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Physiological and comparative proteomic analyses of saline-alkali NaHCO3-responses in leaves of halophyte Puccinellia tenuiflora

  • Zepeng Yin
  • Heng Zhang
  • Qi Zhao
  • Mi-Jeong Yoo
  • Ning Zhu
  • Jianlan Yu
  • Juanjuan Yu
  • Siyi Guo
  • Yuchen Miao
  • Sixue Chen
  • Zhi QinEmail author
  • Shaojun DaiEmail author
Regular Article
First Online:
  • 25 Downloads

Abstract

Aims

Soil alkalization imposes severe ion toxicity, osmotic stress, and high pH stress to plants, inhibiting their growth and productivity. NaHCO3 is a main component of alkaline soil. However, knowledge of the NaHCO3-responsive proteomic pattern of alkaligrass is still lacking. Alkaligrass (Puccinellia tenuiflora) is a monocotyledonous halophyte pasture widely distributed in the Songnen Plain in Northeastern China. This study aims to investigate the NaHCO3-responsive molecular mechanisms in the alkaligrass plants.

Methods

An integrative approach including photosynthetic and redox physiology, and comparative proteomics was used.

Results

NaHCO3 decreased photosynthesis, but increased nonphotochemical quenching, increased membrane electrolyte leakage of alkaligrass, and increased proline and glycine betaine concentrations in leaves. In addition, the NaHCO3 stress increased Na+ concentration and decreased K+/Na+ ratio in leaves, while Ca2+ and Mg2+ concentrations were maintained, contributing to signaling and homeostasis of ion and enzyme activity. Furthermore, O2− generation rate and H2O2 concentration were increased, and the activities of ten antioxidant enzymes and antioxidant concentrations were changed in response to the NaHCO3 stress. Proteomics revealed 90 NaHCO3-responsive proteins, 54% of which were localized in chloroplasts. They were mainly involved in signaling, photosynthesis, stress and defense, carbohydrate and energy metabolism, as well as protein synthesis, processing and turnover. Some protein abundances did not correlate well with their activities, implying that the enzyme activities were affected by NaHCO3-induced post-translational modifications.

Conclusions

To cope with the NaHCO3 stress, alkaligrass deployed multiple strategies, including triggering phospholipase D (PLD)-mediated Ca2+ signaling pathways, enhancing diverse reactive oxygen species (ROS) scavenging pathways, and regulating chloroplast protein synthesis and processing.

Keywords

Soil alkalization Halophyte Puccinellia tenuiflora NaHCO3-responsive mechanisms Proteomics 
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Notes

Acknowledgments

The project was supported by grants from the Foundation of Shanghai Science and Technology Committee, China (No. 17391900600), Capacity Construction Project of Local Universities, Shanghai, China (No. 14390502700) to Shaojun Dai, the Found of Shanghai Engineering Research Center of Plant Germplasm Resources (No.17DZ2252700), and the National Natural Science Foundation of China (31801848) to Zepeng Yin.

Author’s contribution

Shaojun Dai and Zhi Qin conceived and designed the experiments; Zepeng Yin, Heng Zhang, Qi Zhao, Ning Zhu, Siyi Guo, Yuchen Miao, Tai Wang, and Jianlan Yu participated in experiments and data analyses; Zepeng Yin wrote the manuscript with inputs and guidance from Shaojun Dai, Sixue Chen, Mi-Jeong Yoo and Zhi Qin. All authors have read and approved the final manuscript.

Compliance with ethical standards

Conflicts of interest

The authors declare no conflict of interest.

Supplementary material

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References

  1. Aghaei K, Ehsanpour AA, Komatsu S (2008) Proteome analysis of potato under salt stress. J Proteome Res 7:4858–4868.  https://doi.org/10.1021/pr800460y CrossRefGoogle Scholar
  2. Ardie SW, Xie L, Takahashi R, Liu S, Takano T (2009) Cloning of a high-affinity K+ transporter gene PutHKT2;1 from Puccinellia tenuiflora and its functional comparison with OsHKT2;1 from rice in yeast and Arabidopsis. J Exp Bot 60:3491–3502.  https://doi.org/10.1093/jxb/erp184 CrossRefGoogle Scholar
  3. Ardie SW, Liu S, Takano T (2010) Expression of the AKT1-type K+ channel gene from Puccinellia tenuiflora, PutAKT1, enhances salt tolerance in Arabidopsis. Plant Cell Rep 29:865–874.  https://doi.org/10.1007/s00299-010-0872-2 CrossRefGoogle Scholar
  4. Ardie SW, Nishiuchi S, Liu S, Takano T (2011) Ectopic expression of the K+ channel beta subunits from Puccinellia tenuiflora (KPutB1) and rice (KOB1) alters K+ homeostasis of yeast and Arabidopsis. Mol Biotechnol 48:76–86.  https://doi.org/10.1007/s12033-010-9349-3 CrossRefGoogle Scholar
  5. Bandehagh A, Salekdeh GH, Toorchi M, Mohammadi A, Komatsu S (2011) Comparative proteomic analysis of canola leaves under salinity stress. Proteomics 11:1965–1975.  https://doi.org/10.1002/pmic.201000564 CrossRefGoogle Scholar
  6. Bradford MM (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.  https://doi.org/10.1016/0003-2697(76)90527-3 CrossRefGoogle Scholar
  7. Chen W, Cui P, Sun H, Guo W, Yang C, Jin H, Fang B, Shi D (2009) Comparative effects of salt and alkali stresses on organic acid accumulation and ionic balance of seabuckthorn (Hippophae rhamnoides L.). Ind Crop Prod 30:351–358.  https://doi.org/10.1016/j.indcrop.2009.06.007 CrossRefGoogle Scholar
  8. Chen F, Zhang S, Jiang H, Ma W, Korpelainen H, Li C (2011) Comparative proteomics analysis of salt response reveals sex-related photosynthetic inhibition by salinity in Populus cathayana cuttings. J Proteome Res 10:3944–3958.  https://doi.org/10.1021/pr200535r CrossRefGoogle Scholar
  9. Colmer T, Munns R, Flowers T (2005) Improving salt tolerance of wheat and barley: future prospects. Aust J Exp Agric 45:1425–1443.  https://doi.org/10.1071/EA04162 CrossRefGoogle Scholar
  10. Dai S, Li L, Chen T, Chong K, Xue Y, Wang T (2006) Proteomic analyses of Oryza sativa mature pollen reveal novel proteins associated with pollen germination and tube growth. Proteomics 6:2504–2529.  https://doi.org/10.1002/pmic.200401351 CrossRefGoogle Scholar
  11. Fan X, Wang J, Yang N, Dong Y, Liu L, Wang F, Wang N, Chen H, Liu W, Sun Y, Wu JY, Li H (2013) Gene expression profiling of soybean leaves and roots under salt, saline-alkali and drought stress by high-throughput Illumina sequencing. Gene 512:392–402.  https://doi.org/10.1016/j.gene.2012.09.100 CrossRefGoogle Scholar
  12. Gallois JL, Guyon-Debast A, Lecureuil A, Vezon D, Carpentier V, Bonhomme S, Guerche P (2009) The Arabidopsis proteasome RPT5 subunits are essential for gametophyte development and show accession-dependent redundancy. Plant Cell 21:442–459.  https://doi.org/10.1105/tpc.108.062372 CrossRefGoogle Scholar
  13. Ge Y, Li Y, Zhu YM, Bai X, Lv D, Guo D, Ji W, Cai H (2010) Global transcriptome profiling of wild soybean (Glycine soja) roots under NaHCO3 treatment. BMC Plant Biol 10:153.  https://doi.org/10.1186/1471-2229-10-153 CrossRefGoogle Scholar
  14. Gong M, Li Y, Chen S (1998) Abscisic acid-induced thermotolerance in maize seedlings is mediated by calcium and associated with antioxidant systems. J Plant Physiol 153:488–496.  https://doi.org/10.1016/S0176-1617(98)80179-X CrossRefGoogle Scholar
  15. Grieve CM, Grattan SR (1983) Rapid assay for determination of water soluble quaternary ammonium compounds. Plant Soil 70:303–307.  https://doi.org/10.1007/bf02374789 CrossRefGoogle Scholar
  16. Guan Q, Wang Z, Wang X, Takano T, Liu S (2015) A peroxisomal APX from Puccinellia tenuiflora improves the abiotic stress tolerance of transgenic Arabidopsis thaliana through decreasing of H2O2 accumulation. J Plant Physiol 175:183–191.  https://doi.org/10.1016/j.jplph.2014.10.020 CrossRefGoogle Scholar
  17. Guo G, Ge P, Ma C, Li X, Lv D, Wang S, Ma W, Yan Y (2012) Comparative proteomic analysis of salt response proteins in seedling roots of two wheat varieties. J Proteome 75:1867–1885.  https://doi.org/10.1016/j.jprot.2011.12.032 CrossRefGoogle Scholar
  18. Guo R, Yang Z, Li F, Yan C, Zhong X, Liu Q, Xia X, Li H, Zhao L (2015) Comparative metabolic responses and adaptive strategies of wheat (Triticum aestivum) to salt and alkali stress. BMC Plant Biol 15:170.  https://doi.org/10.1186/s12870-015-0546-x CrossRefGoogle Scholar
  19. Guo S, Dai S, Singh P, Wang H, Wang Y, Tan J, Wee W, Ito T (2018) A membrane-bound NAC-like transcription factor OsNTL5 represses the flowering in Oryza sativa. Front Plant Sci 9:555.  https://doi.org/10.3389/fpls.2018.00555 CrossRefGoogle Scholar
  20. Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genomics 2014:701596–701518.  https://doi.org/10.1155/2014/701596 CrossRefGoogle Scholar
  21. Hager A (2003) Role of the plasma membrane H+-ATPase in auxin-induced elongation growth: historical and new aspects. J Plant Res 116:483–505.  https://doi.org/10.1007/s10265-003-0110-x CrossRefGoogle Scholar
  22. Hu G, Liu Y, Zhang X, Yao F, Huang Y, Ervin EH, Zhao B (2015) Physiological evaluation of alkali-salt tolerance of thirty switchgrass (Panicum virgatum) lines. PLoS One 10:e0125305.  https://doi.org/10.1371/journal.pone.0125305 CrossRefGoogle Scholar
  23. Ibrahim MH, Jaafar HZ (2012) Primary, secondary metabolites, H2O2, malondialdehyde and photosynthetic responses of Orthosiphon stimaneus Benth. to different irradiance levels. Molecules 17:1159–1176.  https://doi.org/10.3390/molecules17021159 CrossRefGoogle Scholar
  24. Ji W, Cong R, Li S, Li R, Qin Z, Li Y, Zhou X, Chen S, Li J (2016) Comparative proteomic analysis of soybean leaves and roots by iTRAQ provides insights into response mechanisms to short-term salt stress. Front Plant Sci 7:573.  https://doi.org/10.3389/fpls.2016.00573 Google Scholar
  25. Jiang Y, Yang B, Harris NS, Deyholos MK (2007) Comparative proteomic analysis of NaCl stress-responsive proteins in Arabidopsis roots. J Exp Bot 58:3591–3607.  https://doi.org/10.1093/jxb/erm207 CrossRefGoogle Scholar
  26. Jin S, Cheng Y, Guan Q, Liu D, Takano T, Liu S (2006) A metallothionein-like protein of rice (rgMT) functions in E. coli and its gene expression is induced by abiotic stresses. Biotechnol Lett 28:1749–1753.  https://doi.org/10.1007/s10529-006-9152-1 CrossRefGoogle Scholar
  27. Julkowska MM, Testerink C (2015) Tuning plant signaling and growth to survive salt. Trends Plant Sci 20:586–594.  https://doi.org/10.1016/j.tplants.2015.06.008 CrossRefGoogle Scholar
  28. Kmiec B, Glaser E (2012) A novel mitochondrial and chloroplast peptidasome, PreP. Physiol Plant 145:180–186.  https://doi.org/10.1111/j.1399-3054.2011.01531.x CrossRefGoogle Scholar
  29. Knight H, Trewavas A, Knight M (1997) Calcium signalling in Arabidopsis thaliana responding to drought and salinity. Plant J 12:1067–1078.  https://doi.org/10.1046/j.1365-313X.1997.12051067.x CrossRefGoogle Scholar
  30. Kobayashi S, Abe N, Yoshida KT, Liu S, Takano T (2012) Molecular cloning and characterization of plasma membrane- and vacuolar-type Na+/H+ antiporters of an alkaline-salt-tolerant monocot, Puccinellia tenuiflora. J Plant Res 125:587–594.  https://doi.org/10.1007/s10265-012-0475-9 CrossRefGoogle Scholar
  31. Kobayashi S, Satone H, Tan E, Kurokochi H, Asakawa S, Liu S, Takano T (2014) Transcriptional responses of a bicarbonate-tolerant monocot, Puccinellia tenuiflora, and a related bicarbonate-sensitive species, Poa annua, to NaHCO3 stress. Int J Mol Sci 16:496–509.  https://doi.org/10.3390/ijms16010496 CrossRefGoogle Scholar
  32. Law MY, Charles SA, Halliwell B (1983) Glutathione and ascorbic acid in spinach (spinacia oleracea) chloroplasts. The effect of hydrogen peroxide and of paraquat. Biochem J 210:899–903.  https://doi.org/10.1042/bj2100899 CrossRefGoogle Scholar
  33. Linder P, Jankowsky E (2011) From unwinding to clamping - the DEAD box RNA helicase family. Nat Rev Mol Cell Biol 12:505–516.  https://doi.org/10.1038/nrm3154 CrossRefGoogle Scholar
  34. Liu J, Shi D (2010) Photosynthesis, chlorophyll fluorescence, inorganic ion and organic acid accumulations of sunflower in responses to salt and salt-alkaline mixed stress. Photosynthetica 48:127–134.  https://doi.org/10.1007/s11099-010-0017-4 CrossRefGoogle Scholar
  35. Liu D, Zhang X, Cheng Y, Takano T, Liu S (2006) rHsp90 gene expression in response to several environmental stresses in rice (Oryza sativa L.). Plant Physiol Biochem 44:380–386.  https://doi.org/10.1016/j.plaphy.2006.06.011 CrossRefGoogle Scholar
  36. Liu S, Cheng Y, Zhang X, Guan Q, Nishiuchi S, Hase K, Takano T (2007) Expression of an NADP-malic enzyme gene in rice (Oryza sativa. L) is induced by environmental stresses; over-expression of the gene in Arabidopsis confers salt and osmotic stress tolerance. Plant Mol Biol 64:49–58.  https://doi.org/10.1007/s11103-007-9133-3 CrossRefGoogle Scholar
  37. Liu H, Zhang X, Takano T, Liu S (2009) Characterization of a PutCAX1 gene from Puccinellia tenuiflora that confers Ca2+ and Ba2+ tolerance in yeast. Biochem Biophys Res Commun 383:392–396.  https://doi.org/10.1016/j.bbrc.2009.04.042 CrossRefGoogle Scholar
  38. Lv B, Li X, Ma H, Sun Y, Wei L, Jiang C, Liang Z (2013) Differences in growth and physiology of rice in response to different saline-alkaline stress factors. Agron J 105:1119–1128.  https://doi.org/10.2134/agronj2013.0017 CrossRefGoogle Scholar
  39. Lynch J, Polito VS, Lauchli A (1989) Salinity stress increases cytoplasmic ca activity in maize root protoplasts. Plant Physiol 90:1271–1274.  https://doi.org/10.1104/pp.90.4.1271 CrossRefGoogle Scholar
  40. Makhnevych T, Houry WA (2012) The role of Hsp90 in protein complex assembly. Biochim Biophys Acta 1823:674–682.  https://doi.org/10.1016/j.bbamcr.2011.09.001 CrossRefGoogle Scholar
  41. Meng X, Zhao Q, Jin Y, Yu J, Yin Z, Chen S, Dai S (2016) Chilling-responsive mechanisms in halophyte Puccinellia tenuiflora seedlings revealed from proteomics analysis. J Proteome 143:365–381.  https://doi.org/10.1016/j.jprot.2016.04.038 CrossRefGoogle Scholar
  42. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681.  https://doi.org/10.1146/annurev.arplant.59.032607.092911 CrossRefGoogle Scholar
  43. Pang Q, Chen S, Dai S, Chen Y, Wang Y, Yan X (2010) Comparative proteomics of salt tolerance in Arabidopsis thaliana and Thellungiella halophila. J Proteome Res 9:2584–2599.  https://doi.org/10.1021/pr100034f CrossRefGoogle Scholar
  44. Peng Y, Zhu Y, Mao Y, Wang S, Su W, Tang Z (2004) Alkali grass resists salt stress through high [K+] and an endodermis barrier to Na+. J Exp Bot 55:939–949.  https://doi.org/10.1093/jxb/erh071 CrossRefGoogle Scholar
  45. Peng Z, Wang M, Li F, Lv H, Li C, Xia G (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.  https://doi.org/10.1074/mcp.M900052-MCP200 CrossRefGoogle Scholar
  46. Porcel R, Ruiz-Lozano JM (2004) Arbuscular mycorrhizal influence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. J Exp Bot 55:1743–1750.  https://doi.org/10.1093/jxb/erh188 CrossRefGoogle Scholar
  47. Ritchie S, Gilroy S (2000) Abscisic acid stimulation of phospholipase D in the barley aleurone is G-protein-mediated and localized to the plasma membrane. Plant Physiol 124:693–702.  https://doi.org/10.1104/pp.124.2.693 CrossRefGoogle Scholar
  48. Sengupta S, Majumder AL (2009) Insight into the salt tolerance factors of a wild halophytic rice, Porteresia coarctata: a physiological and proteomic approach. Planta 229:911–929.  https://doi.org/10.1007/s00425-008-0878-y CrossRefGoogle Scholar
  49. Shi DC, Yin L (1993) Difference between salt (NaCl) and alkaline (Na2CO3) stresses on Puccinellia tenuiflora (Griseb.) Scribn. et Merr. Acta Bot Sin 35:144–149Google Scholar
  50. Shi DC, Yin SJ, Yang GH, Zhao KF (2002) Citric acid accumulation in an alkali-tolerant plant Puccinellia tenuiflora under alkaline stress. Acta Bot Sin 44:537–540.  https://doi.org/10.1038/sj/onc/1205418 Google Scholar
  51. Silverman IM, Li F, Gregory BD (2013) Genomic era analyses of RNA secondary structure and RNA-binding proteins reveal their significance to post-transcriptional regulation in plants. Plant Sci 205-206:55–62.  https://doi.org/10.1016/j.plantsci.2013.01.009 CrossRefGoogle Scholar
  52. Sun G, Peng Y, Shao H, Chu L, Zhao X, Min H, Cao W, Wei C (2005) Does Puccinelia tenuiflora have the ability of salt exudation? Colloids Surf B Biointerfaces 46:197–203.  https://doi.org/10.1016/j.colsurfb.2005.11.003 CrossRefGoogle Scholar
  53. Suo J, Zhao Q, Zhang Z, Chen S, Cao J, Liu G, Wei X, Wang T, Yang C, Dai S (2015) Cytological and proteomic analyses of Osmunda cinnamomea germinating spores reveal characteristics of fern spore germination and rhizoid tip growth. Mol Cell Proteomics 14:2510–2534.  https://doi.org/10.1074/mcp.M114.047225 CrossRefGoogle Scholar
  54. Timm S, Florian A, Arrivault S, Stitt M, Fernie AR, Bauwe H (2012) Glycine decarboxylase controls photosynthesis and plant growth. FEBS Lett 586:3692–3697.  https://doi.org/10.1016/j.febslet.2012.08.027 CrossRefGoogle Scholar
  55. Tuteja N (2007) Mechanisms of high salinity tolerance in plants. Methods Enzymol 428:419–438.  https://doi.org/10.1016/s0076-6879(07)28024-3 CrossRefGoogle Scholar
  56. Valpuesta V, Botella MA (2004) Biosynthesis of L-ascorbic acid in plants: new pathways for an old antioxidant. Trends Plant Sci 9:573–577.  https://doi.org/10.1016/j.tplants.2004.10.002 CrossRefGoogle Scholar
  57. van Kooten O, Snel JF (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150.  https://doi.org/10.1007/bf00033156 CrossRefGoogle Scholar
  58. Vizcaíno JA, Csordas A, del-Toro N, Dianes JA, Griss J, Lavidas I, Mayer G, Perez-Riverol Y, Reisinger F, Ternent T, Xu QW, Wang R, Hermjakob H (2016) 2016 update of the PRIDE database and its related tools. Nucleic Acids Res 44:D447–D456.  https://doi.org/10.1093/nar/gkv1145 CrossRefGoogle Scholar
  59. Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252.  https://doi.org/10.1016/j.tplants.2004.03.006 CrossRefGoogle Scholar
  60. Wang Y, Yang C, Liu G, Jiang J (2007a) Development of a cDNA microarray to identify gene expression of Puccinellia tenuiflora under saline-alkali stress. Plant Physiol Biochem 45:567–576.  https://doi.org/10.1016/j.plaphy.2007.05.006 CrossRefGoogle Scholar
  61. Wang Y, Chu Y, Liu G, Wang MH, Jiang J, Hou Y, Qu G, Yang C (2007b) Identification of expressed sequence tags in an alkali grass (Puccinellia tenuiflora) cDNA library. J Plant Physiol 164:78–89.  https://doi.org/10.1016/j.jplph.2005.12.006 CrossRefGoogle Scholar
  62. Wang Y, Yang C, Liu G, Zhang G, Ban Q (2007c) Microarray and suppression subtractive hybridization analyses of gene expression in Puccinellia tenuiflora after exposure to NaHCO3. Plant Sci 173:309–320.  https://doi.org/10.1016/j.plantsci.2007.06.011 CrossRefGoogle Scholar
  63. Wang Y, Ma H, Liu G, Xu C, Zhang D, Ban Q (2008a) Analysis of gene expression profile of Limonium bicolor under NaHCO3 stress using cDNA microarray. Plant Mol Biol Report 26:241–254.  https://doi.org/10.1007/s11105-008-0037-4 CrossRefGoogle Scholar
  64. Wang Y, Ma H, Liu G, Yang C (2008b) Generation and analysis of expressed sequence tags from a NaHCO3-treated Limonium bicolor cDNA library. Plant Physiol Biochem 46:977–986.  https://doi.org/10.1016/j.plaphy.2008.06.001 CrossRefGoogle Scholar
  65. Wang X, Chen S, Zhang H, Shi L, Cao F, Guo L, Xie Y, Wang T, Yan X, Dai S (2010) Desiccation tolerance mechanism in resurrection fern-ally Selaginella tamariscina revealed by physiological and proteomic analysis. J Proteome Res 9:6561–6577.  https://doi.org/10.1021/pr100767k CrossRefGoogle Scholar
  66. Wang S, Kurepa J, Hashimoto T, Smalle JA (2011) Salt stress-induced disassembly of Arabidopsis cortical microtubule arrays involves 26S proteasome-dependent degradation of SPIRAL1. Plant Cell 23:3412–3427.  https://doi.org/10.1105/tpc.111.089920 CrossRefGoogle Scholar
  67. Wang H, Wu Z, Han J, Zheng W, Yang C (2012) Comparison of ion balance and nitrogen metabolism in old and young leaves of alkali-stressed rice plants. PLoS One 7:e37817.  https://doi.org/10.1371/journal.pone.0037817 CrossRefGoogle Scholar
  68. Wang L, Liu X, Liang M, Tan F, Liang W, Chen Y, Lin Y, Huang L, Xing J, Chen W (2014) Proteomic analysis of salt-responsive proteins in the leaves of mangrove Kandelia candel during short-term stress. PLoS One 9:e83141.  https://doi.org/10.1371/journal.pone.0083141 CrossRefGoogle Scholar
  69. Yadav SK, Singla-Pareek SL, Reddy MK, Sopory SK (2005) Transgenic tobacco plants overexpressing glyoxalase enzymes resist an increase in methylglyoxal and maintain higher reduced glutathione levels under salinity stress. FEBS Lett 579:6265–6271.  https://doi.org/10.1016/j.febslet.2005.10.006 CrossRefGoogle Scholar
  70. Yan B, Dai Q, Liu X, Huang S, Wang Z (1996) Flooding-induced membrane damage, lipid oxidation and activated oxygen generation in corn leaves. Plant Soil 179:261–268.  https://doi.org/10.1007/bf00009336 CrossRefGoogle Scholar
  71. Yan SP, Zhang QY, Tang ZC, Su WA, Sun WN (2006) Comparative proteomic analysis provides new insights into chilling stress responses in rice. Mol Cell Proteomics 5:484–496.  https://doi.org/10.1074/mcp.M500251-MCP200 CrossRefGoogle Scholar
  72. Yang C, Chong J, Li C, Kim C, Shi D, Wang D (2007) Osmotic adjustment and ion balance traits of an alkali resistant halophyte Kochia sieversiana during adaptation to salt and alkali conditions. Plant Soil 294:263–276.  https://doi.org/10.1007/s11104-007-9251-3 CrossRefGoogle Scholar
  73. Yang C, Wang P, Li C, Wang D (2008) Comparison of effects of salt and alkali stresses on the growth and photosynthesis of wheat. Photosynthetica 46:107–114.  https://doi.org/10.1007/s11099-008-0018-8 CrossRefGoogle Scholar
  74. Yin Z, Ren J, Zhou L, Sun L, Wang J, Liu Y, Song X (2016) Water deficit mechanisms in perennial shrubs Cerasus humilis leaves revealed by physiological and proteomic analyses. Proteome Sci 15:9.  https://doi.org/10.1186/s12953-017-0117-1 CrossRefGoogle Scholar
  75. Yin Z, Balmant K, Geng S, Zhu N, Zhang T, Dufresne C, Dai S, Chen S (2017) Bicarbonate induced redox proteome changes in Arabidopsis suspension cells. Front Plant Sci 8:58.  https://doi.org/10.3389/fpls.2017.00058 Google Scholar
  76. Yu S, Zhang X, Guan Q, Takano T, Liu S (2007) Expression of a carbonic anhydrase gene is induced by environmental stresses in rice (Oryza sativa L.). Biotechnol Lett 29:89–94. doi:  https://doi.org/10.1007/s10529-006-9199-z
  77. Yu J, Chen S, Zhao Q, Wang T, Yang C, Diaz C, Sun G, Dai S (2011) Physiological and proteomic analysis of salinity tolerance in Puccinellia tenuiflora. J Proteome Res 10:3852–3870.  https://doi.org/10.1021/pr101102p CrossRefGoogle Scholar
  78. Yu J, Chen S, Wang T, Sun G, Dai S (2013) Comparative proteomic analysis of Puccinellia tenuiflora leaves under Na2CO3 stress. Int J Mol Sci 14:1740–1762.  https://doi.org/10.3390/ijms14011740 CrossRefGoogle Scholar
  79. Zhang X, Takano T, Liu S (2006) Identification of a mitochondrial ATP synthase small subunit gene (RMtATP6) expressed in response to salts and osmotic stresses in rice (Oryza sativa L.). J Exp Bot 57:193–200.  https://doi.org/10.1093/jxb/erj025 CrossRefGoogle Scholar
  80. Zhang C, Nishiuchi S, Liu S, Takano T (2008) Characterization of two plasma membrane protein 3 genes (PutPMP3) from the alkali grass, Puccinellia tenuiflora, and functional comparison of the rice homologues, OsLti6a/b from rice. BMB Rep 41:448–454.  https://doi.org/10.5483/BMBRep.2008.41.6.448 CrossRefGoogle Scholar
  81. Zhang H, Han B, Wang T, Chen S, Li H, Zhang Y, Dai S (2012) Mechanisms of plant salt response: insights from proteomics. J Proteome Res 11:49–67.  https://doi.org/10.1021/pr200861w CrossRefGoogle Scholar
  82. Zhang X, Wei L, Wang Z, Wang T (2013) Physiological and molecular features of Puccinellia tenuiflora tolerating salt and alkaline-salt stress. J Integr Plant Biol 55:262–276.  https://doi.org/10.1111/jipb.12013 CrossRefGoogle Scholar
  83. Zhang M, Takano T, Liu S, Zhang X (2014) Abiotic stress response in yeast and metal-binding ability of a type 2 metallothionein-like protein (PutMT2) from Puccinellia tenuiflora. Mol Biol Rep 41:5839–5849.  https://doi.org/10.1007/s11033-014-3458-1 CrossRefGoogle Scholar
  84. Zhang A, Zang W, Zhang X, Ma Y, Yan X, Pang Q (2016) Global proteomic mapping of alkali stress regulated molecular networks in Helianthus tuberosus L. Plant Soil 409:175–202.  https://doi.org/10.1007/s11104-016-2945-7 CrossRefGoogle Scholar
  85. Zhang L, Pu H, Duan Z, Li Y, Liu B, Zhang Q, Li W, Rochaix J, Liu L, Peng L (2018) Nucleus-encoded protein BFA1 promotes efficient assembly of the chloroplast ATP synthase coupling factor 1. Plant Cell 30:1770–1788.  https://doi.org/10.1105/tpc.18.00075 CrossRefGoogle Scholar
  86. Zhao Q, Suo J, Chen S, Jin Y, Ma X, Yin Z, Zhang Y, Wang T, Luo J, Jin W, Zhang X, Zhou Z, Dai S (2016) Na2CO3-responsive mechanisms in halophyte Puccinellia tenuiflora roots revealed by physiological and proteomic analyses. Sci Rep 6:32717.  https://doi.org/10.1038/srep32717 CrossRefGoogle Scholar
  87. Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71.  https://doi.org/10.1016/S1360-1385(00)01838-0 CrossRefGoogle Scholar
  88. Zörb C, Schmitt S, Muhling KH (2010) Proteomic changes in maize roots after short-term adjustment to saline growth conditions. Proteomics 10:4441–4449.  https://doi.org/10.1002/pmic.201000231 CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Development Centre of Plant Germplasm Resources, College of Life SciencesShanghai Normal UniversityShanghaiChina
  2. 2.Alkali Soil Natural Environmental Science Center, Key Laboratory of Saline-alkali Vegetation Ecology Restoration, Ministry of EducationNortheast Forestry UniversityHarbinChina
  3. 3.Horticulture Department, College of HorticultureShenyang Agricultural UniversityShenyangChina
  4. 4.Department of Biology, Genetics Institute, Plant Molecular and Cellular Program, Interdisciplinary Center for Biotechnology ResearchUniversity of FloridaGainesvilleUSA
  5. 5.AB Sciex Asia Pacific Application Support CenterShanghaiChina
  6. 6.Institute of Plant Stress Biology, State Key Laboratory of Cotton Biology, Department of BiologyHenan UniversityKaifengChina

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