Abstract
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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- AKT1:
-
Inward-rectifier K+ channel
- GAPDH:
-
Glyceraldehyde-3-phosphate dehydrogenase
- GAPB:
-
GAPDH β subunit
- GeLC–MS/MS:
-
Gel-based liquid chromatography–tandem mass spectrometry
- GORK:
-
Guard cell ‘outward-rectifying’ K+ channel
- NBS-LRR:
-
Nucleotide-binding site–leucine-rich repeat
- OSBPs:
-
Oxysterol-binding proteins
- PEG6000:
-
Polyethylene glycol 6000
- PP2C:
-
Protein phosphatase 2C
- PPR:
-
Pentatricopeptide repeat
- SKOR:
-
Stelar K+ ‘outward-rectifying’ channel
- SR:
-
Stress resistant
- SS:
-
Stress susceptible
- TE:
-
Transposable element
References
Abere B et al (2012) Proteomic analysis of Chikungunya virus infected microgial cells. PLoS One 7:e34800. doi:10.1371/journal.pone.0034800
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 233:947–960
Naito K et al (2009) Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 461:1130–1134. http://www.nature.com/nature/journal/v461/n7267/suppinfo/nature08479_S1.html
Ambavaram MMR et al (2014) Coordinated regulation of photosynthesis in rice increases yield and tolerance to environmental stress. Nat Commun 5:5302. http://www.nature.com/articles/ncomms6302#supplementary-information
Ali GM, Komatsu S (2006) Proteomic analysis of rice leaf sheath during drought stress. J Proteome Res 5:396–403
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
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 13:1688–1701
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 9:5019–5026
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
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
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
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
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
Boyer JS (1982) Plant productivity and environment. Science 218:443–448
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
Chadha S, Sharma M (2014) Transposable elements as stress adaptive capacitors induce genomic instability in fungal pathogen Magnaporthe oryzae. PLoS One 9:e94415
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
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
Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought—from genes to the whole plant. Funct Plant Biol 30:239–264
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
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
Coordinators NR (2016) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 44:D7–D19. doi:10.1093/nar/gkv1290
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
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
Deshmukh R et al (2014) Integrating omic approaches for abiotic stress tolerance in soybean. Front Plant Sci 5:244
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
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
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
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
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
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
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
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
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
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
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
Hartwell LH, Hopfield JJ, Leibler S, Murray AW (1999) From molecular to modular cell biology. Nature 402:C47–C52
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
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
Hirochika H, Sugimoto K, Otsuki Y, Tsugawa H, Kanda M (1996) Retrotransposons of rice involved in mutations induced by tissue culture. PNAS 93:7783–7788
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
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
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 59:3327–3346
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, 2009
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 65:305–313
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
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
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
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 145:814–830
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 13:172
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
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
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
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Lisch D (2013) How important are transposons for plant evolution? Nat Rev Genet 14:49–61
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
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 37:98–116
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275
Manna S (2015) An overview of pentatricopeptide repeat proteins and their applications. Biochimie 113:93–99. doi:10.1016/j.biochi.2015.04.004
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
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
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
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
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
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
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
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
Park O-MK (2004) Proteomic studies in plants. BMB Rep 37:133–138
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
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
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
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
Saeed AI et al (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34:374–378
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
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
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
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
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
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
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
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 4:250
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
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
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
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
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 30:63–75
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
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
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
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
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
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
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
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
Vajrabhaya M, Vajrabhaya T (1991) Somaclonal variation for salt tolerance in rice. Biotechnol Agric For 14:368–382
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
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
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
Wessler SR (1996) Plant retrotransposons: turned on by stress. Curr Biol 6:959–961. doi:10.1016/S0960-9822(02)00638-3
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
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
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
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
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. http://www.nature.com/articles/srep16363#supplementary-information
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
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
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
Acknowledgements
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. Hajduch.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Chintakovid, N., Maipoka, M., Phaonakrop, N. et al. Proteomic analysis of drought-responsive proteins in rice reveals photosynthesis-related adaptations to drought stress. Acta Physiol Plant 39, 240 (2017). https://doi.org/10.1007/s11738-017-2532-4
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-017-2532-4