Advertisement

Plant Cell, Tissue and Organ Culture (PCTOC)

, Volume 131, Issue 1, pp 75–88 | Cite as

Populus euphratica J3 mediates root K+/Na+ homeostasis by activating plasma membrane H+-ATPase in transgenic Arabidopsis under NaCl salinity

  • Yinan Zhang
  • Yang Wang
  • Gang Sa
  • Yuhong Zhang
  • Jiayin Deng
  • Shurong Deng
  • Meijuan Wang
  • Huilong Zhang
  • Jun Yao
  • Xiuying Ma
  • Rui Zhao
  • Xiaoyang Zhou
  • Cunfu Lu
  • Shanzhi Lin
  • Shaoliang Chen
Original Article

Abstract

NaCl induced PeJ3 (a DnaJ homolog) expression in Populus euphratica cell cultures. In contrast, salt treatment inhibited transcription of a J3-interacting protein kinase gene, PePKS5 (Salt Overly Sensitive 2-Like Protein Kinase 5). To clarify the mechanism by which PeJ3 conferred salinity tolerance, we isolated PeJ3 from P. euphratica and transformed it into Arabidopsis. PeJ3 overexpression inhibited AtPKS5 expression, but had no effect on AtJ3 transcripts. After 10-day exposures to 100 mM NaCl, PeJ3-transgenic lines showed prolonged survival (40–54.4%) and longer roots (43.8–51.1%) compared to wild-type (WT) and vector control (VC) plants. The observed differences in salt acclimation between transgenic and WT depended on their ability to exclude Na+ and maintain intracellular K+. PeJ3-transgenic Arabidopsis accumulated less Na+ in root cells, due at least in part, to the high Na+ efflux in roots. K+ flux recordings revealed that PeJ3-transgenic lines lost less K+ than WT and VC under salt stress. In vitro and in vivo activity assays revealed that PeJ3-overexpression upregulated plasma membrane H+-ATPase activity and enhanced H2O2 signaling in salt-stressed Arabidopsis. Consequently, PeJ3-transgenic plants retained high H+-pumping activity under NaCl salinity, which contributed to K+/Na+ homeostasis in roots. In conclusion, PeJ3 overexpression resulted in H+-ATPase activation through transcriptional AtPKS5 suppression and/or interactions with AtPKS5 kinase. Under salinity stress, upregulated H+-pumps (i) promoted Na+/H+ exchange across the Arabidopsis plasma membrane, (ii) reduced K+ efflux mediated by depolarization-activated plasma membrane channels, and (iii) stimulated H2O2 signaling, which increased cytosolic free Ca2+ and stimulated Na+ extrusion through Salt Overly Sensitive signaling in Arabidopsis.

Keywords

Populus euphratica DnaJ homolog 3 PM H+-ATPase NaCl PKS5 H2O2 Arabidopsis Ion flux NMT 

Notes

Acknowledgements

The research was supported jointly by the Fundamental Research Funds for the Central Universities (Grant No. 2017ZY07), National Natural Science Foundation of China (Grant Nos. 31570587 and 31270654), the Research Project of the Chinese Ministry of Education (Grant No. 113013A), Beijing Natural Science Foundation (Grant No. 6172024), the Program of Introducing Talents of Discipline to Universities (111 Project, Grant No. B13007), and the Program for Changjiang Scholars and Innovative Research Teams in University (Grant No. IRT13047).

Author Contributions

Y-NZ, YW, and SC conceived the original screening and research plans; SC, CL, SL, and RZ supervised the experiments; Y-NZ, YW, GS, Y-HZ, and JD performed most of the experiments; SD, MW, HZ, JY, XM, RZ, and XZ provided technical assistance to Y-NZ, YW, GS, Y-HZ, JD; Y-NZ and YW analyzed the experimental data; Y-NZ wrote the article and SC supervised the writing. All coauthors agreed and approved the manuscript.

Supplementary material

11240_2017_1263_MOESM1_ESM.pdf (687 kb)
Supplementary material 1 (PDF 687 KB)

References

  1. Akbari M, Labeau F (2003) The plasma membrane proton pump ATPase: the significance of gene subfamilies. Planta 216:355–365Google Scholar
  2. Apse MP, Blumwald E (2007) Na+ transport in plants. FEBS Lett 581:2247–2254CrossRefPubMedGoogle Scholar
  3. Blumwald E, Aharon GS, Apse MP (2000) Sodium transport in plant cells. Biochim Biophys Acta 1465:140–151CrossRefPubMedGoogle Scholar
  4. Boston RS, Viitanen PV, Vierling E (1996) Molecular chaperones and protein folding in plants. Plant Mol Biol 32:191–222CrossRefPubMedGoogle Scholar
  5. Britto DT, Kronzucker HJ (2008) Cellular mechanisms of potassium transport in plants. Physiol Plant 133:637–650CrossRefPubMedGoogle Scholar
  6. Camoni L, Iori V, Marra M, Aducci P (2000) Phosphorylation-dependent interaction between plant plasma membrane H+-ATPase and 14-3-3 proteins. J Biol Chem 275:9919–9923CrossRefPubMedGoogle Scholar
  7. Caplan AJ, Cyr DM, Douglas MG (1993) Eukaryotic homologues of Escherichia coli dnaJ: a diverse protein family that functions with hsp70 stress proteins. Mol Biol Cell 4:555–563CrossRefPubMedPubMedCentralGoogle Scholar
  8. Chen S, Polle A (2010) Salinity tolerance of Populus. Plant Biol 12:317–333CrossRefPubMedGoogle Scholar
  9. Chen Z, Newman I, Zhou M, Mendham N, Zhang G, Shabala S (2005) Screening plants for salt tolerance by measuring K+ flux: a case study for barley. Plant Cell Environ 28:1230–1246CrossRefGoogle Scholar
  10. Chen Z, Pottosin II, Cuin TA, Fuglsang AT, Tester M, Jha D, Zepeda-Jazo I, Zhou M, Palmgren MG, Newman IA (2007) Root plasma membrane transporters controlling K+/Na+ homeostasis in salt-stressed barley. Plant Physiol 145:1714–1725CrossRefPubMedPubMedCentralGoogle Scholar
  11. Chen S, Hawighorst P, Sun J, Polle A (2014) Salt tolerance in Populus: significance of stress signaling networks, mycorrhization, and soil amendments for cellular and whole-plant nutrition. Environ Exp Bot 107:113–124CrossRefGoogle Scholar
  12. Chung JS, Zhu JK, Bressan RA, Hasegawa PM, Shi H (2008) Reactive oxygen species mediate Na+-induced SOS1 mRNA stability in Arabidopsis. Plant J 53:554–565CrossRefGoogle Scholar
  13. Clough SJ, Bent AF (1998) Floral dip: a simplified method for grobacteriummediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefPubMedGoogle Scholar
  14. Cuin TA, Betts SA, Chalmandrier R, Shabala S (2008) A root’s ability to retain K+ correlates with salt tolerance in wheat. J Exp Bot 59:2697–2706CrossRefPubMedPubMedCentralGoogle Scholar
  15. Cuin TA, Bose J, Stefano G, Jha D, Tester M, Mancuso S, Shabala S (2011) Assessing the role of root plasma membrane and tonoplast Na+/H+ exchangers in salinity tolerance in wheat: in planta quantification methods. Plant Cell Environ 34:947–961CrossRefPubMedGoogle Scholar
  16. Ding M, Hou P, Shen X, Wang M, Deng S, Sun J, Xiao F, Wang R, Zhou X, Lu C (2010) Salt-induced expression of genes related to Na+/K+ and ROS homeostasis in leaves of salt-resistant and salt-sensitive poplar species. Plant Mol Biol 73:251–269CrossRefPubMedGoogle Scholar
  17. Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446CrossRefPubMedGoogle Scholar
  18. Frías I, Serrano R (1996) A major isoform of the maize plasma membrane H+-ATPase: characterization and induction by auxin in coleoptiles. Plant Cell 8:1533–1544PubMedPubMedCentralGoogle Scholar
  19. Fuglsang AT, Guo Y, Cuin TA, Qiu Q, Song C, Kristinasen KA, Bych K, Schulz A, Shabala S, Schumaker KS (2007) Arabidopsis protein kinase PKS5 inhibits the plasma membrane H+ -ATPase by preventing interaction with 14-3-3 protein. Plant Cell 19:1617–1634CrossRefPubMedPubMedCentralGoogle Scholar
  20. Gévaudant F, Duby G, Stedingk EV, Zhao R, Morsomme P, Boutry M (2007) Expression of a constitutively activated plasma membrane H+-ATPase alters plant development and increases salt tolerance. Plant Physiol 144:1763–1776CrossRefPubMedPubMedCentralGoogle Scholar
  21. Greenway AH, Munns R (2003) Mechanisms of salt tolerance in nonhalophytes. Annu Rev Plant Biol 31:149–190CrossRefGoogle Scholar
  22. Hamdia MA, Shaddad, M. AK (2010) Salt tolerance of crop plants. J Stress Physiol Biochem 6(3):64–90Google Scholar
  23. Han Y, Wang W, Sun J, Ding M, Zhao R, Deng S, Wang F, Hu Y, Wang Y, Lu Y, Du L, Hu Z, Diekmann H, Shen X, Polle A, Chen S (2013) Populus euphratica XTH overexpression enhances salinity tolerance by the development of leaf succulence in transgenic tobacco plants. J Exp Bot 64:4225–4238CrossRefPubMedPubMedCentralGoogle Scholar
  24. Han Y, Sa G, Sun J, Shen Z, Zhao R, Ding M, Deng S, Lu Y, Zhang Y, Shen X, Chen S (2014) Overexpression of Populus euphratica xyloglucan endotransglucosylase/hydrolase gene confers enhanced cadmium tolerance by the restriction of root cadmium uptake in transgenic tobacco. Environ Exp Bot 100:74–83CrossRefGoogle Scholar
  25. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499CrossRefPubMedGoogle Scholar
  26. Horie T, Karahara I, Katsuhara M (2012) Salinity tolerance mechanisms in glycophytes: an overview with the central focus on rice plants. Rice 5:11CrossRefPubMedPubMedCentralGoogle Scholar
  27. Janicka-Russak M (2011) Plant plasma membrane H+-ATPase in adaptation of plants to abiotic stresses. In: Shanker A, Venkateswarlu B (eds) Abiotic stress response in plants—physiological, biochemical and genetic perspectives, Chap. 8. InTech, Rijeka, pp 197–218Google Scholar
  28. Kim YS, Min JK, Kim D, Jung J (2001) A soluble auxin-binding protein, ABP57. Purification with anti-bovine serum albumin antibody and characterization of its mechanistic role in the auxin effect on plant plasma membrane H+-ATPase. J Biol Chem 276:10730–10736CrossRefPubMedGoogle Scholar
  29. Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones J, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. Embo J 22:2623–2633CrossRefPubMedPubMedCentralGoogle Scholar
  30. Larsson C, Widell S, Kjellbom P (1987) Preparation of high-purity plasma membranes. Methods Enzymol 148C:558–568CrossRefGoogle Scholar
  31. Laufen T, Mayer MP, Beisel C, Klostermeier D, Mogk A, Reinstein J, Bukau B (1999) Mechanism of regulation of hsp70 chaperones by DnaJ cochaperones. Proc Natl Acad Sci USA 96:5452–5457CrossRefPubMedPubMedCentralGoogle Scholar
  32. Leshem Y, Melamedbook N, Cagnac O, Ronen G, Nishri Y, Solomon M, Cohen G, Levine A (2006) Suppression of Arabidopsis vesicle-SNARE expression inhibited fusion of H2O2-containing vesicles with tonoplast and increased salt tolerance. Proc Natl Acad Sci 103:18008–18013CrossRefPubMedPubMedCentralGoogle Scholar
  33. Li GL, Li B, Liu HT, Zhou RG (2005) The responses of AtJ2 and AtJ3 gene expression to environmental stresses in Arabidopsis. Acta Photophysiol Sin 31:47–52Google Scholar
  34. Li J, Bao S, Zhang Y, Ma X, Mishra-Knyrim M, Sun J, Sa G, Shen X, Polle A, Chen S (2012) Paxillus involutus strains MAJ and NAU mediate K+/Na+ homeostasis in ectomycorrhizal Populus × canescens under sodium chloride stress. Plant Physiol 159:1771–1786CrossRefPubMedPubMedCentralGoogle Scholar
  35. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–∆∆CT method. Methods 25:402–408CrossRefPubMedGoogle Scholar
  36. Lu Y, Li N, Sun J, Hou P, Jing X, Zhu H, Deng S, Han Y, Huang X, Ma X, Zhao N, Zhang Y, Shen X, Chen S (2013) Exogenous hydrogen peroxide, nitric oxide and calcium mediate root ion fluxes in two non-secretor mangrove species subjected to NaCl stress. Tree Physiol 33:81–95CrossRefPubMedGoogle Scholar
  37. Merlot S, Leonhardt N, Fenzi F, Valon C, Costa M, Piette L, Vavasseur A, Genty B, Boivin K, Müller A (2007) Constitutive activation of a plasma membrane H+-ATPase prevents abscisic acid-mediated stomatal closure. Embo J 26:3216–3226CrossRefPubMedPubMedCentralGoogle Scholar
  38. Mittler R, Vanderauwera S, Gollery M, Van BF (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498CrossRefPubMedGoogle Scholar
  39. Morsomme P, Boutry M (2000) The plant plasma membrane H+-ATPase: structure, function and regulation. Biochim Biophys Acta 1465:1–16CrossRefPubMedGoogle Scholar
  40. Moschou PN, Paschalidis KA, Delis ID, Andriopoulou AH, Lagiotis GD, Yakoumakis DI, Roubelakis-Angelakis KA (2008) Spermidine exodus and oxidation in the apoplast induced by abiotic stress is responsible for H2O2 signatures that direct tolerance responses in tobacco. Plant Cell 20:1708–1724CrossRefPubMedPubMedCentralGoogle Scholar
  41. Moshe S, Robert F (2006) Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol 141:336–340CrossRefGoogle Scholar
  42. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681CrossRefPubMedGoogle Scholar
  43. Ohnishi T, Gall RS, Mayer ML (1975) An improved assay of inorganic phosphate in the presence of extralabile phosphate compounds: application to the ATPase assay in the presence of phosphocreatine. Anal Biochem 69:261–267CrossRefPubMedGoogle Scholar
  44. Ottow EA, Polle A, Brosché M, Kangasjärvi J, Dibrov P, Zörb C, Teichmann T (2005) Molecular characterization of PeNhaD1: the first member of the NhaD Na+/H+ antiporter family of plant origin. Plant Mol Biol 58:75–88CrossRefPubMedGoogle Scholar
  45. Oufattole MM, Boutry M (2000) Identification and expression of three new Nicotiana plumbaginifolia genes which encode isoforms of a plasma-membrane H+-ATPase, and one of which is induced by mechanical stress. Planta 210:715–722CrossRefPubMedGoogle Scholar
  46. Palmgren MG (2001) Plant plasma membrane H+-ATPases: powerhouses for nutrient uptake. Plant Biol 52:817–845Google Scholar
  47. Palmgren MG, Sommarin M, Serrano R, Larsson C (1991) Identification of an autoinhibitory domain in the C-terminal region of the plant plasma membrane H+-ATPase. J Biol Chem 266:20470–20475PubMedGoogle Scholar
  48. Polle A, Chen S (2015) On the salty side of life: molecular, physiological and anatomical adaptation and acclimation of trees to extreme habitats. Plant Cell Environ 38:1794–1816CrossRefPubMedGoogle Scholar
  49. Roberkleber N, Albrechtová JT, Fleig S, Huck N, Michalke W, Wagner E, Speth V, Neuhaus G, Fischeriglesias C (2003) Plasma membrane H+-ATPase is involved in auxin-mediated cell elongation during wheat embryo development. Plant Physiol 131:1302–1312CrossRefGoogle Scholar
  50. Shabala S, Demidchik V, Shabala L, Cuin TA, Smith SJ, Miller AJ, Davies JM, Newman IA (2006) Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+ -permeable channels. Plant Physiol 141:1653–1665CrossRefPubMedPubMedCentralGoogle Scholar
  51. Shabala L, Zhang J, Pottosin I, Bose J, Zhu M, Fuglsang AT, Velardebuendia A, Massart A, Hill CB, Roessner U (2016) Cell-type specific H+-ATPase activity enables root K+ retention and mediates acclimation to salinity. Plant Physiol 172:2445–2458CrossRefPubMedPubMedCentralGoogle Scholar
  52. Shen Z, Ding M, Sun J, Deng S, Zhao R, Wang M, Ma X, Wang F, Zhang H, Qian Z, Hu Y, Yu R, Shen X, Chen S (2013) Overexpression of PeHSF mediates leaf ROS homeostasis in transgenic tobacco lines grown under salt stress conditions. Plant Cell Tiss Organ Cult 115:299–308CrossRefGoogle Scholar
  53. Shen Z, Sun J, Yao J, Wang S, Ding M, Zhang H, Qian Z, Zhao N, Sa G, Zhao R, Shen X, Polle A, Chen S (2015) High rates of virus-induced gene silencing by tobacco rattle virus in Populus. Tree Physiol 35:1016–1029CrossRefPubMedGoogle Scholar
  54. Shi HZ, Ishitani M, Cheolsoo K, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci 97:6896–6901CrossRefPubMedPubMedCentralGoogle Scholar
  55. Shi H, Lee B, Wu SJ, Zhu JK (2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol 21:81–85CrossRefPubMedGoogle Scholar
  56. Silver PA, Way JC (1993) Eukaryotic DnaJ homologs and the specificity of Hsp70 activity. Cell 74:5–6CrossRefPubMedGoogle Scholar
  57. Song X, Duanmu H, Yu Y, Chen C, Sun X, Zhu P, Chen R, Duan X, Li H, Cao L, Nisa Z, Li Q, Zhu Y, Ding X (2017) GsJ11, identified by genome-wide analysis, facilitates alkaline tolerance in transgenic plants. Plant Cell Tiss Organ Cult 129:411–430CrossRefGoogle Scholar
  58. Sun J, Chen S, Dai S, Wang R, Li N, Shen X, Zhou X, Lu C, Zheng X, Hu Z, Zhang Z, Song J, Xu Y (2009a) NaCl-induced alternations of cellular and tissue ion fluxes in roots of salt-resistant and salt-sensitive poplar species. Plant Physiol 149:1141–1153CrossRefPubMedPubMedCentralGoogle Scholar
  59. Sun J, Dai S, Wang R, Chen S, Li N, Zhou X, Lu C, Shen X, Zheng X, Hu Z, Zhang Z, Song J, Xu Y (2009b) Calcium mediates root K+/Na+ homeostasis in poplar species differing in salt tolerance. Tree Physiol 29:1175–1186CrossRefPubMedGoogle Scholar
  60. Sun J, Li L, Liu M, Wang M, Ding M, Deng S, Lu C, Zhou X, Shen X, Zheng X, Chen S (2010a) Hydrogen peroxide and nitric oxide mediate K+/Na+ homeostasis and antioxidant defense in NaCl-stressed callus cells of two contrasting poplars. Plant Cell Tiss Organ Cult 103:205–215CrossRefGoogle Scholar
  61. Sun J, Wang MJ, Ding M, Deng S, Liu M, Lu C, Zhou X, Shen X, Zheng X, Zhang Z, Song Z, Hu Z, Xu Y, Chen S (2010b) H2O2 and cytosolic Ca2+ signals triggered by the PM H+-coupled transport system mediate K+/Na+ homeostasis in NaCl-stressed Populus euphratica cells. Plant Cell Environ 33:943–958CrossRefPubMedGoogle Scholar
  62. Sun J, Zhang X, Deng S, Zhang C, Wang M, Ding M, Zhao R, Shen X, Zhou X, Lu C, Chen S (2012) Extracellular ATP signaling is mediated by H2O2 and cytosolic Ca2+ in the salt response of Populus euphratica cells. PLoS ONE 7(12):e53136CrossRefPubMedPubMedCentralGoogle Scholar
  63. Svennelid F, Olsson A, Piotrowski M, Rosenquist M, Ottman C, Larsson C, Oecking C, Sommarin M (2000) Phosphorylation of Thr-948 at the C terminus of the plasma membrane H+-ATPase creates a binding site for the regulatory 14-3-3 protein. Plant Cell 11:2379–2391Google Scholar
  64. Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperons in the abiotic stress response. Trends Plant Sci 9:244–252CrossRefPubMedGoogle Scholar
  65. Wang F, Deng S, Ding M, Sun J, Wang M, Zhu H, Han Y, Shen Z, Jing X, Zhang F, Hu Y, Shen X, Chen S (2013a) Overexpression of a poplar two-pore K+ channel enhances salinity tolerance in tobacco cells. Plant Cell Tiss Organ Cult 112:19–31CrossRefGoogle Scholar
  66. Wang M, Wang Y, Sun J, Ding M, Deng S, Hou P, Ma X, Zhang Y, Wang F, Sa G, Tan Y, Lang T, Li J, Shen X, Chen S (2013b) Overexpression of PeHA1 enhances hydrogen peroxide signaling in salt-stressed Arabidopsis. Plant Physiol Biochem 71:37–48CrossRefPubMedGoogle Scholar
  67. Waters ER, Vierling E (1996) Evolution, structure and function of the small heat shock proteins in plants. J Exp Bot 47:325–338CrossRefGoogle Scholar
  68. Wu Y, Nan D, Xin Z, Zhao M, Chang Z, Liu J, Zhang L (2007) Molecular characterization of PeSOS1: the putative Na+/H+ antiporter of Populus euphratica. Plant Mol Biol 65:1–11CrossRefPubMedGoogle Scholar
  69. Xing T, Higgins VJ, Blumwald E (1997) Identification of G proteins mediating fungal elicitor-induced dephosphorylation of host plasma membrane H+ -ATPase. J Exp Bot 48:229–237CrossRefGoogle Scholar
  70. Yang Y, Qin Y, Xie C, Zhao F, Zhao J, Liu D, Chen S, Fuglsang AT, Palmgren MG, Schumaker KS (2010) The Arabidopsis chaperone J3 regulates the plasma membrane H+-ATPase through interaction with the PKS5 kinase. Plant Cell 22:1313–1332CrossRefPubMedPubMedCentralGoogle Scholar
  71. Zhang X, Wang H, Takemiya A, Song CP, Kinoshita T, Shimazaki K (2004) Inhibition of blue light-dependent H+ pumping by abscisic acid through hydrogen peroxide-induced dephosphorylation of the plasma membrane H+-ATPase in guard cell protoplasts. Plant Physiol 136:4150–4158CrossRefPubMedPubMedCentralGoogle Scholar
  72. Zhang F, Wang Y, Yang Y, Hao WU, Wang DI, Liu J (2007) Involvement of hydrogen peroxide and nitric oxide in salt resistance in the calluses from Populus euphratica. Plant Cell Environ 30:775–785CrossRefPubMedGoogle Scholar
  73. Zhao N, Wang S, Ma X, Zhu H, Sa G, Sun J, Li N, Zhao C, Zhao R, Chen S (2016) Extracellular ATP mediates cellular K+/Na+ homeostasis in two contrasting poplar species under NaCl stress. Trees 30:825–837CrossRefGoogle Scholar
  74. Zhou RG, Miernyk JA (1999) Cloning and analysis of AtJ3 gene in Arabidopsis thaliana. Acta Bot Sin 41:597–602Google Scholar
  75. Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71CrossRefPubMedGoogle Scholar
  76. Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445CrossRefPubMedGoogle Scholar
  77. Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  • Yinan Zhang
    • 1
  • Yang Wang
    • 1
  • Gang Sa
    • 1
  • Yuhong Zhang
    • 1
  • Jiayin Deng
    • 1
  • Shurong Deng
    • 1
  • Meijuan Wang
    • 1
  • Huilong Zhang
    • 1
  • Jun Yao
    • 1
  • Xiuying Ma
    • 2
  • Rui Zhao
    • 1
  • Xiaoyang Zhou
    • 1
  • Cunfu Lu
    • 1
  • Shanzhi Lin
    • 1
  • Shaoliang Chen
    • 1
  1. 1.Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology (Box 162)Beijing Forestry UniversityBeijingPeople’s Republic of China
  2. 2.Department of life Science and EngineeringJining UniversityQufuPeople’s Republic of China

Personalised recommendations