Proteomic analysis of response to long-term continuous stress in roots of germinating soybean seeds

Journal of Plant Physiology

Volumn 170, Issue 5, 2013, Pages 470-479

  Swigonska, Sylwia ^a   Weidner, Stanislaw ^a  

^a UNIVERSITY OF WARMIA AND MAZURY IN OLSZTYN   (Poland)

Author keywords

Cold stress; Germination; Osmotic stress; Proteomics; Soybean

Indexed keywords

PROTEOME; VEGETABLE PROTEIN;

ARTICLE; GERMINATION; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT ROOT; PLANT SEED; PROTEOMICS; SOYBEAN; TIME; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GERMINATION; PLANT PROTEINS; PLANT ROOTS; PROTEOME; PROTEOMICS; SEEDS; SOYBEANS; STRESS, PHYSIOLOGICAL; TIME FACTORS;

GLYCINE MAX;

EID: 84875532484     PISSN: 01761617     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jplph.2012.11.020     Document Type: Article

References (90)

1. Aarati P., Krishnaprasad B.T., Savitha G.M., Gopalakrishna R., Ramamohan G., Udayakumar M. Expression of an ABA responsive 21kDa protein in finger miller (Eleusine coracana Gaertn.) under stress and its relevance in stress tolerance. Plant Sci 2003, 164:25-34.
2. Adachi M., Takenaka Y., Gidamis A.B., Mikami B., Utsumi S. Crystal structure of soybean proglycinin A1aB1b homotrimer. J Mol Biol 2001, 305(2):291-305.
3. Adams-Phillips L., Briggs A.G., Bent A.F. Disruption of poly(ADP-ribosyl)ation mechanisms alters responses of Arabidopsis thaliana to biotic stress. Plant Physiol 2010, 152:267-280.
4. Aitken A. 14-3-3 proteins: a historic overview. Semin Cancer Biol 2006, 16:162-172.
5. Amor Y., Babiychuk E., Inze D., Levine A. The involvement of poly(ADP-ribose) polymerase in the oxidative stress responses in plants. FEBS Lett 1998, 440:1-7.
6. Ashcroft A.E. Protein and peptide identification: the role of mass spectrometry in proteomics. Nat Prod Rep 2003, 20:202-215.
7. Badowiec A., Swigonska S., Szypulska E., Weidner S. Influence of exogenous abscisic acid on alterations in protein expression in the proteome of Triticosecale seedlings. Acta Physiol Plant 2012, 10.1007/s11738-012-1040-9.
8. Bae M.S., Cho E.J., Choi E.-Y., Park O.K. Analysis of the Arabidopsis nuclear proteome and its response to cold stress. Plant J 2003, 36:652-663.
9. Battaglia M., Olvera-Carrillo Y., Garciarrubio A., Campos F., Covarrubias A.A. The enigmatic LEA proteins and other hydrophilins. Plant Physiol 2008, 148:6-24.
10. Beltran-Pena E., Ortiz-Lopez A., Sanchez de Jimenez E. Synthesis of ribosomal proteins from stored mRNAs early in seed germination. Plant Mol Biol 1995, 28:327-336.
11. Bevan M., Bansroft I., Bent E., Love K., Goodman H., Dean C., et al. Analysis of 1,9Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana. Nature 1998, 391:485-488.
12. Blackman S.A., Obendorf R.L., Leopold A.C. Maturation Proteins and sugars in desiccation tolerance of developing soybean seeds. Plant Physiol 1992, 100:225-230.
13. Bray E.A. Genes commonly regulated by water-deficit stress in Arabidopsis thaliana. J Exp Bot 2009, 55(407):2331-2341.
14. Briat J.-F., Ravet K., Arnaud N., Céline Duc C., Boucherez J., Touraine B., et al. New insights into ferritin synthesis and function highlight a link between iron homeostasis and oxidative stress in plants. Ann Bot 2010, 105(5):811-822.
15. Briggs A.G., Bent A.F. Poly(ADP-ribosyl)ation in plants. Trends Plant Sci 2011, 16(7):372-380.
16. Camoni L., Harper J.F., Palmgreen M.G. 14-3-3 proteins activate a plant calcium-dependent protein kinase (CDPK). FEBS Lett 1998, 430:381-384.
17. Candiano G., Bruschi M., Musante L., Santucci L., Ghiggeri G.M., Carnemolla B., et al. Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 2004, 25:1327-1333.
18. Caruso G., Cavaliere C., Guarino C., Gubbiotti R., Foglia P., Lagana A. Identification of changes in Triticum durum L. leaf proteome in response to salt stress by two-dimensional electrophoresis and MALDI-TOF mass spectrometry. Anal Bioanal Chem 2008, 391:381-390.
19. Chattopadhyay A., Subba P., Pandey A., Bhushan D., Kumar R., Datta A., et al. Analysis of the grasspea proteome and identification of stress-responsive proteins upon exposure to high salinity, low temperature, and abscisic acid treatment. Phytochemistry 2011, 72:1293-1307.
20. Chung H.J., Schenke P.C., Ferl R.J. The 14-3-3 proteins: cellular regulators of plant metabolism. Trends Plant Sci 1999, 9(4):367-371.
21. Clement M., Lambert A., Herouart D., Boncomagni E. Identification of new up-regulated genes under drought stress in soybean nodules. Gene 2008, 426:15-22.
22. Cockcroft S. Phosphatidylinositol transfer proteins couple lipid transport to phosphoinositide synthesis. Semin Cell Dev Biol 2001, 12(2):183-191.
23. Crosby J.S., Vayda M.E. Stress-induced translational control in potato tubers may be mediated by polysome-associated proteins. Plant Cell 1991, 3:1013-1023.
24. Deák M., Horváth G.V., Davletova S., Torok K., Sass L., Vass I., et al. Plants ectopically expressing the iron-binding protein, ferritin, are tolerant to oxidative damage and pathogens. Nat Biotechnol 1999, 17:192-196.
25. Denison F.C., Paul A.-L., Zupanska A.K., Ferl R.J. 14-3-3 proteins in plant physiology. Semin Cell Dev Biol 2011, 22:720-727.
26. Dihazi H., Asif A.R., Agarwal N.K., Doncheva Y., Müller G. Proteomic analysis of cellular response to osmotic stress in thick ascending limb of henle's loop (TALH) cells. Mol Cell Proteomics 2005, 4:1445-1458.
27. Dinakar C., Djilianov D., Bartels D. Photosynthesis in desiccation tolerant plants: energy metabolism andantioxidative stress defense. Plant Sci 2012, 182:29-41.
28. Dixon R.A., Achnine L., Kota P., Liu C.-J., Srinivasa M.S., Wang L. The phenylpropanoid pathway and plant defence - a genomics perspective. Mol Plant Pathol 2002, 3(5):371-390.
29. Dixon R.A., Steele C.L. Flavonoids and isoflavonoids - a gold mine for metabolic engineering. Trends Plant Sci 1999, 4:394-400.
30. Dumont E., Bahrman N., Goulas E., Valot B., Sellier H., Hilbert J.-L., et al. A proteomic approach to decipher chilling response from cold acclimation in pea (Pisum sativum L.). Plant Sci 2011, 180:86-98.
31. Duval M., Loiseau J., Dehaye L., Pepin R., Ledeunff Y., Wang T., et al. SBP65 a seed-specific biotinylated protein, behaves as a LEA protein in developing pea embryos. C R Acad Sci 1996, 319:585-594.
32. Fanucchi F., Alpi E., Olivieri S., Cannistraci C.V., Bachi A., Alpi A., et al. Acclimation increases freezing stress response of Arabidopsis thaliana at proteome level. Biochim Biophys Acta 2012, 1824:813-825.
33. Funatsuki H.H., Kurosaki T., Murakami S., Matsuba K., Kawaguchi S., Yumoto S., et al. Deficiency of a cytosolic ascorbate peroxidase associated with chilling tolerance in soybean. Theor Appl Genet 2003, 106:494-502.
34. Gallardo K., Job C., Groot S.P.C., Puype M., Demol H., Vandekerckhove J., et al. Proteomics of Arabidopsis seed germination: a comparative study of wild-type and gibberellin-deficient seeds. Plant Physiol 2002, 129:823-837.
35. Guo G., Ge P., Ma C., Li X., Lv D., Wang S., et al. Comparative proteomic analysis of salt response proteins in seedling roots of two wheat varieties. J Proteomics 2012, 75:1867-1885.
36. Hanson A.D., Rathinasabapathi B., Rivoal J., Burnet M., Dillon M.O., Gage D.A. Osmoprotective compounds in the Plumbaginaceae: a natural experiment in metabolic engineering of stress tolerance. Proc Natl Acad Sci USA 1994, 91:306-310.
37. Harder A., Wildgruber R., Nawrocki A., Fey S., Larsen P.M., Görg A. Comparison of yeast cell protein solubilization procedures for two-dimensional electrophoresis. Electrophoresis 1999, 20:826-829.
38. Hashida S.N., Takahashi H., Uchimiya H. The role of NAD biosynthesis in plant development and stress responses. Ann Bot 2009, 103:819-824.
39. Hieng B., Ugrinović K., ŠuŠtar-Vozlič J., Kidrič M. Different classes of proteases are involved in the response to drought of Phaseolus vulgaris L. cultivars differing in sensitivity. J Plant Physiol 2004, 161(5):519-530.
40. Huang S.-M., Chuang H.-C., Wu C.-H., Yen G.-C. Cytoprotective effects of phenolic acids on methylglyoxal-induced apoptosis in Neuro-2A cells. Mol Nutr Food Res 2008, 52:940-949.
41. Kalemba E.M., Pukacka S. Possible roles of LEA proteins and sHSPs in seeds protection: a short review. Biol Lett 2007, 44(1):3-16.
42. Kato-Noguchi H. Osmotic stress increase alcohol dehydrogenase activity in maize seedlings. Biol Plant 2000, 43:621-624.
43. Kawaguchi R., Girke T., Bray E.A., Bailey-Serres J. Differential mRNA translation contributes to gene regulation under non-stress and dehydration stress conditions in Arabidopsis thaliana. Plant J 2004, 38:823-839.
44. Kawaguchi R., Williams A., Bray E., Bailey-Serres J. Water-deficit-induced translational control in Nicotiana tabacum. Plant Cell Environ 2003, 26:221-229.
45. Kmieć B., Drynda R., Wołoszyńska M. Molekularne podstawy odpowiedzi roŚlin na niska{ogonek} temperature{ogonek}. Biotechnologia 2005, 70(3):184-200.
46. Kreps J.A., Wu Y., Chang H.S., Zhu T., Wang X., Harper J.F. Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 2002, 130(4):2129-2141.
47. Kurepa J., Toh-e A., Smalle J.A. 26S proteasome regulatory particle mutants have increased oxidative stress tolerance. Plant J 2008, 53:102-114.
48. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
49. Lee D., Ahsan N., Lee S., Lee J., Bahk J., Kang K., et al. Chilling stress-induced proteomic changes in rice roots. J Plant Physiol 2009, 166:1-11.
50. Lee D., Ahsan N., Lee S.-H., Kang K., Lee J.-J., Lee B.-H. An approach to identify cold-induced low-abundant proteins in rice leaf. C R Biol 2007, 330:215-225.
51. Lin D., Tabb D.L., Yates J.R. Large-scale protein identification using mass spectrometry. BBA Proteins Proteomics 2003, 1646:1-10.
52. Liu X., Theil E.C. Ferritin reactions: direct identification of the site for the diferric peroxide reaction intermediate. Proc Natl Acad Sci USA 2004, 101(23):8557-8562.
53. Liu X., Wang Z., Wang L., Wu R., Philips J., Deng X. LEA 4 group genes from the resurrection plant Boea hygrometrica confer dehydration tolerance in transgenic tobacco. Plant Sci 2009, 176:90-98.
54. Mehles P., Schulze-Osthoff K., Arrigo A. Small stress proteins as novel regulators of apoptosis. J Biol Chem 1996, 271(28):16510-16514.
55. Minhas D., Grover A. Transcript levels of genes encoding various glycolytic and fermentation enzymes change in response to abiotic stress. Plant Sci 1999, 146:41-51.
56. Mittler R. Abiotic stress, the field environment and stress combination. Trends Plant Sci 2006, 11(1):15-19.
57. Münz K., Belozerski M.A., Dunaevski Y.E., Schlereth A., Tiedemann J. Stored proteinases and the initiation of storage protein mobilization in seed during germination and seedling growth. J Exp Bot 2001, 52(362):1741-1752.
58. Newman K.D., VanToai T.T. Molecular characterization of the soybean alcohol dehydrogenase gene family amplified in vitro by the polymerase chain reaction. Plant Physiol 1992, 100:489-495.
59. Nieuwland J., Feron R., Huisman B.A.H., Fasolino A., Hilbers C.W., Derksen J., et al. Lipid transfer proteins enhance cell wall extension in tobacco. Plant Cell 2005, 17:2009-2019.
60. Nouri M.-Z., Komatsu S. Comparative analysis of soybean plasma membrane proteins under osmotic stress using gel-based and LC MS/MS-based proteomics approaches. Proteomics 2010, 10:1930-1945.
61. Pappin D.J.C., Hojrup P., Bleasby A.J. Rapid identification of proteins by peptide-mass fingerprinting. Curr Biol 1993, 3:327-332.
62. Phartiyal P., Kim W.-S., Cahoon R.E., Jez J.M., Krishnan H.B. Soybean ATP sulfurylase, a homodimeric enzyme involved in sulphur assimilation, is abundantly expressed in roots and induced by cold treatment. Arch Biochem Biophys 2006, 450:20-29.
63. Phartiyal P., Kim W.-S., Cahoon R.E., Jez J.M., Krishnan H.B. The role of 5'-adenylylsulfate reductase in the sulphur assimilation pathway of soybean: molecular cloning, kinetic characterization and gene expression. Phytochemistry 2008, 69:356-364.
64. Qureshi M.I., Muneer S., Bashir H., Ahmad J., Iqbal M. Chapter 1: nodule physiology and proteomics of stresses legumes. Adv Botanical Res 2010, 56:1-48.
65. Renaut J., Hausman J., Wiśniewski E. Proteomics and low-temperature studies: bridging the gap between gene expression and metabolism. Physiol Plant 2006, 126:97-109.
66. Reumann S., Quan S., Aung K., Yang P., Manandhar-Shrestha K., Holbrook D., et al. In-depth proteome analysis of Arabidopsis leaf peroxisomes combined with in vivo subcellular targeting verification indicates novel metabolic and regulatory functions of peroxisomes. Plant Physiol 2009, 150:125-143.
67. Sakamoto A., Murata N. The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant Cell Environ 2002, 25:163-171.
68. Salekdeh H., Siopongco J., Wade L., Ghareyazie B., Bennett J. A proteomic approach to analyzing drought- and salt-responsiveness in rice. Field Crop Res 2002, 76:199-219.
69. Salekdeh H., Siopongco J., Wade L., Ghareyazie B., Bennett J. Proteomic analysis of rice leaves during drought stress and recovery. Proteomics 2002, 2(9):1131-1145.
70. Sarry J.E., Kuhn L., Lay P.L., Garin J., Bourguinon J. Dynamics of Arabidopsis thaliana soluble proteome in response to different nutrient culture conditions. Electrophoresis 2006, 27:495-507.
71. Schiltz S., Gallardo K., Huart M., Negroni L., Sommerer N., Burstin J. Proteome reference maps of vegetative tissues in pea. An investigation of nitrogen mobilization from leaves during seed filling. Plant Physiol 2004, 135:2241-2260.
72. Schulz P., Neukermans J., Van Der Kelen K., Muhlenbock P., Van Breusegem F., Noctor G., et al. Chemical PARP inhibition enhances growth of Arabidopsis and reduces anthocyanin accumulation and the activation of stress protective mechanisms. PLoS ONE 2012, 7(5):1-13.
73. Shevchenko A., Tomas H., Havlis J., Olsen J.V., Mann M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 2006, 1(6):2856-2860.
74. Solecka D. Role of phenylpropanoid compounds in plant responses to different stress factors. Acta Physiol Plant 1997, 19(3):257-268.
75. Swami A.K., Alam S.I., Sengubta N., Sarin R. Differential proteomic analysis of salt stress response in Sorghum bicolor leaves. Environ Exp Bot 2011, 71:321-328.
76. Szalai G., Kellös T., Galiba G., Kocsy G. Glutathione as an antioxidants and regulatory molecule in plants under abiotic stress conditions. J Plant Growth Regul 2009, 28:66-80.
77. Thomashow M.F. Role of cold-responsive genes in plant freezing tolerance. Plant Physiol 1998, 118:1-8.
78. Vanderauwera S., de Block M., Van de Steene N., van de Cotte B., Metzlaff M. Silencing of poly(ADP-ribose) polymerase in plants alters abiotic stress signal transduction. Proc Natl Acad Sci USA 2007, 104(38):15150-15155.
79. Veeranagamalliah G., Jyothsnakumari G., Thippeswamy M., Reddy P.C.O., Surabhi G.-K., Sriranganayakulu G., et al. Proteomic analysis of salt stress responses in foxtail millet (Setaria italica L. cv. Prasad) seedlings. Plant Sci 2008, 175:631-641.
80. Vincent D., Lapierre C., Pollet B., Cornic G., Negroni L., Zivy M. Water deficit affects caffeate-o-methyltransferase, lignification and related enzymes in maize leaves. A proteomic investigation. Plant Physiol 2005, 137:949-960.
81. Waditee R., Bhuiyan N.H., Rai V., Aoki K., Tanaka Y., Hibino T., et al. Genes for direct methylation of glycine provide high levels of glycinebetaine and abiotic-stress tolerance in Synechococcus and Arabidopsis. Proc Natl Acad Sci USA 2005, 102(5):1318-1323.
82. Whitley D., Goldberg S.P., Jordan W.D. Heat shock proteins: a review of the molecular chaperones. J Vasc Surg 1999, 29(4):748-751.
83. Williams B.A., Tsang A. Nucleotide sequence of an abscisic acid-responsive, embryo-specific maize gene. Plant Physiol 1992, 100:1067-1068.
84. Wisniewski M., Close T.J., Artlip T., Arora R. Seasonal patterns of dehydrins and 70-kDa heat-shock proteins in bark tissue of eight species of woody plants. Physiol Plant 1996, 96:496-505.
85. Witte C.-P., Isidore E., Tiller S.A., Davies H.V., Taylor M.A. Functional characterization of urease accessory protein G (ureG) from potato. Plant Mol Biol 2001, 45:169-179.
86. Yang P., Li X., Wang X., Chen H., Chen F., Shen S. Proteomic analysis of rice (Oryza sativa) seeds during germination. Proteomics 2007, 7:3358-3368.
87. Yoshimura K., Masuda A., Kuwano M., Yokota A., Akashi K. Programmed proteome response for drought avoidance/tolerance in the root of a C3 xenophyte (wild watermelon) under water deficits. Plant Cell Physiol 2008, 49(2):226-241.
88. Yu C.K.Y., Springob K., Schmidt J., Nicholson R.L., Chu I.K., Yip W.K., et al. A stilbene synthase gene (SbSTS1) is involved in host and non-host defense responses in sorghum. Plant Physiol 2005, 138:393-401.
89. Zang X., Komatsu S. A proteomic approach for identifying osmotic-stress-related proteins in rice. Phytochemistry 2007, 68:426-437.
90. Zhang S., Klessig D.F. MAPK cascades in plant defense signaling. Trends Plant Sci 2001, 6:520-528.