Comparative proteomics illustrates the complexity of drought resistance mechanisms in two wheat (Triticum aestivum L.) cultivars under dehydration and rehydration

BMC Plant Biology

Volumn 16, Issue 1, 2016, Pages

  Cheng, Lixiang ^a   Wang, Yuping ^a   He, Qiang ^a   Li, Huijun ^a,b   Zhang, Xiaojing ^a,c   Zhang, Feng ^a  

^a GANSU AGRICULTURAL UNIVERSITY   (China)

^b Wuwei Agricultural and Animal Husbandry Bureau   (China)

^c Gansu Dingxi Academy of Agricultural Science   (China)

Author keywords

2 DE; Differentially abundant proteins; Drought stress; MALDI TOF TOF; Proteomics; Wheat

Indexed keywords

PLANT PROTEIN; PROTEOME; WATER;

CHEMISTRY; COMPARATIVE STUDY; DROUGHT; GENE EXPRESSION REGULATION; GENETICS; MATRIX-ASSISTED LASER DESORPTION-IONIZATION MASS SPECTROMETRY; METABOLISM; PHOTOSYNTHESIS; PROTEOMICS; TWO DIMENSIONAL GEL ELECTROPHORESIS; WHEAT;

DROUGHTS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION REGULATION, PLANT; PHOTOSYNTHESIS; PLANT PROTEINS; PROTEOME; PROTEOMICS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TRITICUM; WATER;

EID: 84984652701     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/s12870-016-0871-8     Document Type: Article

References (155)

1. Wang W, Vinocur B, Altman A. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta. 2003;218:1-14.
2. Tardif G, Kane NA, Adam H, Labrie L, Major G, Gulick P, Sarhan F, Laliberté JF. Interaction network of proteins associated with abiotic stress response and development in wheat. Plant Mol Biol. 2007;63:703-18.
3. The International Wheat Genome Sequencing Consortium (IWGSC). A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science. 2014. doi: 10.1126/science.1251788.
4. Wilkinson S, Davies WJ. Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant Cell Environ. 2010;33:510-25.
5. Lee SC, Luan S. ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant Cell Environ. 2012;35:53-60.
6. Hossain Z, Nouri MZ, Komatsu S. Plant cell organelle proteomics in response to abiotic stress. J Proteome Res. 2012;11:37-48.
7. Chaves MM, Maroco JP, Pereira JS. Understanding plant responses to drought from genes to the whole plant. Funct Plant Biol. 2003;30:239-74.
8. Mahajan S, Tuteja N. Cold, salinity and drought stresses: an overview. Arch Biochem Biophys. 2005;444:139-58.
9. Bhushan D, Pandey A, Choudhary MK, Datta A, Chakraborty S, Chakraborty N. Comparative proteomics analysis of differentially expressed proteins in chickpea extracellular matrix during dehydration stress. Mol Cell Proteomics. 2007;6:1868-84.
10. Reddy AR, Chaitanya KV, Vivekanandan M. Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol. 2004;161:1189-202.
11. Zang X, Komatsu S. A proteomic approach for identifying osmotic-stress-related proteins in rice. Phytochemistry. 2007;68:426-37.
12. Cui SX, Hu J, Yang B, Shi L, Huang F, Tsai SN, et al. Proteomic characterization of Phragmites communis in ecotypes of swamp and desert dune. Proteomics. 2009;9:3950-67.
13. Ramanjulu S, Bartels D. Drought- and desiccation-induced modulation of gene expression in plants. Plant Cell Environ. 2002;25:141-51.
14. Bartels D, Sunkar R. Drought and salt tolerance in plants. Crit Rev Plant Sci. 2005;24:23-58.
15. Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, et al. Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell. 2006;18:1292-309.
16. Nakashima K, Ito Y, Yamaguchi-Shinozaki K. Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol. 2009;149:88-95.
17. Morran S, Eini O, Pyvovarenko T, Parent B, Singh R, Ismagul A, et al. Improvement of stress tolerance of wheat and barley by modulation of expression of DREB/CBF factors. Plant Biotechnol J. 2011;9:230-49.
18. Xue GP, Way HM, Richardson T, Drenth J, Joyce PA, McIntyre CL. Overexpression of TaNAC69 leads to enhanced transcript levels of stress up-regulated genes and dehydration tolerance in bread wheat. Mol Plant. 2011;4:697-712.
19. Rahaie M, Xue GP, Naghavi MR, Alizadeh H, Schenk PM. A MYB gene from wheat (Triticum aestivum L.) is up-regulated during salt and drought stresses and differentially regulated between salt-tolerant and sensitive genotypes. Plant Cell Rep. 2010;29:835-44.
20. Pandey A, Chakraborty S, Datta A, Chakraborty N. Proteomics approach to identify dehydration responsive nuclear proteins from chickpea (Cicer arietinum L.). Mol Cell Proteomics. 2008;7:88-107.
21. Choudhary MK, Basu D, Datta A, Chakraborty N, Chakraborty S. Dehydration-responsive nuclear proteome of rice (Oryza sativa L.) illustrates protein network, novel regulators of cellular adaptation, and evolutionary perspective. Mol Cell Proteomics. 2009;8:1579-98.
22. Timperio AM, Egidi G, Zolla L. Proteomics applied on plant abiotic stresses: Role of heat shock proteins (HSP). J Proteomics. 2008;71:391-411.
23. Rorat T. Plant dehydrins - tissue location, structure and function. Cell Mol Biol Lett. 2006;11:536-56.
24. Lopez CG, Banowetz GM, Peterson CJ, Kronstad WE. Dehydrin expression and drought tolerance in seven wheat cultivars. Crop Sci. 2003;43:577-82.
25. Rampino P, Pataleo S, Gerardi C, Mita G, Perrotta C. Drought stress response in wheat: physiological and molecular analysis of resistant and sensitive genotypes. Plant Cell Environ. 2006;29:2143-52.
26. Muñoz-Mayor A, Pineda B, Garcia-Abellán JO, Antón T, Garcia-Sogo B, Sanchez-Bel P, et al. Overexpression of dehydrin tas14 gene improves the osmotic stress imposed by drought and salinity in tomato. J Plant Physiol. 2012;169:459-68.
27. Imamura T, Higuchi A, Takahashi H. Dehydrins are highly expressed in overwintering buds and enhance drought and freezing tolerance in Gentiana triflora. Plant Sci. 2013;213:55-66.
28. Vaseva II, Anders I, Feller U. Identification and expression of different dehydrin subclasses involved in the drought response of Trifolium repens. J Plant Physiol. 2014;171:213-24.
29. Mohammadi M, Kav NN, Deyholos MK. Transcript expression profile of water-limited roots of hexaploid wheat (Triticum aestivum 'Opata'). Genome. 2008;51:357-67.
30. Aprile A, Mastrangelo AM, De Leonardis AM, Galiba G, Roncaglia E, Ferrari F, et al. Transcriptional profiling in response to terminal drought stress reveals differential responses along the wheat genome. BMC Genomics. 2009;10:279.
31. Ergen NZ, Budak H. Sequencing over 13000 expressed sequence tags from six subtractive cDNA libraries of wild and modern wheats following slow drought stress. Plant Cell Environ. 2009;32:220-36.
32. Wang J, Ding B, Guo Y, Li M, Chen S, Huang G, et al. Overexpression of a wheat phospholipase D gene, TaPLDα, enhances tolerance to drought and osmotic stress in Arabidopsis thaliana. Planta. 2014;240:103-15.
33. Manaa A, Ben Ahmed H, Valot B, Bouchet JP, Aschi-Smiti S, Causse M, et al. Salt and genotype impact on plant physiology and root proteome variations in tomato. J Exp Bot. 2011;62:2797-813.
34. Mohammadi M, Kav NN, Deyholos MK. Transcriptional profiling of hexaploid wheat (Triticum aestivum L.) roots identifies novel, dehydration-responsive genes. Plant Cell Environ. 2007;30:630-45.
35. Ergen NZ, Thimmapuram J, Bohnert HJ, Budak H. Transcriptome pathways unique to dehydration tolerant relatives of modern wheat. Funct Integr Genomics. 2009;9:377-96.
36. Sečenji M, Lendvai Á, Miskolczi P, Kocsy G, Gallé Á, Szucs A, et al. Differences in root functions during long-term drought adaptation: comparison of active gene sets of two wheat genotypes. Plant Biol (Stuttg). 2010;12:871-82.
37. Aprile A, Havlickova L, Panna R, Marè C, Borrelli GM, Marone D, et al. Different stress responsive strategies to drought and heat in two durum wheat cultivars with contrasting water use efficiency. BMC Genomics. 2013;14:821.
38. Fleury D, Jefferies S, Kuchel H, Langridge P. Genetic and genomic tools to improve drought tolerance in wheat. J Exp Bot. 2010;61:3211-22.
39. Pradet-Balade B, Boulme F, Beug H, Muliner EW, Garcia-Sanz JA. Translation control: bridging the gap between genomics and proteomics? Trends Biochem Sci. 2001;26:225-9.
40. Agrawal L, Chakraborty S, Jaiswal DK, Gupta S, Datta A, Chakraborty N. Comparative proteomics of tuber induction, development and maturation reveal the complexity of tuberization process in potato (Solanum tuberosum L.). J Proteome Res. 2008;7:3803-17.
41. Ford KL, Cassin A, Bacic A. Quantitative proteomic analysis of wheat cultivars with differing drought stress tolerance. Front Plant Sci. 2011;2:1-11.
42. Bazargani MM, Sarhadi E, Bushehri AA, Matros A, Mock HP, Naghavi MR, et al. A proteomics view on the role of drought-induced senescence and oxidative stress defense in enhanced stem reserves remobilization in wheat. J Proteomics. 2011;74:1959-73.
43. Ge P, Ma C, Wang S, Gao L, Li X, Guo G, et al. Comparative proteomic analysis of grain development in two spring wheat varieties under drought stress. Anal Bioanal Chem. 2012;402:1297-313.
44. Hao P, Zhu J, Gu A, Lv D, Ge P, Chen G, et al. An integrative proteome analysis of different seedling organs in tolerant and sensitive wheat cultivars under drought stress and recovery. Proteomics. 2014. doi: 10.1002/pmic.201400179.
45. Faghani E, Gharechahi J, Komatsu S, Mirzaei M, Khavarinejad RA, Najafi F, et al. Comparative physiology and proteomic analysis of two wheat genotypes contrasting in drought tolerance. J Proteomics. 2015;114:1-15.
46. Bates LS, Waldren RP, Teare ID. Rapid determination of free proline for water stress studies. Plant Soil. 1973;39:205-7.
47. Hodges DM, DeLong JM, Forney CF, Prange RK. Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta. 1999;207:604-11.
48. Yan SP, Zhang QY, Tang ZC, Su WA, Sun WN. Comparative proteomic analysis provides new insights into chilling stress responses in rice. Mol Cell Proteomics. 2006;5:484-96.
49. Veljovic-Jovanovic S, Noctor G, Foyer CH. Are leaf hydrogen peroxide concentrations commonly overestimated? The potential influence of artefactual interference by tissue phenolics and ascorbate. Plant Physiol Biochem. 2002;40:501-7.
50. Beyer WF, Fridovich I. Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem. 1987;161:559-66.
51. Aebi H. Catalase in vitro. Methods Enzymol. 1984;105:121-6.
52. Donnelly BE, Madden RD, Ayoubi P, Porter DR, Dillwith JW. The wheat (Triticum aestivum L.) leaf proteome. Proteomics. 2005;5:1624-33.
53. Chaves MM, Flexas J, Pinheiro C. Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot. 2009;103:551-60.
54. Kosová K, Vítámvás P, Prásil IT, Renaut J. Plant proteome changes under abiotic stress -- contribution of proteomics studies to understanding plant stress response. J Proteomics. 2011;74:1301-22.
55. Danshina PV, Schmalhausen EV, Avetisyan AV, Muronetz VI. Mildly oxidized glyceraldehydes-3-phosphate dehydrogenase as a possible regulator of glycolysis. IUBMB Life. 2001;51:309-14.
56. Bedhomme M, Adamo M, Marchand CH, Couturier J, Rouhier N, Lemaire SD, et al. Glutathionylation of cytosolic glyceraldehyde-3-phosphate dehydrogenase from the model plant Arabidopsis thaliana is reversed by both glutaredoxins and thioredoxins in vitro. Biochem J. 2012;445:337-47.
57. 2 resistance. Proteomics. 2012;12:1792-805.
58. Wierenga RK, Kapetaniou EG, Venkatesan R. Triosephosphate isomerise: a highly evolved biocatalyst. Cell Mol Life Sci. 2010;67:3961-82.
59. Riccardi F, Gazeau P, de Vienne D, Zivy M. Protein changes in response to progressive water deficit in maize: quantitative variation and polypeptide identification. Plant Physiol. 1998;117:1253-63.
60. Salekdeh GH, Siopongco J, Wade LJ, Ghareyazie B, Bennett J. Proteomics analysis of rice leaves during drought stress and recovery. Proteomics. 2002;2:1131-45.
61. Umeda M, Hara C, Matsubayashi Y, Li HH, Liu Q, Tadokoro F, et al. Expressed sequence tags from cultured cells of rice (Oryza sativa L.) under stressed conditions: analysis of transcripts of genes engaged in ATP-generating pathways. Plant Mol Biol. 1994;25:469-78.
62. Fei G, Zhou Y, Huang L, He D, Zhang G. Proteomic analysis of long-term salinity stress-responsive proteins in Thellungiella halophila leaves. Chinese Sci Bull. 2008;53:3530-7.
63. Pandey S, Rai R, Rai LC. Proteomics combines morphological, physiological and biochemical attributes to unravel the survival strategy of Anabaena sp. PCC7120 under arsenic stress. J Proteomics. 2012;75:921-37.
64. Brugiere N, Dubois F, Limami AM, Lelandais M, Roux Y, Sangwan RS, et al. Glutamine synthetase in the phloem plays a major role in controlling proline production. Plant Cell. 1999;11:1995-2012.
65. Gadaleta A, Nigro D, Giancaspro A, Blanco A. The glutamine synthetase (GS2) genes in relation to grain protein content of durum wheat. Funct Integr Genomics. 2011;11:665-70.
66. Díaz P, Betti M, Sánchez DH, Udvardi MK, Monza J, Márquez AJ. Deficiency in plastidic glutamine synthetase alters proline metabolism and transcriptomic response in Lotus japonicus under drought stress. New Phytol. 2010;188:1001-13.
67. Roje S. S-Adenosyl-L-methionine: beyond the universal methyl group donor. Phytochemistry. 2006;67:1686-98.
68. Roeder S, Dreschler K, Wirtz M, Cristescu SM, van Harren FJ, Hell R, et al. SAM levels, gene expression of SAM synthetase, methionine synthase and ACC oxidase, and ethylene emission from N. suaveolens flowers. Plant Mol Biol. 2009;70:535-46.
69. Mayne MB, Coleman JR, Blumwald E. Differential expression during drought conditioning of a root-specific S-adenosylmethionine synthetase from jack pine (Pinus banksiana Lamb.) seedlings. Plant Cell Environ. 1996;19:958-66.
70. Quiroga M, Guerrero C, Botella MA, Ros Barceló A, Amaya I, Medina MI, et al. A tomato peroxidase involved in the synthesis of lignin and suberin. Plant Physiol. 2000;122:1119-27.
71. Sánchez-Aguayo I, Rodríguez-Galán JM, García R, Torreblanca J, Pardo JM. Salt stress enhances xylem development and expression of S-adenosyl-l-methionine synthase in lignifying tissues of tomato plants. Planta. 2004;220:278-85.
72. Yan XL, Liao H, Trull MC, Beebe SE, Lynch JP. Induction of a major leaf acid phosphatase does not confer adaptation to low phosphorus availability in common bean. Plant Physiol. 2001;125:1901-11.
73. Yun SJ, Kaeppler SM. Induction of maize acid phosphatase activities under phosphorus starvation. Plant Soil. 2001;237:109-15.
74. Tian J, Liao H, Wang X, Cao A, Yan XL. Phosphorus starvation-induced expression of leaf acid phosphatase isoforms in soybean. Acta Bot Sin. 2003;45:1037-42.
75. Tsuji H, Meguro N, Suzuki Y, Tsutsumi N, Hirai A, Nakazono M. Induction of mitochondrial aldehyde dehydrogenase by submergence facilitates oxidation of acetaldehyde during re-aeration in rice. FEBS Lett. 2003;546:369-73.
76. Marchitti SA, Brocker C, Stagos D, Vasiliou V. Non-P450 aldehyde oxidizing enzymes: the aldehyde dehydrogenase superfamily. Expert Opin Drug Metab Toxicol. 2008;4:697-720.
77. Sunkar R, Bartels D, Kirch HH. Overexpression of a stress-inducible aldehyde dehydrogenase gene from Arabidopsis thaliana in transgenic plants improves stress tolerance. Plant J. 2003;35:452-64.
78. Shiraishi T, Fukusaki E, Kobayashi A. Formate dehydrogenase in rice plant: growth stimulation effect of formate in rice plant. J Biosci Bioeng. 2000;89:241-6.
79. Alekseeva AA, Savin SS, Tishkov VI. NAD(+)-dependent formate dehydrogenase from plants. Acta Nat. 2011;3:38-54.
80. Bykova NV, Stensballe A, Egsgaard H, Jensen ON, Moller IM. Phosphorylation of formate dehydrogenase in potato tuber mitochondria. J Biol Chem. 2003;278:26021-30.
81. Lehner I, Niehof M, Borlak J. An optimized method for the isolation and identification of membrane proteins. Electrophoresis. 2003;24:1795-808.
82. Heide H, Kalisz HM, Follmann H. The oxygen evolving enhancer protein 1 (OEE) of photosystem II in green algae exhibits thioredoxin activity. J Plant Physiol. 2004;161:139-49.
83. Marin-Navarro J, Moreno J. Modification of the proteolytic fragmentation pattern upon oxidation of cysteines from ribulose-1,5-bisphosphate carboxylase/oxygenase. Biochemistry. 2003;42:14930-8.
84. 2 concentration. New Phytol. 2006;172:73-82.
85. Galmés J, Aranjuelo I, Medrano H, Flexas J. Variation in Rubisco content and activity under variable climatic factors. Photosynth Res. 2013;117:73-90.
86. Nakahara K, Yamamoto H, Miyake C, Yokota A. Purification and characterization of class-I and class-II fructose-1,6-bisphosphate aldolase from the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol. 2003;44:326-33.
87. Patron NJ, Rogers MB, Keeling PJ. Gene replacement of fructose-1,6-bisphosphate aldolase supports the hypothesis of a single photosynthetic ancestor of chromalveolates. Eukaryot Cell. 2004;3:1169-75.
88. Yamazaki S, Nomata J, Fujita Y. Differential operation of dual protochlorophyllide reductases for chlorophyll biosynthesis in response to environmental oxygen levels in the cyanobacterium Leptolyngbya boryana. Plant Physiol. 2006;142:911-22.
89. Sakuraba Y, Rahman L, Cho SH, Kim YS, Koh HJ, Yoo SC, et al. The rice faded green leaf locus encodes protochlorophyllide oxidoreductase B and is essential for chlorophyll synthesis under high light conditions. Plant J. 2013;74:122-33.
90. Reinbothe S, Reinbothe C. The regulation of enzymes involved in chlorophyll biosynthesis. Eur J Biochem. 1996;237:323-43.
91. Shepherd M, Reid JD, Hunter CN. Purification and kinetic characterization of the magnesium protoporphyrin IX methyltransferase from Synechocystis PCC6803. Biochem J. 2003;371:351-60.
92. Jiang GQ, Wang Z, Shang HH, Yang WL, Hu ZA, Phillips J, et al. Proteome analysis of leaves from the resurrection plant Boea hygrometrica in response to dehydration and rehydration. Planta. 2007;225:1405-20.
93. Frova C. The plant glutathione transferase gene family: genomic structure, functions, expression and evolution. Physiol Plantarum. 2003;119:469-79.
94. Frova C. Glutathione transferases in the genomics era: New insights and perspectives. Biomol Eng. 2006;23:149-69.
95. Margis R, Dunand C, Teixeira FK, Margis-Pinheiro M. Glutathione peroxidase family: an evolutionary overview. J FEBS. 2008;275:3959-70.
96. Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem. 2010;48:909-30.
97. Suzuki N, Koussevitzky S, Mittler R, Miller G. ROS and redox signaling in the response of plants to abiotic stress. Plant Cell Environ. 2011;35:259-70.
98. Raven EL, Lad L, Sharp KH, Mewies M, Moody PC. Defining substrate specificity and catalytic mechanism in ascorbate peroxidase. Biochem Soc Symp. 2004;71:27-38.
99. Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, et al. Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell. 2005;17:268-81.
100. Morgan MJ, Lehmann M, Schwarzländer M, Baxter CJ, Sienkiewicz-Porzucek A, Williams TC, et al. Decrease in manganese superoxide dismutase leads to reduced root growth and affects tricarboxylic acid cycle flux and mitochondrial redox homeostasis. Plant Physiol. 2008;147:101-14.
101. Miriyala S, Spasojevic I, Tovmasyan A, Salvemini D, Vujaskovic Z, St Clair D, et al. Manganese superoxide dismutase, MnSOD and its mimics. Biochim Biophys Acta. 1822;2012:794-814.
102. Franklin CC, Backos DS, Mohar I, White CC, Forman HJ, Kavanagh TJ. Structure, function, and post-translational regulation of the catalytic and modifier subunits of glutamate cysteine ligase. Mol Aspects Med. 2009;30:86-98.
103. Lu SC. Regulation of glutathione synthesis. Mol Aspects Med. 2009;30:42-59.
104. Ganapathi S, Chidambaram P, Natarajan S, Vengoji R, Karuppannan V. Combined expression of chitinase and β-1,3-glucanase genes in indica rice (Oryza sativa L.) enhances resistance against Rhizoctonia solani. Plant Sci. 2008;175:283-90.
105. Meirinho S, Carvalho M, Dominguez Á, Choupina A. Isolation and characterization by asymmetric PCR of the ENDO1 gene for glucan endo-1,3-β-D-glucosidase in Phytophthora cinnamomi associated with the ink disease of Castanea sativa Mill. Braz Ach Bol Technol. 2010;53:513-8.
106. Chen AP, Wang GL, Qu ZL, Lu CX, Liu N, Wang F, et al. Ectopic expression of ThCYP1, a stress-resposive cyclophilin gene from Thellungiella halophila, confers salt tolerance in fission yeast and tobacco cells. Plant Cell Rep. 2007;26:237-45.
107. Gan PH, Shan W, Blackman LM, Hardham AR. Characterization of cyclophilin-encoding genes in phytophthora. Mol Genet Genomics. 2009;281:565-78.
108. Weng XY, Huang YY, Gao H, Sun JY. Characterization of a xylanase inhibitor TAXI-I from wheat. Biol Plantarum. 2010;54:154-8.
109. Moscetti I, Tundo S, Janni M, Sella L, Gazzetti K, Tauzin A, et al. Constitutive expression of the xylanase inhibitor TAXI-III delays Fusarium head blight symptoms in durum wheat transgenic plants. Mol Plant Microbe Interact. 2013;26:1464-72.
110. Hemant RK, Anil KS, Sudhir KS, Sneh LSP, Ashwani P. Genome wide expression analysis of CBS domain containing proteins in Arabidopsis thaliana (L.) Heynh and Oryza sativa L. reveals their developmental and stress regulation. BMC Genomics. 2009;10:200.
111. Singh AK, Kumar R, Pareek A, Sopory SK, Singla-Pareek SL. Overexpression of rice CBS domain containing protein improves salinity, oxidative, and heavy metal tolerance in transgenic tobacco. Mol Biotechnol. 2012;52:205-16.
112. Youssef A, Laizet Y, Block MA, Marechal E, Alcaraz JP, Larson TR, et al. Plant lipid-associated fibrillin proteins condition jasmonate production under photosynthetic stress. Plant J. 2009;61:436-45.
113. Recklies AD, White C, Ling H. The chitinase 3-like protein human cartilage glycoprotein 39 (HC-gp39) stimulates proliferation of human connective-tissue cells and activates both extracellular signal-regulated kinase- and protein kinase B-mediated signalling pathways. Biochem J. 2002;365:119-26.
114. Liu JJ, Sturrock R, Ekramoddoullah AK. The superfamily of thaumatin-like proteins: its origin, evolution, and expression towards biological function. Plant Cell Rep. 2010;29:419-36.
115. Leyva JA, Bianchet MA, Amzel LM. Understanding ATP synthesis: structure and mechanism of the F1-ATPase (Review). Mol Membr Biol. 2003;20:27-33.
116. Itoh H, Takahashi A, Adachi K, Noji H, Yasuda R, Yoshida M, et al. Mechanically driven ATP synthesis by F1-ATPase. Nature. 2004;427:465-8.
117. Christie AH, Allen GG, Gregory JT. Induction of vacuolar ATPase and mitochondrial ATP synthase by aluminum in an aluminum-resistant cultivar of wheat. Plant Physiol. 2001;125:2068-77.
118. Zhang XX, Takano T, Liu SK. Identification of a mitochondrial ATP synthase small subunit gene (RMtATP6) expressed in response to salts and osmotic stresses in rice (Oryza sativa L.). J Exp Bot. 2006;57:193-200.
119. Zhang XX, Liu SK, Takano T. Overexpression of a mitochondrial ATP synthase small subunit gene (AtMtATP6) confers tolerance to several abiotic stresses in Saccharomyces cerevisiae and Arabidopsis thaliana. Biotechnol Lett. 2008;30:1289-94.
120. Dzeja PP, Terzic A. Adenylate kinase and AMP signaling networks: metabolic monitoring, signal communication and body energy sensing. Int J Mol Sci. 2009;10:1729-72.
121. Singh BN, Mishra RN, Agarwal PK, Goswami M, Nair S, Sopory SK, et al. A pea chloroplast translation elongation factor that is regulated by abiotic factors. Biochem Biophys Res Commun. 2004;320:523-30.
122. Wan XY, Liu JY. Comparative proteomics analysis reveals an intimate protein network provoked by hydrogen peroxide stress in rice seedling leaves. Mol Cell Proteomics. 2008;7:1469-88.
123. Ristic Z, Momcilović I, Fu J, Callegari E, DeRidder BP. Chloroplast protein synthesis elongation factor, EF-Tu, reduces thermal aggregation of rubisco activase. J Plant Physiol. 2007;164:1564-71.
124. Margus T, Remm M, Tenson T. A computational study of elongation factor G (EFG) duplicated genes: diverged nature underlying the innovation on the same structural template. PLoS One. 2011;6:e22789.
125. Ma H, Song L, Shu Y, Wang S, Niu J, Wang Z, et al. Comparative proteomic analysis of seedling leaves of different salt tolerant soybean genotypes. J Proteomics. 2012;75:1529-46.
126. Rodnina M, Wintermeyer W. The ribosome as a molecular machine: the mechanism of tRNA-mRNA movement in translocation. Biochem Soc Trans. 2011;39:658-62.
127. Xu M, Wang Y, Chen L, Pan B, Chen F, Fang Y, et al. Down-regulation of ribosomal protein S15A mRNA with a short hairpin RNA inhibits human hepatic cancer cell growth in vitro. Gene. 2014;536:84-9.
128. Palma JM, Sandalio LM, Corpas FJ, Romero-Puertas MC, McCarthy I, del Río LA. Plant proteases, protein degradation, and oxidative stress: role of peroxisomes. Plant Physiol Bioch. 2002;40:521-30.
129. Chamieh H, Marty V, Guetta D, Perollier A, Franzetti B. Stress regulation of the PAN-proteasome system in the extreme halophilic archaeon Halobacterium. Extremophiles. 2012;16:215-25.
130. Pang QY, Chen SX, Dai SJ, Chen YZ, Wang Y, Yan XF. Comparative proteomics of salt tolerance in Arabidopsis thaliana and Thellungiella halophila. J Proteome Res. 2010;9:2584-99.
131. Wang W, Vinocur B, Shoseyov O, Altman A. Role of plant heatshock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci. 2004;9:244-52.
132. Feng JT, Liu YK, Song HY, Dai Z, Qin LX, Almofti MR, et al. Heat-shock protein 27: a potential biomarker for hepatocellular carcinoma identified by serum proteome analysis. Proteomics. 2005;5:4581-8.
133. Jiang Y, Yang B, Harris NS, Deyholos MK. Comparative proteomics analysis of NaCl stress-responsive proteins in Arabidopsis roots. J Exp Bot. 2007;58:3591-607.
134. Cheng LX, Zhang X, Zhao QX, Li HJ, Wang YP, Wang DX, et al. Comparative proteomic analysis of cold-induced sweetening in potato (Solanum tuberosum L.) tuber. Acta Physiol Plant. 2014;36:1197-210.
135. Cuéllar J, Perales-Calvo J, Muga A, Valpuesta JM, Moro F. Structural insights into the chaperone activity of the 40-kDa heat shock protein DnaJ: binding and remodeling of a native substrate. J Biol Chem. 2013;288:15065-74.
136. Maruyama T, Furuani M. Archael Peptidyl-Prolyl cis/trans Isomerases (PPIases). Front Biosci. 2000;5:821-36.
137. Pemberton TJ. Identification and comparative analysis of sixteen fungal peptidyl-prolyl cis/trans isomerase repertoires. BMC Genomics. 2006;7:244.
138. Hoogenboom BW, Suda K, Engel A, Fotiadis D. The supramolecular assemblies of voltage-dependent anion channels in the native membrane. J Mol Biol. 2007;370:246-55.
139. De Pinto V, Messina A, Lane DJR, Lawen A. Voltage-dependent anion-selective channel (VDAC) in the plasma membrane. FEBS Lett. 2010;584:1793-9.
140. +-ATPase subunit B cloning and its involvementin salt tolerance. Planta. 2011;234:1-7.
141. Agarwal P, Reddy MK, Sopory SK, Agarwal PK. Plant rabs: characterization, functional diversity, and role in stress tolerance. Plant Mol Biol Rep. 2009;27:417-30.
142. Pollard TD. Regulation of actin filament assembly by Arp2/3 complex and formins. Annu Rev Biophys Biomol Struct. 2007;36:451-77.
143. Pollard TD, Cooper JA. Actin, a central player in cell shape and movement. Science. 2009;326:1208-12.
144. Nakamura K, Zuppini A, Arnaudeau S, Lynch J, Ahsan I, Krause R, et al. Functional specialization of calreticulin domains. J Cell Biol. 2001;154:961-72.
145. Chen MH, Tain GW, Gafni Y, Citovsky V. Effects of calreticulin on viral cell-to-cell movement. Plant Physiol. 2005;138:1866-76.
146. Jia XY, Xu CY, Jing RL, Jing RL, Li RZ, Mao XG, et al. Molecular cloning and characterization of wheat calreticulin (CRT) gene involved in drought-stressed responses. J Exp Bot. 2008;59:739-51.
147. Komatsu S, Yamada E, Furukawa K. Cold stress changes the concanavalin A - positive glycosylation pattern of proteins expressed in the basal parts of rice leaf sheaths. Amino Acids. 2009;36:115-23.
148. Pan YX, Wang XF, Liu HW, Zhang GY, Ma ZY. Molecular cloning of three UDP-glucuronate decarboxylase genes that are preferentially expressed in Gossypium fibers from elongation to secondary cell wall synthesis. J Plant Biol. 2010;53:367-73.
149. Yan J, Wang J, Zhang H. An ankyrin repeat-containing protein plays a role in both disease resistance and antioxidation metabolism. Plant J. 2002;29:193-202.
150. Wolpert TJ, Navarre DA, Moore DL, Macko V. Identification of the 100-kD victorin binding protein from oats. Plant Cell. 1994;6:1145-55.
151. Liang L, Lai Z, Ma W, Zhang Y, Xue Y. AhSL28, a senescence- and phosphate starvation-induced S-like RNase gene in Antirrhinum. Biochim Biophys Acta. 2002;1579:64-71.
152. Hugot K, Ponchet M, Marais A, Ricci P, Galiana E. A tobacco S-like RNase inhibits hyphal elongation of plant pathogens. Mol Plant Microbe Interact. 2002;15:243-50.
153. Zheng J, Wang YY, He YN, Zhou JJ, Li YP, Liu QQ, et al. Overexpression of an S-like ribonuclease gene, OsRNS4, confers enhanced tolerance to high salinity and hyposensitivity to phytochrome-mediated light signals in rice. Plant Sci. 2014;214:99-105.
154. Zhou GA, Chang RZ, Qiu LJ. Overexpression of soybean ubiquitin-conjugating enzyme gene GmUBC2 confers enhanced drought and salt tolerance through modulating abiotic stress-responsive gene expression in Arabidopsis. Plant Mol Biol. 2010;72:357-67.
155. Patridge EV, Ferry JG. WrbA from Escherichia coli and Archaeoglobus fulgidus is an NAD(P)H: quinone oxidoreductase. J Bacteriol. 2005;188:3498-506.