophyllum Wall. and A. balfourii Stapf.: important Himalayan species of medical value. Seed Sci Tech 28: 39-48.
78. Petruzzelli L, Coraggio I, Leubner-Metzger G (2000) Ethylene promotes ethylene biosynthesis during pea seed germination by positive feedback regulation of 1-aminocyclopropane-1-carboxylic acid oxidase. Planta 211: 144-149.
79. Posmyk MM, Corbineau F, Vinel D, Bailly C, Côme D (2001) Osmoconditioning reduces physiological and biochemical damage induced by chilling in soybean seeds. Physiol Plant 111: 473-482.
80. Puntarulo S, Galleano M, Sanchez RA, Boveris A (1991) Superoxide anion and hydrogen peroxide metabolism in soybean embryonic axes during germination. Biochem Biophys Acta 1074: 277-283.
81. Rajjou L, Gallardo K, Debeaujon I, Vandekerckhove J, Job C et al (2004) The effect of α-amanitin on the Arabidopsis seed proteome highlights the distinct roles of stored and neosynthesized mRNAs during germination. Plant Physiol 134: 1598-1613.
82. Rajjou L, Belghazu M, Huget R, Robin C, Moreau A, Job C, Job D (2006) Proteomic investigation of the effect of salicylic acid on Arabidopsis seed germination and establishment of early defense mechanisms. Plant Physiol 141: 910-923.
83. Rajjou L, Duval M, Gallardo K, Catusse J, Bally J, Job C, Job D (2012) Seed germination and vigor. Annu Rev Plant Biol 63: 507-533.
84. Ramachandran S, Christensen HE, Ishimaru Y, Dong CH, Chao MW, Cleary AL (2000) Profilin plays a role in cell elongation, cell shape maintenance, and flowering in Arabidopsis. Plant Physiol 124: 1637-1647.
85. Ranjan R, Lewak S (1995) Interaction of jasmonic and abscisic acid in the control of lipases and proteases in germinating apple embryos. Physiol Plant 93: 421-426.
86. Roach T, Beckett RP, Minibayeva FV, Colville L, Whitaker C, Chen H, 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.
87. Ros-Barceló A, Gómez-Ros LV, Ferrer MA, Hernández JA (2006) The apoplastic antioxidant enzymatic system in the wood-forming tissues of trees. Trees-Struct Funct 20: 145-156.
88. Sassa H, Oguchi S, Inoue T, Hirano H (2000) Primary structural features of the 20S proteasome subunits of rice (Oryza sativa). Gene 250: 61-66.
89. 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.
90. Shakirova FM, Sakhabutdinova AR, Bezrukova MV, Fatkhutdinova RA, Fatkhutdinova DR (2003) Changes in the hormonal status of wheat seedlings induced by salicylic acid and salinity. Plant Sci 164: 317-322.
91. Simontacchi M, Jasid S, Puntarulo S (2004) Nitric oxide generation during early germination of sorghum seeds. Plant Sci 167: 839-847.
92. Singh S, Sawhney VK (1992) Endogenous hormones in seeds, germination behaviour and early seedling characteristics in a normal and ogura cytoplasmic male sterile line of rapeseed (Brassica napus L.). J Exp Bot 43: 1497-1505.
93. Sreenivasulu N, Borisjuk L, Junker BH, Mock HP, Rolletschek H, Seiffert U, Weschke W, Wobus U (2010) Barley grain development: toward an integrative view. Int Rev Cell Mol Biol 281: 49-89.
94. Tanou G, Job C, Rajjou L, Arc E, Belghazi M, Diamantidis G, Molassiotis A, Job D (2009) Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. Plant J 60: 795-804.
95. 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 Exp Bot 52: 1647-1654.
96. Wang P, Song CP (2008) Guard-cell signaling for hydrogen peroxide and abscisic acid. New Phytol 178: 703-718.
97. Wang M, van der Meulen RM, Visser K, van Schaik HP, van Duijn B, de Boer AH (1998) Effects of dormancy-breaking chemicals on ABA levels in barley grain embryos. Seed Sci Res 8: 129-137.
98. Wang WQ, Møller IM, Song SQ (2012) Proteomic analysis of embryogenic axis of Pisum sativum seeds during germination and identification of proteins associated with loss of desiccation tolerance. J Proteomics 77: 68-86.
99. Weitbrecht K, Müller K, Leubner-Metzger G (2011) First on the mark: early seed germination. J Exp Bot 62: 3289-3309.
100. Wrzaczek M, Hirt H (2001) Plant MAP kinase pathways: how many and what for? Biol Cell 93: 81-87.
101. Xie Z, Zhang ZL, Hanzlik S, Cook E, Shen QJ (2007) Salicylic acid inhibits gibberellin-induced alpha-amylase expression and seed germination via a pathway involving an abscisic-acid-inducible WRKY gene. Plant Mol Biol 64: 293-303.
102. Xu HN, Li KZ, Yang FJ, Shi Q, Wang X (2010) Overexpression of CsNMAPK in tobacco enhanced seed germination under salt and osmotic stresses. Mol Biol Rep 37: 3157-3163.
103. Xu Z-Y, Kim DH, Hwang I (2013) ABA homeostasis and signaling involving multiple subcellular compartments and multiple receptors. Plant Cell Rep 32: 807-813. doi: 10. 1007/s00299-013-1396-3.
104. Yamane H, Takagi H, Abe H, Yokota T, Takahashi N (1981) Identification of jasmonic acid in three species of higher plants and its biological activities. Plant Cell Physiol 22: 689-697.
105. Zhang S, Klessig DF (2001) MAPK cascades in plant defense signaling. Trends Plant Sci 6: 520-527.