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Proteomic response of oat leaves to long-term salinity stress

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Abstract

Salinity adversely affects plant growth and production. Oat is a moderately salt-tolerant crop and can contribute to improving saline soil. The physiological and molecular responses of the oat plant to long-term salinity were studied. After a 16-day salt treatment (150 mmol L−1NaCl in Hoagland’s solution), photosynthetic rate, maximum photosystem II photochemical efficiency, and actual efficiency of photosystem II decreased. The activities of superoxide dismutase, peroxidase, and catalase significantly increased. We also investigated the protein profiles of oat leaves in response to salinity and detected 30 reproducible protein spots by two-dimensional gel electrophoresis that were differentially abundant. Specifically, one protein was up-regulated and 29 proteins were down-regulated compared with the control. These 29 proteins were identified using MALDI-TOF mass spectrometry, and 19 corresponding genes were further investigated by quantitative real-time PCR. These proteins were involved in four types of biological processes: photosynthesis, carbohydrate metabolism and energy, protein biosynthesis, and folding and detoxification. This study indicates that the lower levels of Calvin cycle-related proteins, 50S ribosomal protein L10 and adenosine-triphosphate regulation-related proteins, and the high levels of antioxidant enzymes play important roles in the response of oat to long-term salinity stress.

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References

  • Abdel-Aal E, Wood P (2004) Specialty grains for food and feed. In: Burrows V (ed) Hulless oats. Amer Assn of Cereal Chemists, Saint Paul, pp. 223–251

    Google Scholar 

  • Aghaei K, Ehsanpour AA, Shah AH, Komatsu S (2009) Proteome analysis of soybean hypocotyl and root under salt stress. Amino Acids 36:91–98

    Article  CAS  Google Scholar 

  • Anjaneyulu E, Reddy PS, Sunita MS, Kishor PK, Meriga B (2014) Salt tolerance and activity of antioxidative enzymes of transgenic finger millet overexpressing a vacuolar H+-pyrophosphatase gene (SbVPPase) from Sorghum bicolor. J Plant Physiol 171:789–798

    Article  CAS  Google Scholar 

  • Bohler S, Bagard M, Oufir M, Planchon S, Hoffmann L, Jolivet Y, Hausman J, Dizengremel P, Renaut J (2007) A DIGE analysis of developing poplar leaves subjected to ozone reveals major changes in carbon metabolism. Proteomics 7:1584–1599

    Article  CAS  Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Bunney TD, Walraven HS, Boer AH (2001) 14-3-3 protein is a regulatorof the mitochondrial and chloroplast ATP synthase. PNAS 98:4249–4254

    Article  CAS  Google Scholar 

  • Burgess P, Huang B (2014) Root protein metabolism in association with improved root growth and drought tolerance by elevated carbon dioxide in creeping bentgrass. Field Crop Res 165:80–91

    Article  Google Scholar 

  • Campbell MT, Knecht AC, Berger B, Brien CJ, Wang D, Walia H (2015) Integrating image-based phenomicsand association analysis to dissect the genetic architecture of temporal salinity responses in rice. Plant Physiol 168:1476–1489

    Article  CAS  Google Scholar 

  • Chang TC, Hsiao CD, Wu SJ, Wang C (2001) The effect of mutating arginine-469 on the substrate binding and refolding activities of 70-kDa heat shock cognate protein. Arch BiochemBiophys 386:30–36

    Article  CAS  Google Scholar 

  • Chen PY, Jia JF, Han XL (2009) Weak microwave can alleviate water deficit induced by osmotic stress in wheat seedlings. Planta 229:291–298

    Article  CAS  Google Scholar 

  • Dahal K, Gadapati W, Savitch LV, Singh J, Hüner NPA (2012) Cold acclimation and BnCBF17-over-expression enhance photosynthetic performance and energy conversion efficiency during long-term growth of Brassica napus under elevated CO2 conditions. Planta 236:1639–1652

    Article  CAS  Google Scholar 

  • Fan Y, Ren CZ, Li PF, Ren TS (2011) Oat growth and cation absorption characteristics under salt and alkali stress. Chin J Appl Ecol 22:2875–2882

    CAS  Google Scholar 

  • Fatehi F, Hosseinzadeh A, Alizadeh H, Brimavandi T, Struik PC (2012) The proteome response of salt-resistant and salt-sensitive barley genotypes to long-term salinity stress. MolBiol Rep 39:6387–6397

    CAS  Google Scholar 

  • Gao WR, Wang XS, Liu QY, Peng H, Chen C, Li JG, Zhang JS, Hu SN, Ma H (2008) Comparative analysis of ESTs in response to drought stress in chickpea (C. arietinum L.). BiochemBioph Res 376:578–583

    Article  CAS  Google Scholar 

  • Gao ZW, Zhang JT, Liu Z, Xu QT, Li XJ, Mu CS (2012) Comparative effects of two alkali stresses, Na2CO3 and NaHCO3 on cell ionic balance, osmotic adjustment, pH, photosynthetic pigments and growth in oat (Avena sativa L.). Aust J Crop Sci 6:995–1003

    CAS  Google Scholar 

  • Garcia JS, Souza GHMF, Eberlin NN, Arruda MAZ (2009) Evaluation of metal-ion stress in sunflower (Helianthus annuus L.) leaves through proteomic changes. Metallomics 1:107–113

    Article  CAS  Google Scholar 

  • Golldack D, Dietz K (2001) Salt-induced expression of the vacuolar H+-ATPase in the common ice plant is developmentally controlled and tissue specific. Plant Physiol 125:1643–1654

    Article  CAS  Google Scholar 

  • Gygi SP, Rochon Y, Franza B, Aebersold R (1999) Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 19:1720–1730

    Article  CAS  Google Scholar 

  • Hanitzsch M, Schnitzer D, Seidel T, Golldack D, Dietz KJ (2007) Transcript level regulation of the vacuolar H+-ATPase subunit isoforms VHA-a, VHA-E and VHA-G in Arabidopsis thaliana. Mol Membr Biol 24:507–518

    Article  CAS  Google Scholar 

  • Heidarvand L, Maali-Amiri R (2013) Physio-biochemical and proteome analysis of chickpea in early phases of cold stress. J Plant Physiol 170:459–469

    Article  CAS  Google Scholar 

  • Hoque TS, Uraji M, Ye WX, Hossain MA, Nakamura Y, Murata Y (2012) Methylglyoxal-induced stomatal closure accompanied by peroxidase-mediated ROS production in Arabidopsis. J Plant Physiol 169:979–986

    Article  CAS  Google Scholar 

  • Hua S, Yuan S, Shamsi IH, Zhao XQ, Zhang X, Liu Y, Wen G, Wang X, Zhang H (2008) A comparison of three isolines of cotton differing in fiber color for yield, quality, and photosynthesis. Crop Sci 49:983–989

    Article  Google Scholar 

  • Imai A, Komura M, Kawano E, Kuwashiro Y, Takahashi T (2008) A semi-dominant mutation in the ribosomal protein L10 gene suppresses the dwarf phenotype of the acl5 mutant in Arabidopsis thaliana. Plant J 56:881–890

    Article  CAS  Google Scholar 

  • Jiang L, Zhang L, Shi Y, Lu ZX, Yu ZF (2014) Proteomic analysis of peach fruit during ripening upon post-harvest heat combined with 1-MCP treatment. J Proteome 98:31–43

    Article  CAS  Google Scholar 

  • Kabała K, Janicka-Russak M, Reda M, Migocka M (2014) Transcriptional regulation of the V-ATPase subunit c and V-PPase isoforms in Cucumis sativus under heavy metal stress. Physiol Plantarum 150:32–45

    Article  Google Scholar 

  • Li G, Wan SW, Zhou J, Yang ZY, Qin P (2010) Leaf chlorophyll fluorescence, hyperspectral reflectance, pigments content, malondialdehyde and proline accumulation responses of castor bean (Ricinuscommunis L.) seedlings to salt stress levels. Ind Crop Prod 31:13–19

    Article  Google Scholar 

  • Liu CW, Chang TS, Hsu YK, Wang AZ, Yen HC, Wu YP, Wang CS, Lai CC (2014) Comparative proteomic analysis of early salt stress responsive proteins in roots and leaves of rice. Proteomics 14:1759–1775

    Article  Google Scholar 

  • Lv WT, Lin B, Zhang M, Hua XJ (2011) Proline accumulation is inhibitory to arabidopsis seedlings during heat stress. Plant Physiol 156:1921–1933

    Article  CAS  Google Scholar 

  • Majee M, Maitra S, Ghosh KG, Pattnaik S, Chatterjee A, Hait NC, Das KP, Majumder AL (2004) A novel salt-tolerant L-myo-inositol-1-phosphate synthase from porteresiacoarctata (Roxb.) Tateoka, a halophytic wild rice. J BiolChem 279:28539–28552

    CAS  Google Scholar 

  • Manaa A, Ahmed HB, Valot B, Bouchet JP, Aschi-Smiti S, Causse M, Faurobert M (2011) Salt and genotype impact on plant physiology and root proteome variations in tomato. J Exp Bot 62:2797–2813

    Article  CAS  Google Scholar 

  • Massacci A, Nabiev SM, Pietrosanti L, Nematov SK, Chernikova TN, Thor K, Leipner J (2008) Response of the photosynthetic apparatus of cotton (Gossypiumhirsutum) to the onset of drought stress under field conditions studied by gas-exchange analysis and chlorophyll fluorescence imaging. Plant physiolBioch 46:189–195

    CAS  Google Scholar 

  • Menz RI, Walker JE, Leslie AGW (2001) Structure of bovine mitochondrial F1-ATPase with nucleotide bound to all three catalytic sites: implications for the mechanism of rotary catalysis. Cell 106:331–341

    Article  CAS  Google Scholar 

  • Moolna A, Bowsher CG (2010) The physiological importance of photosynthetic ferredoxin NADP+ oxidoreductase (FNR) isoforms in wheat. J Exp Bot 61:2669–2681

    Article  CAS  Google Scholar 

  • Munns R, Schachtman DP, Condon AG (1995) The significance of a two-phase growth response to salinity in wheat and barley. Aust J Plant Physiol 22:561–569

    Article  CAS  Google Scholar 

  • Ozfidan-Konakci C, Yildiztugay E, Kucukoduk M (2015) Upregulation of antioxidant enzymes by exogenous gallic acid contributes to the amelioration in Oryza sativa roots exposed to salt and osmotic stress. Environ SciPollut Res 22:1487–1498

    Article  CAS  Google Scholar 

  • Pang QY, Chen SX, Dai SJ, Chen YZ, Wang Y, Yan XF (2010) Comparative proteomics of salt tolerance in Arabidopsis thaliana and thellungiella halophile. J Proteome Res 9:2584–2599

    Article  CAS  Google Scholar 

  • Peng ZY, Wang MC, Li F, Lv HJ, li CL, Xia GM (2009) A proteomic study of the response to salinity and drought stress in an introgression strain of bread wheat. Mol Cell Proteomics 8:2676–2686

    Article  CAS  Google Scholar 

  • Pesaresi P, Varotto C, Meurer J, Jahns P, Salamini F, Leister D (2001) Knock-out of the plastid ribosomal protein L11 in Arabidopsis: effects on mRNA translation and photosynthesis. Plant J 27:179–189

    Article  CAS  Google Scholar 

  • Pinon V, Etchells JP, Rossignol P, Collier SA, Arroyo JM, Martienssen RA, Byrne ME (2008) Three PIGGYBACK genes that specifically influence leaf patterning encode ribosomal proteins. Development 135:1315–1324

    Article  CAS  Google Scholar 

  • Rodríguez AA, Taleisnik EL (2012) Determination of reactive oxygen species in salt-stressed plant tissues. Methods Mol Biol 913:225–236

    Google Scholar 

  • Rogalski M, Schöttler MA, Thiele W, Schulze WX, Bock R (2008) Rpl33, a nonessential plastid-encoded ribosomal protein in tobacco, is required under cold stress conditions. Plant Cell 20:2221–2237

    Article  CAS  Google Scholar 

  • Salekdeh GH, Siopongco J, Wade LJ, Ghareyazie B, Bennett J (2002) A proteomic approach to analyzing drought- and salt-responsiveness in rice. Field Crops Res 76:199–219

    Article  Google Scholar 

  • Sambongi Y, Iko Y, Tanabe M, Omote H, Iwamoto-Kihara A, Ueda I, Yanagida T, Wada Y, Futai M (1999) Mechanical rotation of the c subunit oligomer in ATP synthase (F0F1): direct observation. Science 286:1722–1724

    Article  CAS  Google Scholar 

  • Sreenivasulu N, Miranda M, Prakash HS, Wobus U, Weschke W (2004) Transcriptome changes in foxtail millet genotypes at high salinity: identification and characterization of a PHGPX gene specifically up-regulated by NaCl in a salt-tolerant line. J Plant Physiol 161:467–477

    Article  CAS  Google Scholar 

  • Tian XH, Li XP, Zhou HL, Zhang JS, Gong ZZ, Chen SY (2005) OsDREB 4 genes in rice encode AP2 containing proteins that bind specifically to the dehydration responsive element. J Integr Plant Biol 47:467–476

    Article  CAS  Google Scholar 

  • Turan S, Tripathy BC (2013) Salt and genotype impact on antioxidative enzymes and lipid peroxidation in two rice cultivars during de-etiolation. Protoplasma 250:209–222

    Article  CAS  Google Scholar 

  • Wang B, Song FB (2006) Physiological responses and adaptive capacity of oats to saline-alkali stress. Ecol Environ 15:625–629

    Google Scholar 

  • Wang MC, Peng ZY, Li CL, Li F, Liu C, Xia GM (2008) Proteomic analysis on a high salt tolerance introgression strain of Triticumaestivum/Thinopyrumponticum. Proteomics 8:1470–1489

    Article  CAS  Google Scholar 

  • Xu S, Hu B, He ZY, Ma F, Feng JF, Shen WB, Yang J (2011) Enhancement of salinity tolerance during rice seed germination by presoaking with hemoglobin. Int J MolSci 12:2488–2501

    Article  CAS  Google Scholar 

  • Xu J, Duan XG, Yang J, Beeching JR, Zhang P (2013) Enhanced reactive oxygen species scavenging by overproduction of superoxide dismutase and catalase delays postharvest physiological deterioration of cassava storage roots. Plant Physiol 161:1517–1528

    Article  CAS  Google Scholar 

  • Yan SP, Tang ZC, Su WA, Sun WN (2005) Proteomic analysis of salt stress-responsive proteins in rice root. Proteomics 5:235–244

    Article  CAS  Google Scholar 

  • Yang S, Jiang ZQ, Yan QJ, Zhu HF (2008) Characterization of a thermostable extracellular-glucosidase with activities of exoglucanase and transglycosylation from paecilomyces thermophile. J Agric Food Chem 56:602–608

    Article  CAS  Google Scholar 

  • Zhao GQ, Ma BL, Ren CZ (2006) Growth, gas exchange, chlorophyll fluorescence, and ion content of naked oat in response to salinity. Crop Sci 47:123–131

    Article  Google Scholar 

  • Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by the National Natural Science Foundation of China (31060174, 30660084), the Natural Science Foundation of Inner Mongolia, China (2010ZD07, 200607010301), the Technology System of Agricultural Industry of China (CARS-08-B-5), and the Item of Science Innovation Team of Inner Mongolia Agricultural University (NDTD2010-8). We thank Dr. Yan Weikai from the Eastern Cereal and Oilseed Research Center of Agriculture and the Agri-Food Canada.

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Correspondence to Jinghui Liu or Yuqing Wang.

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Responsible editor: Yi-ping Chen

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Bai, J., Qin, Y., Liu, J. et al. Proteomic response of oat leaves to long-term salinity stress. Environ Sci Pollut Res 24, 3387–3399 (2017). https://doi.org/10.1007/s11356-016-8092-0

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