Comparative Proteomic Analysis of Brassica napus in Response to Drought Stress

Journal of Proteome Research

Volumn 14, Issue 8, 2015, Pages 3068-3081

  Koh, Jin ^a   Chen, Gang ^a,b   Yoo, Mi Jeong ^a   Zhu, Ning ^a   Dufresne, Daniel ^c   Erickson, John E ^a   Shao, Hongbo ^d   Chen, Sixue ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b YANGZHOU UNIVERSITY   (China)

^c Palm Beach Central High School   (United States)

^d YANTAI INSTITUTE OF COASTAL ZONE RESEARCH   (China)

Author keywords

Brassica napus; drought stress; iTRAQ; proteomics; PTMs; transcription

Indexed keywords

ARGININOSUCCINATE SYNTHASE; ASPARTIC PROTEINASE; DEHYDROASCORBIC ACID REDUCTASE; GLUTAMATE AMMONIA LIGASE; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE PEROXIDASE; GLUTATHIONE TRANSFERASE; GLYCINE HYDROXYMETHYLTRANSFERASE; HEAT SHOCK PROTEIN; JACALIN; LECTIN; MALATE DEHYDROGENASE; MITOGEN ACTIVATED PROTEIN KINASE 7; PEROXIREDOXIN; PROLINE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; RIBULOSEBISPHOSPHATE CARBOXYLASE; RNA BINDING PROTEIN; THIOGLUCOSIDASE; TRIOSEPHOSPHATE ISOMERASE; VEGETABLE PROTEIN; PROTEOME;

ARTICLE; BIOCHEMICAL ANALYSIS; CHLOROPHYLL FLUORESCENCE; COMPARATIVE STUDY; CONTROLLED STUDY; DROUGHT STRESS; DROUGHT TOLERANCE; ENZYME ACTIVITY; GENETIC TRANSCRIPTION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; PHOTOSYNTHESIS; PLANT DEFENSE; PLANT GENE; PLANT GROWTH; PLANT METABOLISM; PLANT RESPONSE; PLANT STRUCTURES; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; PROTEOMICS; RAPESEED; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; SEEDLING; SIGNAL TRANSDUCTION; WATER CONTENT; CLASSIFICATION; CLUSTER ANALYSIS; DROUGHT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGICAL STRESS; PROCEDURES; TANDEM MASS SPECTROMETRY; TIME FACTOR;

BRASSICA NAPUS; BRASSICA NAPUS VAR. NAPUS;

BRASSICA NAPUS; CHROMATOGRAPHY, LIQUID; CLUSTER ANALYSIS; DROUGHTS; GENE EXPRESSION REGULATION, PLANT; PLANT PROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME; PROTEOMICS; STRESS, PHYSIOLOGICAL; TANDEM MASS SPECTROMETRY; TIME FACTORS;

EID: 84938808427     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr501323d     Document Type: Article

References (99)

1. van Velthuizen, H.; Huddelston, B.; Fischer, G.; Salvatore, M.; Ataman, E.; Nachtergaele, F.; Zanetti, M., Mapping Biophysical Factors That Influence Agricultural Production and Rural Vulnerability. In Environment and Natural Resources Series 10; Food and Agriculture Organization of the United Nations: Rome, 2007.
2. Zhu, J. K. Salt and drought stress signal transduction in plants Annu. Rev. Plant Biol. 2002, 53, 247-73
3. Boyer, J. S. Plant productivity and environment Science 1982, 218 (4571) 443-8
4. Parry, M. A.; Hawkesford, M. J. An integrated approach to crop genetic improvement J. Integr. Plant Biol. 2012, 54 (4) 250-9
5. Aghaei, K.; Komatsu, S. Crop and medicinal plants proteomics in response to salt stress Front Plant Sci. 2013, 4, 8
6. Zhang, X.; Lu, G.; Long, W.; Zou, X.; Li, F.; Nishio, T. Recent progress in drought and salt tolerance studies in Brassica crops Breed Sci. 2014, 64 (1) 60-73
7. Mahajan, S.; Tuteja, N. Cold, salinity, and drought stresses: An overview Arch. Biochem. Biophys. 2005, 444 (2) 139-58
8. Breshears, D. D.; Cobb, N. S.; Rich, P. M.; Price, K. P.; Allen, C. D.; Balice, R. G.; Romme, W. H.; Kastens, J. H.; Floyd, M. L.; Belnap, J.; Anderson, J. J.; Myers, O. B.; Meyer, C. W. Regional vegetation die-off in response to global-change-type drought Proc. Natl. Acad. Sci. U. S. A. 2005, 102 (42) 15144-8
9. Hoekstra, F. A.; Golovina, E. A.; Buitink, J. Mechanisms of plant desiccation tolerance Trends Plant Sci. 2001, 6 (9) 431-8
10. Lawlor, D. W.; Tezara, W. Causes of decreased photosynthetic rate and metabolic capacity in water-deficient leaf cells: A critical evaluation of mechanisms and integration of processes Ann. Bot. 2009, 103 (4) 561-79
11. Reddy, A. R.; Chaitanya, K. V.; Vivekanandan, M. Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants J. Plant Physiol. 2004, 161 (11) 1189-202
12. Horn, R.; Chudobova, I.; Hansel, U.; Herwartz, D.; Koskull-Doring, P.; Schillberg, S. Simultaneous treatment with tebuconazole and abscisic acid induces drought and salinity stress tolerance in Arabidopsis thaliana by maintaining key plastid protein levels J. Proteome Res. 2013, 12 (3) 1266-81
13. Miura, K.; Okamoto, H.; Okuma, E.; Shiba, H.; Kamada, H.; Hasegawa, P. M.; Murata, Y. SIZ1 deficiency causes reduced stomatal aperture and enhanced drought tolerance via controlling salicylic acid-induced accumulation of reactive oxygen species in Arabidopsis Plant J. 2013, 73 (1) 91-104
14. Chan, K. X.; Wirtz, M.; Phua, S. Y.; Estavillo, G. M.; Pogson, B. J. Balancing metabolites in drought: The sulfur assimilation conundrum Trends Plant Sci. 2013, 18 (1) 18-29
15. Chen, T. H.; Murata, N. Glycinebetaine: An effective protectant against abiotic stress in plants Trends Plant Sci. 2008, 13 (9) 499-505
16. Nayyar, H.; Walia, D. P. Water stress induced proline accumulationin contrasting wheat genotypes as affected by calcium and abscisic acid Biol. Plant 2003, 46, 275-9
17. Nakabayashi, R.; Mori, T.; Saito, K. Alternation of flavonoid accumulation under drought stress in Arabidopsis thaliana Plant Signal Behav. 2014, 9 e29518
18. Apel, K.; Hirt, H. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction Annu. Rev. Plant Biol. 2004, 55, 373-99
19. Cruz de Carvalho, M. H. Drought stress and reactive oxygen species: Production, scavenging, and signaling Plant Signal Behav. 2008, 3 (3) 156-65
20. Hu, H.; Xiong, L. Genetic engineering and breeding of drought-resistant crops Annu. Rev. Plant Biol. 2014, 65, 715-41
21. Shu, L.; Lou, Q.; Ma, C.; Ding, W.; Zhou, J.; Wu, J.; Feng, F.; Lu, X.; Luo, L.; Xu, G.; Mei, H. Genetic, proteomic, and metabolic analysis of the regulation of energy storage in rice seedlings in response to drought Proteomics 2011, 11 (21) 4122-38
22. Dong, M. H.; Gu, J. R.; Zhang, L.; Chen, P. F.; Liu, T. F.; Deng, J. H.; Lu, H. Q.; Han, L. Y.; Zhao, B. H. Comparative proteomics analysis of superior and inferior spikelets in hybrid rice during grain filling and response of inferior spikelets to drought stress using isobaric tags for relative and absolute quantification J. Proteomics 2014, 109, 382-399
23. Rabello, F. R.; Villeth, G. R. C.; Rabello, A. R.; Rangel, P. H. N.; Guimaraes, C. M.; Huergo, L. F.; Souza, E. M.; Pedrosa, F. O.; Ferreira, M. E.; Mehta, A. Proteomic analysis of upland rice (Oryza sativa L.) exposed to intermittent water deficit Protein J. 2014, 33 (3) 221-30
24. Benesova, M.; Hola, D.; Fischer, L.; Jedelsky, P. L.; Hnilicka, F.; Wilhelmova, N.; Rothova, O.; Kocova, M.; Prochazkova, D.; Honnerova, J.; Fridrichova, L.; Hnilickova, H. The physiology and proteomics of drought tolerance in maize: Early stomatal closure as a cause of lower tolerance to short-term dehydration? PLoS One 2012, 7 (6) e38017
25. Yang, L.; Jiang, T.; Fountain, J. C.; Scully, B. T.; Lee, R. D.; Kemerait, R. C.; Chen, S.; Guo, B. Protein profiles reveal diverse responsive signaling pathways in kernels of two maize inbred lines with contrasting drought sensitivity Int. J. Mol. Sci. 2014, 15 (10) 18892-918
26. Gong, F.; Yang, L.; Tai, F.; Hu, X.; Wang, W. "Omics" of maize stress response for sustainable food production: Opportunities and challenges OMICS 2014, 18 (12) 714-32
27. Hao, P.; Zhu, J.; Gu, A.; Lv, D.; Ge, P.; Chen, G.; Li, X.; Yan, Y. An integrative proteome analysis of different seedling organs in tolerant and sensitive wheat cultivars under drought stress and recovery Proteomics 2014, 15 (9) 1544-63
28. Faghani, E.; Gharechahi, J.; Komatsu, S.; Mirzaei, M.; Khavarinejad, R. A.; Najafi, F.; Farsad, L. K.; Salekdeh, G. H. Comparative physiology and proteomic analysis of two wheat genotypes contrasting in drought tolerance J. Proteomics 2015, 114, 1-15
29. Zhang, M.; Lv, D.; Ge, P.; Bian, Y.; Chen, G.; Zhu, G.; Li, X.; Yan, Y. Phosphoproteome analysis reveals new drought response and defense mechanisms of seedling leaves in bread wheat (Triticum aestivum L.) J. Proteomics 2014, 109, 290-308
30. Zhang, M.; Ma, C. Y.; Lv, D. W.; Zhen, S. M.; Li, X. H.; Yan, Y. M. Comparative phosphoproteome analysis of the developing grains in bread wheat (Triticum aestivum L.) under well-watered and water-deficit conditions J. Proteome Res. 2014, 13 (10) 4281-97
31. Ashoub, A.; Baeumlisberger, M.; Neupaertl, M.; Karas, M.; Bruggemann, W. Characterization of common and distinctive adjustments of wild barley leaf proteome under drought acclimation, heat stress, and their combination Plant Mol. Biol. 2015, 87 (4-5) 459-71
32. Ashoub, A.; Beckhaus, T.; Berberich, T.; Karas, M.; Bruggemann, W. Comparative analysis of barley leaf proteome as affected by drought stress Planta 2013, 237 (3) 771-81
33. Rollins, J. A.; Habte, E.; Templer, S. E.; Colby, T.; Schmidt, J.; von Korff, M. Leaf proteome alterations in the context of physiological and morphological responses to drought and heat stress in barley (Hordeum vulgare L.) J. Exp. Bot. 2013, 64 (11) 3201-12
34. Deeba, F.; Pandey, A. K.; Ranjan, S.; Mishra, A.; Singh, R.; Sharma, Y. K.; Shirke, P. A.; Pandey, V. Physiological and proteomic responses of cotton (Gossypium herbaceum L.) to drought stress Plant Physiol. Biochem. 2012, 53, 6-18
35. Zheng, M.; Meng, Y.; Yang, C.; Zhou, Z.; Wang, Y.; Chen, B. Protein expression changes during cotton fiber elongation in response to drought stress and recovery Proteomics 2014, 14 (15) 1776-95
36. Bhushan, D.; Pandey, A.; Choudhary, M. K.; 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 (11) 1868-84
37. 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 (1) 88-107
38. Subba, P.; Kumar, R.; Gayali, S.; Shekhar, S.; Parveen, S.; Pandey, A.; Datta, A.; Chakraborty, S.; Chakraborty, N. Characterisation of the nuclear proteome of a dehydration-sensitive cultivar of chickpea and comparative proteomic analysis with a tolerant cultivar Proteomics 2013, 13 (12-13) 1973-92
39. Zadraznik, T.; Hollung, K.; Egge-Jacobsen, W.; Meglic, V.; Sustar-Vozlic, J. Differential proteomic analysis of drought stress response in leaves of common bean (Phaseolus vulgaris L.) J. Proteomics 2013, 78, 254-72
40. Hajheidari, M.; Abdollahian-Noghabi, M.; Askari, H.; Heidari, M.; Sadeghian, S. Y.; Ober, E. S.; Salekdeh, G. H. Proteome analysis of sugar beet leaves under drought stress Proteomics 2005, 5 (4) 950-60
41. Castillejo, M. A.; Maldonado, A. M.; Ogueta, S.; Jorrin, J. V. Proteomic analysis of responses to drought stress in sunflower (Helianthus annuus) leaves by 2DE gel electrophoresis and mass spectrometry Open Proteomics J. 2008, 1, 59-71
42. Fulda, S.; Mikkat, S.; Stegmann, H.; Horn, R. Physiology and proteomics of drought stress acclimation in sunflower (Helianthus annuus L.) Plant Biol. (Stuttgart, Ger.) 2011, 13 (4) 632-42
43. Chen, S.; Ding, G.; Wang, Z.; Cai, H.; Xu, F. Proteomic and comparative genomic analysis reveals adaptability of Brassica napus to phosphorus-deficient stress J. Proteomics 2015, 117, 106-19
44. Ismaili, A.; Salavati, A.; Mohammadi, P. P. A comparative proteomic analysis of responses to high temperature stress in hypocotylof canola (Brassica napus L.) Protein Pept. Lett. 2014, 22 (3) 285-99
45. DHooghe, P.; Dubousset, L.; Gallardo, K.; Kopriva, S.; Avice, J. C.; Trouverie, J. Evidence for proteomic and metabolic adaptations associated with alterations of seed yield and quality in sulfur-limited Brassica napus L Mol. Cell Proteomics 2014, 13 (5) 1165-83
46. DAlessandro, A.; Taamalli, M.; Gevi, F.; Timperio, A. M.; Zolla, L.; Ghnaya, T. Cadmium stress responses in Brassica juncea: Hints from proteomics and metabolomics J. Proteome Res. 2013, 12 (11) 4979-97
47. Bandehagh, A.; Salekdeh, G. H.; Toorchi, M.; Mohammadi, A.; Komatsu, S. Comparative proteomic analysis of canola leaves under salinity stress Proteomics 2011, 11 (10) 1965-75
48. Zhu, M.; Simons, B.; Zhu, N.; Oppenheimer, D. G.; Chen, S. Analysis of abscisic acid responsive proteins in Brassica napus guard cells by multiplexed isobaric tagging J. Proteomics 2010, 73 (4) 790-805
49. Zhu, M.; Zhu, N.; Song, W. Y.; Harmon, A. C.; Assmann, S. M.; Chen, S. Thiol-based redox proteins in abscisic acid and methyl jasmonate signaling in Brassica napus guard cells Plant J. 2014, 78 (3) 491-515
50. Chu, P.; Yan, G. X.; Yang, Q.; Zhai, L. N.; Zhang, C.; Zhang, F. Q.; Guan, R. Z. iTRAQ-based quantitative proteomics analysis of Brassica napus leaves reveals pathways associated with chlorophyll deficiency J. Proteomics 2015, 113, 244-59
51. Chen, S.; Harmon, A. C. Advances in plant proteomics Proteomics 2006, 6 (20) 5504-16
52. 1 line under drought stress Amino Acids 2012, 43 (5) 2137-52
53. Jensen, C. R.; Mogensen, V. O.; Mortensen, G.; Andersen, M. N.; Schjoerring, J. K.; Thage, J. H.; Koribidis, J. Leaf photosynthesis and drought adaptation in field grown oilseed rape (Brassica napus L.) Aust J. Plant Physiol. 1996, 23, 631-44
54. Sangtarash, M. H.; Qaderi, M. M.; Chinnappa, C. C.; Reid, D. M. Differential sensitivity of canola (Brassica napus) seedlings to ultraviolet-B radiation, water stress, and abscisic acid Environ. Exp. Bot. 2009, 66, 212-9
55. Hosseini, S. M.; Hassibi, P. Effects of water deficit stress on several quantitative and qualitative characteristics of canola (Brassica napus L.) cultivars Nat. Sci. Biol. 2011, 3, 120-5
56. Smart, R. E. Rapid estimates of relative water content Plant Physiol. 1974, 53 (2) 258-60
57. 1 hybrid Plant Physiol. 1988, 88 (1) 213-7
58. Willits, D. H.; Peet, M. M. Measurement of chlorophyll fluorescence as a heat stress indicator in tomato: Laboratory and greenhouse comparisons J. Am. Soc. Hortic. Sci. 2001, 126, 188-94
59. Irigoyen, J. J.; Einerich, D. W.; Sánchez-Díaz, M. Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants Physiol. Plantarum 1992, 84, 55-60
60. Grieve, C. M.; M, E. V., Betaine accumulation in salt-stressed sorghum Physiol. Plantarum 1984, 61, 167-71
61. Stewart, R. R.; Bewley, J. D. Lipid peroxidation associated with accelerated aging of soybean axes Plant Physiol. 1980, 65 (2) 245-8
62. Nakano, Y.; Asada, K. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts Plant Cell Physiol. 1981, 22, 867-80
63. Davis, D. G.; Swanson, H. R. Activity of stress-related enzymes in the perennial weed leafy spurge (Euphorbia esula L.) Environ. Exp. Bot. 2001, 46, 95-108
64. Aebi, H. Catalase in vitro Methods Enzymol. 1984, 105, 121-6
65. Koh, J.; Chen, S.; Zhu, N.; Yu, F.; Soltis, P. S.; Soltis, D. E. Comparative proteomics of the recently and recurrently formed natural allopolyploid Tragopogon mirus (Asteraceae) and its parents New Phytol. 2012, 196 (1) 292-305
66. Eng, J. K.; Mccormack, A. L.; Yates, J. R. An approach to correlate tandem mass-spectral data of peptides with amino-acid-sequences in a protein database J. Am. Soc. Mass Spectrom. 1994, 5 (11) 976-89
67. Shilov, I. V.; Seymour, S. L.; Patel, A. A.; Loboda, A.; Tang, W. H.; Keating, S. P.; Hunter, C. L.; Nuwaysir, L. M.; Schaeffer, D. A. The Paragon Algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra Mol. Cell Proteomics 2007, 6 (9) 1638-55
68. Keller, A.; Nesvizhskii, A. I.; Kolker, E.; Aebersold, R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search Anal. Chem. 2002, 74 (20) 5383-92
69. Nesvizhskii, A. I.; Keller, A.; Kolker, E.; Aebersold, R. A statistical model for identifying proteins by tandem mass spectrometry Anal. Chem. 2003, 75 (17) 4646-58
70. Du, Z.; Zhou, X.; Ling, Y.; Zhang, Z.; Su, Z. agriGO: A GO analysis toolkit for the agricultural community Nucleic Acids Res. 2010, 38 (Web Server issue) W64-70
71. Vizcaino, J. A.; Cote, R. G.; Csordas, A.; Dianes, J. A.; Fabregat, A.; Foster, J. M.; Griss, J.; Alpi, E.; Birim, M.; Contell, J.; OKelly, G.; Schoenegger, A.; Ovelleiro, D.; Perez-Riverol, Y.; Reisinger, F.; Rios, D.; Wang, R.; Hermjakob, H. The PRoteomics IDEntifications (PRIDE) database and associated tools: Status in 2013 Nucleic Acids Res. 2013, 41 (Database issue) D1063-9
72. Parker, J.; Koh, J.; Yoo, M. J.; Zhu, N.; Feole, M.; Yi, S.; Chen, S. Quantitative proteomics of tomato defense against Pseudomonas syringae infection Proteomics 2013, 13 (12-13) 1934-46
73. Bevan, M.; Bancroft, I.; Bent, E.; Love, K.; Goodman, H.; Dean, C.; Bergkamp, R.; Dirkse, W.; Van Staveren, M.; Stiekema, W.; Drost, L.; Ridley, P.; Hudson, S. A.; Patel, K.; Murphy, G.; Piffanelli, P.; Wedler, H.; Wedler, E.; Wambutt, R.; Weitzenegger, T.; Pohl, T. M.; Terryn, N.; Gielen, J.; Villarroel, R.; De Clerck, R.; Van Montagu, M.; Lecharny, A.; Auborg, S.; Gy, I.; Kreis, M.; Lao, N.; Kavanagh, T.; Hempel, S.; Kotter, P.; Entian, K. D.; Rieger, M.; Schaeffer, M.; Funk, B.; Mueller-Auer, S.; Silvey, M.; James, R.; Montfort, A.; Pons, A.; Puigdomenech, P.; Douka, A.; Voukelatou, E.; Milioni, D.; Hatzopoulos, P.; Piravandi, E.; Obermaier, B.; Hilbert, H.; Dusterhoft, A.; Moores, T.; Jones, J. D.; Eneva, T.; Palme, K.; Benes, V.; Rechman, S.; Ansorge, W.; Cooke, R.; Berger, C.; Delseny, M.; Voet, M.; Volckaert, G.; Mewes, H. W.; Klosterman, S.; Schueller, C.; Chalwatzis, N. Analysis of 1.9 Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana Nature 1998, 391 (6666) 485-8
74. Dalal, M.; Tayal, D.; Chinnusamy, V.; Bansal, K. C. Abiotic stress and ABA-inducible Group 4 LEA from Brassica napus plays a key role in salt and drought tolerance J. Biotechnol. 2009, 139 (2) 137-45
75. Bae, M. J.; Kim, Y. S.; Kim, I. S.; Choe, Y. H.; Lee, E. J.; Kim, Y. H.; Park, H. M.; Yoon, H. S. Transgenic rice overexpressing the Brassica juncea gamma-glutamylcysteine synthetase gene enhances tolerance to abiotic stress and improves grain yield under paddy field conditions Mol. Breed 2013, 31, 931-45
76. Alikhan, M.; Ashraf, M. Y.; Mujtaba, S. M.; Shirazi, M. U.; Khan, M. A.; Shereen, A.; Mumtaz, S.; Siddiqui, M. A.; Kaleri, G. M. Evaluation of high yielding canola type Brassica genotypes/mutants for drought tolerance using physiological indices as screening tool Pak. J. Bot. 2010, 42, 3807-16
77. Fariduddin, Q.; Khanam, S.; Hasan, S. A.; Ali, B.; Hayat, S.; Ahmad, A. Effect of 28-homobrassinolide on the drought stress induced changes in photosynthesis and antioxidant system of Brassica juncea L Acta Physiol. Plant 2009, 31, 889-97
78. Harb, A.; Krishnan, A.; Ambavaram, M. M.; Pereira, A. Molecular and physiological analysis of drought stress in Arabidopsis reveals early responses leading to acclimation in plant growth Plant Physiol. 2010, 154 (3) 1254-71
79. Boldt, R.; Edner, C.; Kolukisaoglu, U.; Hagemann, M.; Weckwerth, W.; Wienkoop, S.; Morgenthal, K.; Bauwe, H. d -GLYCERATE 3-KINASE, the last unknown enzyme in the photorespiratory cycle in Arabidopsis, belongs to a novel kinase family Plant Cell 2005, 17 (8) 2413-20
80. Kim, J. S.; Jung, H. J.; Lee, H. J.; Kim, K. A.; Goh, C. H.; Woo, Y.; Oh, S. H.; Han, Y. S.; Kang, H. Glycine-rich RNA-binding protein 7 affects abiotic stress responses by regulating stomata opening and closing in Arabidopsis thaliana Plant J. 2008, 55 (3) 455-66
81. Koussevitzky, S.; Suzuki, N.; Huntington, S.; Armijo, L.; Sha, W.; Cortes, D.; Shulaev, V.; Mittler, R. Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination J. Biol. Chem. 2008, 283 (49) 34197-203
82. Wittstock, U.; Burow, M. Glucosinolate breakdown in Arabidopsis: Mechanism, regulation, and biological significance Arabidopsis Book 2010, 8, e0134
83. Stotz, H. U.; Sawada, Y.; Shimada, Y.; Hirai, M. Y.; Sasaki, E.; Krischke, M.; Brown, P. D.; Saito, K.; Kamiya, Y. Role of camalexin, indole glucosinolates, and side chain modification of glucosinolate-derived isothiocyanates in defense of Arabidopsis against Sclerotinia sclerotiorum Plant J. 2011, 67 (1) 81-93
84. Valero-Galvan, J.; Gonzalez-Fernandez, R.; Navarro-Cerrillo, R. M.; Gil-Pelegrin, E.; Jorrin-Novo, J. V. Physiological and proteomic analyses of drought stress response in Holm oak provenances J. Proteome Res. 2013, 12 (11) 5110-23
85. Ngara, R.; Ndimba, B. K. Understanding the complex nature of salinity and drought-stress response in cereals using proteomics technologies Proteomics 2014, 14 (4-5) 611-21
86. Kang, G.; Li, G.; Xu, W.; Peng, X.; Han, Q.; Zhu, Y.; Guo, T. Proteomics reveals the effects of salicylic acid on growth and tolerance to subsequent drought stress in wheat J. Proteome Res. 2012, 11 (12) 6066-79
87. Zheng, Z. L. Carbon and nitrogen nutrient balance signaling in plants Plant Signal Behav. 2009, 4 (7) 584-91
88. Jiang, Y.; Yang, B.; Harris, N. S.; Deyholos, M. K. Comparative proteomic analysis of NaCl stress-responsive proteins in Arabidopsis roots J. Exp. Bot. 2007, 58 (13) 3591-607
89. Xiang, Y.; Song, M.; Wei, Z.; Tong, J.; Zhang, L.; Xiao, L.; Ma, Z.; Wang, Y. A jacalin-related lectin-like gene in wheat is a component of the plant defence system J. Exp. Bot. 2011, 62 (15) 5471-83
90. Hossain, M. A.; Mostofa, M. G.; Fujita, M. Heat-shock positively modulates oxidative protection of salt and drought-stressed mustard (Brassica campestris L.) seedlings J. Plant Sci. Mol. Breed 2013, 2, 2
91. Marmagne, A.; Rouet, M. A.; Ferro, M.; Rolland, N.; Alcon, C.; Joyard, J.; Garin, J.; Barbier-Brygoo, H.; Ephritikhine, G. Identification of new intrinsic proteins in Arabidopsis plasma membrane proteome Mol. Cell Proteomics 2004, 3 (7) 675-91
92. Sweetlove, L. J.; Heazlewood, J. L.; Herald, V.; Holtzapffel, R.; Day, D. A.; Leaver, C. J.; Millar, A. H. The impact of oxidative stress on Arabidopsis mitochondria Plant J. 2002, 32 (6) 891-904
93. Baier, M.; Dietz, K. J. Protective function of chloroplast 2-cysteine peroxiredoxin in photosynthesis. Evidence from transgenic Arabidopsis Plant Physiol 1999, 119 (4) 1407-14
94. Murakami, R.; Ifuku, K.; Takabayashi, A.; Shikanai, T.; Endo, T.; Sato, F. Functional dissection of two Arabidopsis PsbO proteins: PsbO1 and PsbO2 FEBS J. 2005, 272 (9) 2165-75
95. Singh, K. K.; Ghosh, S. Regulation of glutamine synthetase isoforms in two differentially drought-tolerant rice (Oryza sativa L.) cultivars under water-deficit conditions Plant Cell Rep. 2013, 32 (2) 183-93
96. Pawłowicz, I.; Kosmala, A.; Rapacz, M. Expression pattern of the psbO gene and its involvement in acclimation of the photosynthetic apparatus during abiotic stresses in Festuca arundinacea and F. pratensis Acta Physiol. Plant 2012, 34, 1915-24
97. Xie, K.; Chen, J.; Wang, Q.; Yang, Y. Direct phosphorylation and activation of a mitogen-activated protein kinase by a calcium-dependent protein kinase in rice Plant Cell 2014, 26 (7) 3077-89
98. Mlynarova, L.; Nap, J. P.; Bisseling, T. The SWI/SNF chromatin-remodeling gene AtCHR12 mediates temporary growth arrest in Arabidopsis thaliana upon perceiving environmental stress Plant J. 2007, 51 (5) 874-85
99. Achard, P.; Cheng, H.; De Grauwe, L.; Decat, J.; Schoutteten, H.; Moritz, T.; Van Der Straeten, D.; Peng, J.; Harberd, N. P. Integration of plant responses to environmentally activated phytohormonal signals Science 2006, 311 (5757) 91-4