Acta Physiologiae Plantarum

, 39:240 | Cite as

Proteomic analysis of drought-responsive proteins in rice reveals photosynthesis-related adaptations to drought stress

  • Nutwadee Chintakovid
  • Maiporn Maipoka
  • Narumon Phaonakrop
  • Michael V. Mickelbart
  • Sittiruk Roytrakul
  • Supachitra Chadchawan
Original Article


Drought stress inhibits rice growth and biomass accumulation. To identify novel regulators of drought-stress responses in rice, we conducted a proteome-level study of the stress-susceptible (SS) Oryza sativa L. cv. ‘Leung Pratew 123’ and its stress-resistant (SR) somaclonal mutant line. In response to osmotic-stress treatments, 117 proteins were differentially accumulated, with 62 and 49 of these proteins detected in the SS and SR rice lines, respectively. There were six proteins that accumulated in both lines. The proteins in the SS line were mainly related to metabolic processes, whereas the proteins identified in the SR line were primarily related to retrotransposons. These observations suggest that retrotransposons may influence the epigenetic regulation of gene expression in response to osmotic stress. To identify the biological processes associated with drought tolerance in rice, we conducted a co-expression network analysis of 55 proteins that were differentially accumulated in the SR line under osmotic-stress conditions. We identified a major hub gene; LOC_Os04g38600 (encoding a glyceraldehyde-3-phosphate dehydrogenase), suggesting that photosynthetic adaptation via NADP(H) homeostasis contributes to drought tolerance in rice.


Rice GeLC–MS/MS Drought stress Glyceraldehyde-3-phosphate dehydrogenase 



Inward-rectifier K+ channel


Glyceraldehyde-3-phosphate dehydrogenase


GAPDH β subunit


Gel-based liquid chromatography–tandem mass spectrometry


Guard cell ‘outward-rectifying’ K+ channel


Nucleotide-binding site–leucine-rich repeat


Oxysterol-binding proteins


Polyethylene glycol 6000


Protein phosphatase 2C


Pentatricopeptide repeat


Stelar K+ ‘outward-rectifying’ channel


Stress resistant


Stress susceptible


Transposable element



This work was supported by the Ratchadaphiseksompoj Research Fund, Chulalongkorn University (Grant No. CU-57-011-FW). NC was supported by the Science Achievement Scholarship of Thailand. MM was supported by DPST. OSBC was supported by CUAASC.

Supplementary material

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Supplementary material 1 (DOCX 15 kb)
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Supplementary material 2 (XLSX 72 kb)
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Supplementary material 3 (XLSX 35 kb)
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Supplementary material 4 (XLSX 17 kb)


  1. Abere B et al (2012) Proteomic analysis of Chikungunya virus infected microgial cells. PLoS One 7:e34800. doi: 10.1371/journal.pone.0034800 PubMedPubMedCentralCrossRefGoogle Scholar
  2. Akashi K et al (2011) Dynamic changes in the leaf proteome of a C-3 xerophyte, Citrullus lanatus (wild watermelon), in response to water deficit. Planta 233:947–960PubMedCrossRefGoogle Scholar
  3. Naito K et al (2009) Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 461:1130–1134.
  4. Ambavaram MMR et al (2014) Coordinated regulation of photosynthesis in rice increases yield and tolerance to environmental stress. Nat Commun 5:5302.
  5. Ali GM, Komatsu S (2006) Proteomic analysis of rice leaf sheath during drought stress. J Proteome Res 5:396–403PubMedCrossRefGoogle Scholar
  6. Altaf-Ul-Amin M, Shinbo Y, Mihara K, Kurokawa K, Kanaya S (2006) Development and implementation of an algorithm for detection of protein complexes in large interaction networks. BMC Bioinform 7:207. doi: 10.1186/1471-2105-7-207 CrossRefGoogle Scholar
  7. Alvarez S, Choudhury SR, Pandey S (2014) Comparative quantitative proteomics analysis of the ABA response of roots of drought-sensitive and drought-tolerant wheat varieties identifies proteomic signatures of drought adaptability. J Proteome Res 13:1688–1701PubMedCrossRefGoogle Scholar
  8. Alzohairy A, Yousef M, Edris S, Kerti B, Gyulai G, Bahieldin A (2012) Detection of LTR retrotransposons reactivation induced by in vitro environmental stresses in barley (Hordeum vulgare) via RT-qPCR. Life Sci J 9:5019–5026Google Scholar
  9. Anca I-A, Fromentin J, Bui QT, Mhiri C, Grandbastien M-A, Simon-Plas F (2014) Different tobacco retrotransposons are specifically modulated by the elicitor cryptogein and reactive oxygen species. J Plant Physiol 171:1533–1540. doi: 10.1016/j.jplph.2014.07.003 PubMedCrossRefGoogle Scholar
  10. Aoki K, Ogata Y, Shibata D (2007) Approaches for extracting practical information from gene co-expression networks in plant biology. Plant Cell Physiol 48:381–390. doi: 10.1093/pcp/pcm013 PubMedCrossRefGoogle Scholar
  11. Baldoni E, Genga A, Cominelli E (2015) Plant MYB transcription factors: their role in drought response mechanisms. Int J Mol Sci 16:15811–15851. doi: 10.3390/ijms160715811 PubMedPubMedCentralCrossRefGoogle Scholar
  12. Barak S, Yadav NS, Khan A (2014) DEAD-Box RNA helicases and epigenetic control of abiotic stress-responsive gene expression. Plant Signal Behav 9:e977729–e977734. doi: 10.4161/15592324.2014.977729 PubMedPubMedCentralCrossRefGoogle Scholar
  13. Bhardwaj J, Mahajan M, Yadav SK (2013) Comparative analysis of DNA methylation polymorphism in drought sensitive (HPKC2) and Tolerant (HPK4) genotypes of horse gram (Macrotyloma uniflorum). Biochem Genet 51:493–502. doi: 10.1007/s10528-013-9580-2 PubMedCrossRefGoogle Scholar
  14. Boyer JS (1982) Plant productivity and environment. Science 218:443–448PubMedCrossRefGoogle Scholar
  15. Budak H, Akpinar BA, Unver T, Turktas M (2013) Proteome changes in wild and modern wheat leaves upon drought stress by two-dimensional electrophoresis and nanoLC–ESI–MS/MS. Plant Mol Biol 83:89–103. doi: 10.1007/s11103-013-0024-5 PubMedCrossRefGoogle Scholar
  16. Chadha S, Sharma M (2014) Transposable elements as stress adaptive capacitors induce genomic instability in fungal pathogen Magnaporthe oryzae. PLoS One 9:e94415PubMedPubMedCentralCrossRefGoogle Scholar
  17. Chamnanmanoontham N, Pongprayoon W, Pichayangkura R, Roytrakul S, Chadchawan S (2015) Chitosan enhances rice seedling growth via gene expression network between nucleus and chloroplast. Plant Growth Regul 75:101–114. doi: 10.1007/s10725-014-9935-7 CrossRefGoogle Scholar
  18. Chang L et al (2015) The beta subunit of glyceraldehyde 3-phosphate dehydrogenase is an important factor for maintaining photosynthesis and plant development under salt stress—based on an integrative analysis of the structural, physiological and proteomic changes in chloroplasts in Thellungiella halophila. Plant Sci 236:223–238. doi: 10.1016/j.plantsci.2015.04.010 PubMedCrossRefGoogle Scholar
  19. Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought—from genes to the whole plant. Funct Plant Biol 30:239–264CrossRefGoogle Scholar
  20. Chen J, Zhang Y, Liu J, Xia M, Wang W, Shen F (2014) Genome-wide analysis of the RNA helicase gene family in Gossypium raimondii. Int J Mol Sci 15:4635–4656. doi: 10.3390/ijms15034635 PubMedPubMedCentralCrossRefGoogle Scholar
  21. Cheng Z et al (2015) Identification of leaf proteins differentially accumulated between wheat cultivars distinct in their levels of drought tolerance. PLoS One 10:e0125302. doi: 10.1371/journal.pone.0125302 PubMedPubMedCentralCrossRefGoogle Scholar
  22. Coordinators NR (2016) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 44:D7–D19. doi: 10.1093/nar/gkv1290 CrossRefGoogle Scholar
  23. Cushing DA, Forsthoefel NR, Gestaut DR, Vernon DM (2005) Arabidopsis emb175 and other ppr knockout mutants reveal essential roles for pentatricopeptide repeat (PPR) proteins in plant embryogenesis. Planta 221:424–436. doi: 10.1007/s00425-004-1452-x PubMedCrossRefGoogle Scholar
  24. Deeba F et al (2012) Physiological and proteomic responses of cotton (Gossypium herbaceum L.) to drought stress. Plant Physiol Biochem 53:6–18. doi: 10.1016/j.plaphy.2012.01.002 PubMedCrossRefGoogle Scholar
  25. Deshmukh R et al (2014) Integrating omic approaches for abiotic stress tolerance in soybean. Front Plant Sci 5:244PubMedPubMedCentralCrossRefGoogle Scholar
  26. Doerks T, Copley R, Bork P (2001) DDT- a novel domain in different transcription and chromosome remodeling factors. Trends Biochem Sci 26:145–146. doi: 10.1016/S0968-0004(00)01769-2 PubMedCrossRefGoogle Scholar
  27. Dubouzet JG et al (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J 33:751–763. doi: 10.1046/j.1365-313X.2003.01661.x PubMedCrossRefGoogle Scholar
  28. Ford KL, Cassin A, Bacic A (2011) Quantitative proteomic analysis of wheat cultivars with differing drought stress tolerance. Front Plant Sci 2:44. doi: 10.3389/fpls.2011.00044 PubMedPubMedCentralCrossRefGoogle Scholar
  29. Gao S, Zhang YL, Yang L, Song JB, Yang ZM (2014) AtMYB20 is negatively involved in plant adaptive response to drought stress. Plant Soil 376:433–443. doi: 10.1007/s11104-013-1992-6 CrossRefGoogle Scholar
  30. Gelli M, Duo Y, Konda AR, Zhang C, Holding D, Dweikat I (2014) Identification of differentially expressed genes between sorghum genotypes with contrasting nitrogen stress tolerance by genome-wide transcriptional profiling. BMC Genom 15:179. doi: 10.1186/1471-2164-15-179 CrossRefGoogle Scholar
  31. Gharechahi J, Hajirezaei M-R, Salekdeh GH (2015) Comparative proteomic analysis of tobacco expressing cyanobacterial flavodoxin and its wild type under drought stress. J Plant Physiol 175:48–58. doi: 10.1016/j.jplph.2014.11.001 PubMedCrossRefGoogle Scholar
  32. Grandbastien M-A (2015) LTR retrotransposons, handy hitchhikers of plant regulation and stress response. Biochim Biophys Acta 1849:403–416. doi: 10.1016/j.bbagrm.2014.07.017 PubMedCrossRefGoogle Scholar
  33. Hadiarto T, Tran L-SP (2010) Progress studies of drought-responsive genes in rice. Plant Cell Rep 30:297–310. doi: 10.1007/s00299-010-0956-z PubMedCrossRefGoogle Scholar
  34. Haefele SM, Kato Y, Singh S (2016) Climate ready rice: augmenting drought tolerance with best management practices. Field Crops Res 190:60–69. doi: 10.1016/j.fcr.2016.02.001 CrossRefGoogle Scholar
  35. Hald S, Nandha B, Gallois P, Johnson GN (2008) Feedback regulation of photosynthetic electron transport by NADP(H) redox poise. Biochim Biophys Acta 1777:433–440. doi: 10.1016/j.bbabio.2008.02.007 PubMedCrossRefGoogle Scholar
  36. Hancock RD et al (2014) Physiological, biochemical and molecular responses of the potato (Solanum tuberosum L.) plant to moderately elevated temperature. Plant Cell Environ 37:439–450. doi: 10.1111/pce.12168 PubMedCrossRefGoogle Scholar
  37. Hartwell LH, Hopfield JJ, Leibler S, Murray AW (1999) From molecular to modular cell biology. Nature 402:C47–C52PubMedCrossRefGoogle Scholar
  38. Hildebrandt T, Knuesting J, Berndt C, Morgan B, Scheibe R (2015) Cytosolic thiol switches regulating basic cellular functions: GAPDH as an information hub? Biol Chem 396:523–537. doi: 10.1515/hsz-2014-0295 PubMedCrossRefGoogle Scholar
  39. Himmelbach A, Hoffmann T, Leube M, Höhener B, Grill E (2002) Homeodomain protein ATHB6 is a target of the protein phosphatase ABI1 and regulates hormone responses in Arabidopsis. EMBO J 21:3029–3038. doi: 10.1093/emboj/cdf316 PubMedPubMedCentralCrossRefGoogle Scholar
  40. Hirochika H, Sugimoto K, Otsuki Y, Tsugawa H, Kanda M (1996) Retrotransposons of rice involved in mutations induced by tissue culture. PNAS 93:7783–7788PubMedPubMedCentralCrossRefGoogle Scholar
  41. Huang X-S, Liu J-H, Chen X-J (2010) Overexpression of PtrABF gene, a bZIP transcription factor isolated from Poncirus trifoliata, enhances dehydration and drought tolerance in tobacco via scavenging ROS and modulating expression of stress-responsive genes. BMC Plant Biol 10:230. doi: 10.1186/1471-2229-10-230 PubMedPubMedCentralCrossRefGoogle Scholar
  42. Huang X-S, Luo T, Fu X-Z, Fan Q-J, Liu J-H (2011) Cloning and molecular characterization of a mitogen-activated protein kinase gene from Poncirus trifoliata whose ectopic expression confers dehydration/drought tolerance in transgenic tobacco. J Exp Bot 62:5191–5206. doi: 10.1093/jxb/err229 PubMedPubMedCentralCrossRefGoogle Scholar
  43. Izanloo A, Condon AG, Langridge P, Tester M, Schnurbusch T (2008) Different mechanisms of adaptation to cyclic water stress in two South Australian bread wheat cultivars. J Exp Bot 59:3327–3346PubMedPubMedCentralCrossRefGoogle Scholar
  44. Jaresitthikunchai J, Phaonakrop N, Kittisenachai S, Roytrakul S (2009) Rapid in-gel digestion protocol for protein identification by peptide mass fingerprint. In: The 2nd biochemistry and molecular biology conference: biochemistry and molecular biology for regional sustainable development, Khon Kaen, May 7–8, 2009Google Scholar
  45. Javid MG, Sorooshzadeh A, Sanavy SAMM, Allahdadi I, Moradi F (2011) Effects of the exogenous application of auxin and cytokinin on carbohydrate accumulation in grains of rice under salt stress. Plant Growth Regul 65:305–313CrossRefGoogle Scholar
  46. Ji K, Wang Y, Sun W, Lou Q, Mei H, Shen S, Chen H (2012) Drought-responsive mechanisms in rice genotypes with contrasting drought tolerance during reproductive stage. J Plant Physiol 169:336–344. doi: 10.1016/j.jplph.2011.10.010 PubMedCrossRefGoogle Scholar
  47. Jia Y et al (2015) Effect of low water temperature at reproductive stage on yield and glutamate metabolism of rice (Oryza sativa L.) in China. Field Crops Res 175:16–25. doi: 10.1016/j.fcr.2015.01.004 CrossRefGoogle Scholar
  48. Johansson C, Samskog J, Sundström L, Wadensten H, Björkesten L, Flensburg J (2006) Differential expression analysis of Escherichia coli proteins using a novel software for relative quantitation of LC–MS/MS data. Proteomics 6:4475–4485. doi: 10.1002/pmic.200500921 PubMedCrossRefGoogle Scholar
  49. Kant P, Kant S, Gordon M, Shaked R, Barak S (2007) STRESS RESPONSE SUPPRESSOR1 and STRESS RESPONSE SUPPRESSOR2, two DEAD-box RNA helicases that attenuate Arabidopsis responses to multiple abiotic stresses. Plant Physiol 145:814–830PubMedPubMedCentralCrossRefGoogle Scholar
  50. Kapazoglou A, Drosou V, Argiriou A, Tsaftaris A (2013) The study of a barley epigenetic regulator, HvDME, in seed development and under drought. BMC Plant Biol 13:172PubMedPubMedCentralCrossRefGoogle Scholar
  51. Kappachery S, Baniekal-Hiremath G, Yu JW, Park SW (2014) Effect of over-and under-expression of glyceraldehyde 3-phosphate dehydrogenase on tolerance of plants to water-deficit stress. Plant Cell Tissue Organ Cult 121:97–107. doi: 10.1007/s11240-014-0684-0 CrossRefGoogle Scholar
  52. Kawahara Y et al (2013) Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice 6:1–10. doi: 10.1186/1939-8433-6-4 CrossRefGoogle Scholar
  53. Kosová K, Vítámvás P, Urban MO, Klíma M, Roy A, Prášil IT (2015) Biological networks underlying abiotic stress tolerance in temperate crops—a proteomic perspective. Int J Mol Sci 16:20913–20942. doi: 10.3390/ijms160920913 PubMedPubMedCentralCrossRefGoogle Scholar
  54. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685PubMedCrossRefGoogle Scholar
  55. Lisch D (2013) How important are transposons for plant evolution? Nat Rev Genet 14:49–61PubMedCrossRefGoogle Scholar
  56. Liu W et al (2014) The stripe rust resistance gene Yr10 encodes an evolutionary-conserved and unique CC-NBS-LRR sequence in wheat. Mol Plant 7:1740–1755. doi: 10.1093/mp/ssu112 PubMedCrossRefGoogle Scholar
  57. Lovisolo C, Perrone I, Carra A, Ferrandino A, Flexas J, Medrano H, Schubert A (2010) Drought-induced changes in development and function of grapevine (Vitis spp.) organs and in their hydraulic and non-hydraulic interactions at the whole-plant level: a physiological and molecular update. Funct Plant Biol 37:98–116CrossRefGoogle Scholar
  58. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275PubMedGoogle Scholar
  59. Manna S (2015) An overview of pentatricopeptide repeat proteins and their applications. Biochimie 113:93–99. doi: 10.1016/j.biochi.2015.04.004 PubMedCrossRefGoogle Scholar
  60. Meierhoff K, Felder S, Nakamura T, Bechtold N, Schuster G (2003) HCF152, an Arabidopsis RNA binding pentatricopeptide repeat protein involved in the processing of chloroplast psbB-psbT-psbH-petB-petD RNAs. Plant Cell 15:1480–1495. doi: 10.1105/tpc.010397 PubMedPubMedCentralCrossRefGoogle Scholar
  61. Meyer TS, Lamberts BL (1965) Use of coomassie brilliant blue R250 for the electrophoresis of microgram quantities of parotid saliva proteins on acrylamide-gel strips. Biochim Biophys Acta 107:144–145. doi: 10.1016/0304-4165(65)90403-4 PubMedCrossRefGoogle Scholar
  62. Morsy MR, Jouve L, Hausman J-F, Hoffmann L, Stewart JM (2007) Alteration of oxidative and carbohydrate metabolism under abiotic stress in two rice (Oryza sativa L.) genotypes contrasting in chilling tolerance. J Plant Physiol 164:157–167. doi: 10.1016/j.jplph.2005.12.004 PubMedCrossRefGoogle Scholar
  63. Nikolaeva MK, Maevskaya SN, Shugaev AG, Bukhov NG (2010) Effect of drought on chlorophyll content and antioxidant enzyme activities in leaves of three wheat cultivars varying in productivity. Russ J Plant Phys 57:87–95. doi: 10.1134/s1021443710010127 CrossRefGoogle Scholar
  64. Nounjan N, Siangliw JL, Toojinda T, Chadchawan S, Theerakulpisut P (2016) Salt-responsive mechanisms in chromosome segment substitution lines of rice (Oryza sativa L. cv. KDML105). Plant Physiol Biochem 103:96–105. doi: 10.1016/j.plaphy.2016.02.038 PubMedCrossRefGoogle Scholar
  65. Nouri M-Z, Moumeni A, Komatsu S (2015) Abiotic stresses: insight into gene regulation and protein expression in photosynthetic pathways of plants. Int J Mol Sci 16:20392–20416. doi: 10.3390/ijms160920392 PubMedPubMedCentralCrossRefGoogle Scholar
  66. Oh M, Komatsu S (2015) Characterization of proteins in soybean roots under flooding and drought stresses. J Proteom 114:161–181. doi: 10.1016/j.jprot.2014.11.008 CrossRefGoogle Scholar
  67. Pandey V, Shukla A (2015) Acclimation and tolerance strategies of rice under drought stress. Rice Sci 22:147–161. doi: 10.1016/j.rsci.2015.04.001 CrossRefGoogle Scholar
  68. Park O-MK (2004) Proteomic studies in plants. BMB Rep 37:133–138CrossRefGoogle Scholar
  69. Perkins DN, Pappin DJC, Creasy DM, Cottrell JS (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20:3551–3567. doi: 10.1002/(SICI)1522-2683(19991201)20:18<3551:AID-ELPS3551>3.0.CO;2-2 PubMedCrossRefGoogle Scholar
  70. Pongprayoon W, Roytrakul S, Pichayangkura R, Chadchawan S (2013) The role of hydrogen peroxide in chitosan-induced resistance to osmotic stress in rice (Oryza sativa L.). Plant Growth Regul 70:159–173. doi: 10.1007/s10725-013-9789-4 CrossRefGoogle Scholar
  71. Pusnik M, Small I, Read LK, Fabbro T, Schneider A (2007) Pentatricopeptide repeat proteins in Trypanosoma brucei function in mitochondrial ribosomes. Mol Cell Biol 27:6876–6888. doi: 10.1128/mcb.00708-07 PubMedPubMedCentralCrossRefGoogle Scholar
  72. Rai A, Singh R, Shirke PA, Tripathi RD, Trivedi PK, Chakrabarty D (2015) Expression of rice CYP450-like gene (Os08g01480) in Arabidopsis modulates regulatory network leading to heavy metal and other abiotic stress tolerance. PLoS One 10:e0138574. doi: 10.1371/journal.pone.0138574 PubMedPubMedCentralCrossRefGoogle Scholar
  73. Saeed AI et al (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34:374–378PubMedGoogle Scholar
  74. Saeng-ngam S, Takpirom W, Buaboocha T, Chadchawan S (2012) The role of the OsCam1-1 salt stress sensor in ABA accumulation and salt tolerance in rice. J Plant Biol 55:198–208. doi: 10.1007/s12374-011-0154-8 CrossRefGoogle Scholar
  75. Saikumar S, Varma CMK, Saiharini A, Kalmeshwer GP, Nagendra K, Lavanya K, Ayyappa D (2016) Grain yield responses to varied level of moisture stress at reproductive stage in an interspecific population derived from Swarna/O. glaberrima introgression line. NJAS Wagening J Life. doi: 10.1016/j.njas.2016.05.005 Google Scholar
  76. Sakai H et al (2013) Rice Annotation Project Database (RAP-DB): an integrative and interactive database for rice genomics. Plant Cell Physiol 54:e6–e6. doi: 10.1093/pcp/pcs183 PubMedPubMedCentralCrossRefGoogle Scholar
  77. Santoni V, Molloy M, Rabilloud T (2000) Membrane proteins and proteomics: un amour impossible? Electrophoresis 21:1054–1070. doi: 10.1002/(SICI)1522-2683(20000401)21:6<1054:AID-ELPS1054>3.0.CO;2-8 PubMedCrossRefGoogle Scholar
  78. Sato Y et al (2013) RiceFREND: a platform for retrieving coexpressed gene networks in rice. Nucleic Acids Res 41:D1214–D1221. doi: 10.1093/nar/gks1122 PubMedCrossRefGoogle Scholar
  79. Smita S, Katiyar A, Pandey DM, Chinnusamy V, BansaL KC (2015) Transcriptional regulatory network analysis of MYB transcription factor family genes in rice. Front Plant Sci. doi: 10.3389/fpls.2015.01157 Google Scholar
  80. Sripinyowanich S et al (2013) Overexpression of a partial fragment of the salt-responsive gene OsNUC1 enhances salt adaptation in transgenic Arabidopsis thaliana and rice (Oryza sativa L.) during salt stress. Plant Sci 213:67–78. doi: 10.1016/j.plantsci.2013.08.013 PubMedCrossRefGoogle Scholar
  81. Tai F, Yuan Z, Wu X, Zhao P, Hu X, Wang W (2011) Identification of membrane proteins in maize leaves, altered in expression under drought stress through polyethylene glycol treatment. Plant Omics 4:250Google Scholar
  82. Takahashi S, Murata N (2005) Interruption of the Calvin cycle inhibits the repair of Photosystem II from photodamage. Biochim Biophys Acta 1708:352–361. doi: 10.1016/j.bbabio.2005.04.003 PubMedCrossRefGoogle Scholar
  83. Takahashi S, Murata N (2006) Glycerate-3-phosphate, produced by CO2 fixation in the Calvin cycle, is critical for the synthesis of the D1 protein of photosystem II. Biochim Biophys Acta 1757:198–205. doi: 10.1016/j.bbabio.2006.02.002 PubMedCrossRefGoogle Scholar
  84. Tang X-M, Tao X, Wang Y, Ma D-W, Li D, Yang H, Ma X-R (2014) Analysis of DNA methylation of perennial ryegrass under drought using the methylation-sensitive amplification polymorphism (MSAP) technique. Mol Genet Genom 289:1075–1084. doi: 10.1007/s00438-014-0869-6 CrossRefGoogle Scholar
  85. Tefon BE, Maaß S, Özcengiz E, Becher D, Hecker M, Özcengiz G (2011) A comprehensive analysis of Bordetella pertussis surface proteome and identification of new immunogenic proteins. Vaccine 29:3583–3595. doi: 10.1016/j.vaccine.2011.02.086 PubMedCrossRefGoogle Scholar
  86. Thikart P, Kowanij D, Selanan T, Vajrabhaya M, Bangyeekhun T, Chadchawan S (2005) Genetic variation and stress tolerance of somaclonal variegated rice and its original cultivar. J Sci Res Chula Univ 30:63–75Google Scholar
  87. Thorsell A, Portelius E, Blennow K, Westman-Brinkmalm A (2007) Evaluation of sample fractionation using micro-scale liquid-phase isoelectric focusing on mass spectrometric identification and quantitation of proteins in a SILAC experiment. Rapid Commun Mass Spectrom 21:771–778. doi: 10.1002/rcm.2898 PubMedCrossRefGoogle Scholar
  88. Tuteja N, Tarique M, Tuteja R (2014) Rice SUV3 is a bidirectional helicase that binds both DNA and RNA. BMC Plant Biol 14:283. doi: 10.1186/s12870-014-0283-6 PubMedPubMedCentralCrossRefGoogle Scholar
  89. Tuteja N, Sahoo RK, Huda KMK, Tula S, Tuteja R (2015) OsBAT1 augments salinity stress tolerance by enhancing detoxification of ROS and expression of stress-responsive genes in transgenic rice. Plant Mol Biol Rep 33:1192–1209. doi: 10.1007/s11105-014-0827-9 CrossRefGoogle Scholar
  90. Udomchalothorn T, Maneeprasobsuk S, Bangyeekhun E, Boon-Long P, Chadchawan S (2009) The role of the bifunctional enzyme, fructose-6-phosphate-2-kinase/fructose-2,6-bisphosphatase, in carbon partitioning during salt stress and salt tolerance in Rice (Oryza sativa L.). Plant Sci 176:334–341. doi: 10.1016/j.plantsci.2008.11.009 CrossRefGoogle Scholar
  91. Udomchalothorn T, Plaimas K, Comai L, Buaboocha T, Chadchawan S (2014) Molecular karyotyping and exome analysis of salt-tolerant rice mutant from somaclonal variation. Plant Genome. doi: 10.3835/plantgenome2014.04.0016 Google Scholar
  92. Umezawa T et al (2006) CYP707A3, a major ABA 8′-hydroxylase involved in dehydration and rehydration response in Arabidopsis thaliana. Plant J 46:171–182. doi: 10.1111/j.1365-313X.2006.02683.x PubMedCrossRefGoogle Scholar
  93. Urano K, Kurihara Y, Seki M, Shinozaki K (2010) ‘Omics’ analyses of regulatory networks in plant abiotic stress responses. Curr Opin Plant Biol 13:132–138. doi: 10.1016/j.pbi.2009.12.006 PubMedCrossRefGoogle Scholar
  94. Usadel B et al (2009) Co-expression tools for plant biology: opportunities for hypothesis generation and caveats. Plant Cell Environ 32:1633–1651. doi: 10.1111/j.1365-3040.2009.02040.x PubMedCrossRefGoogle Scholar
  95. Vajrabhaya M, Vajrabhaya T (1991) Somaclonal variation for salt tolerance in rice. Biotechnol Agric For 14:368–382Google Scholar
  96. Wang W-S et al (2011) Drought-induced site-specific DNA methylation and its association with drought tolerance in rice (Oryza sativa L.). J Exp Bot 62:1951–1960. doi: 10.1093/jxb/erq391 PubMedCrossRefGoogle Scholar
  97. Wang C, Yang Y, Wang H, Ran X, Li B, Zhang J, Zhang H (2016) Ectopic expression of a cytochrome P450 monooxygenase gene PtCYP714A3 from Populus trichocarpa reduces shoot growth and improves tolerance to salt stress in transgenic rice. Plant Biotechnol J 14:1838–1851. doi: 10.1111/pbi.12544 PubMedPubMedCentralCrossRefGoogle Scholar
  98. Webster DE, Thomas MC (2012) Post-translational modification of plant-made foreign proteins; glycosylation and beyond. Biotechnol Adv 30:410–418. doi: 10.1016/j.biotechadv.2011.07.015 PubMedCrossRefGoogle Scholar
  99. Wessler SR (1996) Plant retrotransposons: turned on by stress. Curr Biol 6:959–961. doi: 10.1016/S0960-9822(02)00638-3 PubMedCrossRefGoogle Scholar
  100. Wolff S et al (2006) Gel-free and gel-based proteomics in Bacillus subtilis. Mol Cell Proteom 5:1183–1192. doi: 10.1074/mcp.M600069-MCP200 CrossRefGoogle Scholar
  101. Xiao X, Yang F, Zhang S, Korpelainen H, Li C (2009) Physiological and proteomic responses of two contrasting Populus cathayana populations to drought stress. Physiol Plant 136:150–168. doi: 10.1111/j.1399-3054.2009.01222.x PubMedCrossRefGoogle Scholar
  102. Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803. doi: 10.1146/annurev.arplant.57.032905.105444 PubMedCrossRefGoogle Scholar
  103. Yoo CY, Pence HE, Jin JB, Miura K, Gosney MJ, Hasegawa PM, Mickelbart MV (2010) The Arabidopsis GTL1 transcription factor regulates water use efficiency and drought tolerance by modulating stomatal density via transrepression of SDD1. Plant Cell 22:4128–4141. doi: 10.1105/tpc.110.078691 PubMedPubMedCentralCrossRefGoogle Scholar
  104. Zavafer A, Cheah MH, Hillier W, Chow WS, Takahashi S (2015) Photodamage to the oxygen evolving complex of photosystem II by visible light. Sci Rep 5:16363.
  105. Zhang XM et al (2014) The cloning and characterization of a DEAD-box RNA helicase from stress-responsive wheat. Physiol Mol Plant Pathol 88:36–42. doi: 10.1016/j.pmpp.2014.07.004 CrossRefGoogle Scholar
  106. Zhu M, Chen G, Dong T, Wang L, Zhang J, Zhao Z, Hu Z (2015) SlDEAD31, a putative DEAD-box RNA helicase gene, regulates salt and drought tolerance and stress-related genes in tomato. PLoS One. doi: 10.1371/journal.pone.0133849 Google Scholar
  107. Zörb C, Herbst R, Forreiter C, Schubert S (2009) Short-term effects of salt exposure on the maize chloroplast protein pattern. Proteomics 9:4209–4220. doi: 10.1002/pmic.200800791 PubMedCrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2017

Authors and Affiliations

  1. 1.Center of Excellence in Environment and Plant Physiology, Department of Botany, Faculty of ScienceChulalongkorn UniversityBangkokThailand
  2. 2.National Center for Genetic Engineering and Biotechnology, Thailand Science ParkPathumthaniThailand
  3. 3.Department of Botany and Plant PathologyPurdue UniversityWest LafayetteUSA
  4. 4.Omics Sciences and Bioinformatics Center, Faculty of ScienceChulalongkorn UniversityBangkokThailand

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