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Plant Molecular Biology

, Volume 73, Issue 3, pp 251–269 | Cite as

Salt-induced expression of genes related to Na+/K+ and ROS homeostasis in leaves of salt-resistant and salt-sensitive poplar species

  • Mingquan Ding
  • Peichen Hou
  • Xin Shen
  • Meijuan Wang
  • Shurong Deng
  • Jian Sun
  • Fei Xiao
  • Ruigang Wang
  • Xiaoyang Zhou
  • Cunfu Lu
  • Deqiang Zhang
  • Xiaojiang Zheng
  • Zanmin Hu
  • Shaoliang Chen
Article

Abstract

Using the Affymetrix poplar genome array, we explored the leaf transcriptome of salt-tolerant Populus euphratica Oliv. and salt-sensitive P. popularis 35-44 (P. popularis) under control and saline conditions. Our objective was to clarify the genomic differences in regulating K+/Na+ and reactive oxygen species (ROS) homeostasis between the two species. Compared to P. popularis, salt-tolerant P. euphratica responses to salinity involved induction of a relatively larger number of probesets after short-term (ST) exposure to 150 mM NaCl (24 h) and relatively fewer probesets after a long-term (LT) exposure to salinity (200 mM NaCl, 28 days). Compared to P. popularis, leaves of the control P. euphratica plants exhibited a higher transcript abundance of genes related to Na+/H+ antiport (Na+/H+ antiporters, H+ pumps) and K+ uptake and transport. Notably, the expression of these genes did not decrease (with a few exceptions) during salt treatment. Regarding ROS homeostasis, P. euphratica exhibited rapid up-regulation of a variety of antioxidant enzymes after exposure to ST salinity, indicating a rapid adaptive response to salt stress. However, the effect of NaCl on transcription in P. popularis leaves was more pronounced after exposure to prolonged salinity. LT-stressed P. popularis up-regulated some genes mediating K+/Na+ homeostasis but decreased transcription of main scavengers of superoxide radicals and H2O2 except for some isoforms of a few scavengers. Mineral and ROS analyses show that NaCl induced a marked increase of leaf Na+ and H2O2 in LT-stressed plants of the two species and the effects were even more pronounced in the salt-sensitive poplar. We place the transcription results in the context of our physiological measurements to infer some implications of NaCl-induced alterations in gene expression related to K+/Na+ and ROS homeostasis.

Keywords

Affymetrix poplar genome array NaCl Populus euphratica P. popularis Salt tolerance 

Notes

Acknowledgments

The research was supported jointly by the HI-TECH Research and Development Programme of China (863 Programme, grant number 2006AA10Z131), the National Natural Science Foundation of China (grant numbers 30430430, 30872005), the Foundation for Supervisors of Beijing Excellent Doctoral Dissertations (grant number YB20081002201), the Foundation for Authors of the National Excellent Doctoral Dissertation of PR China (grant number 200152), the Teaching and Research Award Programme for Outstanding Young Teachers at Higher Education Institutions of the Ministry of Education (MOE), PRC (grant number 2002-323), the Key project of the MOE, PRC (grant number 2009-84) and the Natural Science Foundation of Hubei Province (grant number 2007ABB003). We thank Prof. Dr. Tom Hazenberg (Faculty of Forestry and the Forest Environment, Lakehead University, Thunder Bay, ON, Canada) for his English corrections. We acknowledge the offer for the use of the confocal miscroscope by the Platform of Large Instruments and Equipment at Beijing Forestry University.

Supplementary material

11103_2010_9612_MOESM1_ESM.doc (633 kb)
(DOC 633 kb)
11103_2010_9612_MOESM2_ESM.doc (562 kb)
(DOC 562 kb)

References

  1. Amtmann A, Sanders D (1999) Mechanisms of Na+ uptake by plant cells. Adv Bot Res 29:75–112CrossRefGoogle Scholar
  2. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Ann Rev Plant Biol 55:373–399CrossRefGoogle Scholar
  3. Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285:1256–1258CrossRefPubMedGoogle Scholar
  4. Beritognolo I, Piazzai M, Benucci S, Kuzminsky E, Sabatti M, Mugnozza GS, Muleo R (2007) Functional characterisation of three Italian Populus alba L. genotypes under salinity stress. Trees (Berl) 21:465–477CrossRefGoogle Scholar
  5. Brosché M, Vinocur B, Alatalo ER, Lamminmäki A, Teichmann T, Ottow EA, Djilianov D, Afif D, Bogeat-Triboulot M-B, Altman A, Polle A, Dreyer E, Rudd S, Paulin L, Auvinen P, Kangasjärvi J (2005) Gene expression and metabolite profiling of Populus euphratica growing in the Negev desert. Genome Biol 6(R101):1–17Google Scholar
  6. Chen CX (2007). PeNhaD1 gene transformation and salt resistance of transgenic Populus tomentosa. PhD thesis, Beijing Forestry University, Beijing, People’s Republic of China (in Chinese)Google Scholar
  7. Chen S, Polle A (2010) Salinity tolerance of Populus. Plant Biol 12:317–333CrossRefPubMedGoogle Scholar
  8. Chen S, Li J, Wang S, Hüttermann A, Altman A (2001) Salt, nutrient uptake and transport, and ABA of Populus euphratica; a hybrid in response to increasing soil NaCl. Trees (Berl) 15:186–194CrossRefGoogle Scholar
  9. Chen S, Li J, Fritz E, Wang S, Hüttermann A (2002a) Sodium and chloride distribution in roots and transport in three poplar genotypes under increasing NaCl stress. For Ecol Manag 168:217–230CrossRefGoogle Scholar
  10. Chen S, Li J, Wang T, Wang S, Polle A, Hüttermann A (2002b) Osmotic stress and ion-specific effects on xylem abscisic acid and the relevance to salinity tolerance in poplar. J Plant Growth Regul 21:224–233CrossRefGoogle Scholar
  11. Chen S, Li J, Wang S, Fritz E, Hüttermann A, Altman A (2003a) Effects of NaCl on shoot growth, transpiration, ion compartmentation, and transport in regenerated plants of Populus euphratica and Populus tomentosa. Can J For Res 33:967–975CrossRefGoogle Scholar
  12. Chen S, Li J, Wang T, Wang S, Polle A, Hüttermann A (2003b) Gas exchange, xylem ions and abscisic acid response to Na+-salts and Cl-salts in Populus euphratica. Acta Bot Sin 45:561–566Google Scholar
  13. 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
  14. Chen Z, Pottosin II, Cuin TA, Fuglsang AT, Tester M, Jha D, Zepeda-Jazo I, Zhou M, Palmgren MG, Newman IA, Shabala S (2007) Root plasma membrane transporters controlling K+/Na+ homeostasis in salt stressed barley. Plant Physiol 145:1714–1725CrossRefPubMedGoogle Scholar
  15. Chinnusamy V, Jagendorf A, Zhu J-K (2005) Understanding and improving salt tolerance in plants. Crop Sci 45:437–448CrossRefGoogle Scholar
  16. 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 59:2697–2706CrossRefPubMedGoogle Scholar
  17. Czempinski K, Frachisse JM, Maurel C, Barbier-Brygoo H, Mueller-Roeber B (2002) Vacuolar membrane localization of the Arabidopsis ‘two-pore’ K+ channel KCO1. Plant J 29:809–820CrossRefPubMedGoogle Scholar
  18. Dai S, Chen S, Fritz E, Olbrich A, Kettner C, Polle A, Hüttermann A (2006) Ion compartmentation in leaf cells of Populus euphratica and P. tomentosa under salt stress. J Beijing For Univ 28(Suppl 2):1–5 (in Chinese with English abstract)Google Scholar
  19. Darley CP, van Wuytswinkel OC, van der Woude K, Mager WH, de Boer AH (2000) Arabidopsis thaliana and Saccharomyces cerevisiae NHX1 genes encode amiloride sensitive electroneutral Na+/H+ exchangers. Biochem J 351:241–249CrossRefPubMedGoogle Scholar
  20. Demidchik V, Maathuis FJM (2007) Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. New Phytol 175:387–404CrossRefPubMedGoogle Scholar
  21. Escalante-Pérez M, Lautner S, Nehls U, Selle A, Teuber M, Schnitzler JP, Teichmann T, Fayyaz P, Hartung W, Polle A, Fromm J, Hedrich R, Ache P (2009) Salt stress affects xylem differentiation of grey poplar (Populus × canescens). Planta 229:299–309CrossRefPubMedGoogle Scholar
  22. Fukuda A, Nakamura A, Tanaka Y (1999) Molecular cloning and expression of the Na+/H+ exchanger gene in Oryza sativa. Biochim Biophys Acta 1446:149–155PubMedGoogle Scholar
  23. Gaxiola RA, Rao R, Sherman A, Grisafi P, Alper SL, Fink GR (1999) The Arabidopsis thaliana proton transporters, AtNhx1 and Avp1, can function in cation detoxification in yeast. Proc Natl Acad Sci USA 96:1480–1485CrossRefPubMedGoogle Scholar
  24. Grene (2002) Oxidative stress and acclimation mechanisms in plants. The Arabidopsis Book (Special revue), The American Society of Plant Biologists, Rockville, MD, USA, pp 1–20Google Scholar
  25. Gu R, Fonseca S, Puskás LG, Hackler L Jr, Zvara Á, Dudits D, Pais MS (2004) Transcript identification and profiling during salt stress and recovery of Populus euphratica. Tree Physiol 24:265–276PubMedGoogle Scholar
  26. Kreps JA, Wu Y, Chang H-S, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130:2129–2141CrossRefPubMedGoogle Scholar
  27. Laurie S, Feeney KA, Maathuis FJ, Heard PJ, Brown SJ, Leigh RA (2002) A role for HKT1 in sodium uptake by wheat roots. Plant J 32:139–149CrossRefPubMedGoogle Scholar
  28. Ma T, Liu Q, Li Z, Zhang X (2002) Tonoplast H+-ATPase in response to salt stress in Populus euphratica cell suspensions. Plant Sci 163:499–505CrossRefGoogle Scholar
  29. Mäser P, Gierth M, Schroder J (2002) Molecular mechanisms of potassium and sodium uptake in plants. Plant Soil 247:43–54CrossRefGoogle Scholar
  30. Ottow EA, Brinker M, Teichmann T, Fritz E, Kaiser W, Brosché M, Kangasjärvi J, Jiang X, Polle A (2005a) Populus euphratica displays apoplastic sodium accumulation, osmotic adjustment by decreases in calcium and soluble carbohydrates, and develops leaf succulence under salt stress. Plant Physiol 139:1762–1772CrossRefPubMedGoogle Scholar
  31. Ottow EA, Polle A, Brosché M, Kangasjärvi J, Dibrov P, Zörb C, Teichmann T (2005b) Molecular characterization of PeNhaD1: the first member of the NhaD Na+/H+ antiporter family of plant origin. Plant Mol Biol 58:73–86CrossRefGoogle Scholar
  32. Quintero FJ, Blatt MR, Pardo JM (2000) Functional conservation between yeast and plant endosomal Na+/H+ antiporters. FEBS Lett 471:224–228CrossRefPubMedGoogle Scholar
  33. Roxas VP, Smith RK Jr, Allen ER, Allen RD (1997) Overexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nat Biotechnol 15:988–991CrossRefPubMedGoogle Scholar
  34. Roxas VP, Lodhi SA, Garrett DK, Mahan JR, Allen RD (2000) Stress tolerance in transgenic tobacco seedlings that overexpress glutathione S-transferase/glutathione peroxidase. Plant Cell Physiol 41:1229–1234CrossRefPubMedGoogle Scholar
  35. Rubio F, Gassmann W, Schroeder JI (1995) Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science 270:1660–1663CrossRefPubMedGoogle Scholar
  36. Rus A, Yokoi S, Sharkhuu A, Reddy M, Lee BH, Matsumoto TK, Koiwa H, Zhu JK, Bressan RA, Hasegawa PM (2001) AtHKT1 is a salt tolerance determinant that controls Na+ entry into plant roots. Proc Natl Acad Sci USA 98:14150–14155CrossRefPubMedGoogle Scholar
  37. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, Sturn A, Snuffin M, Rezantsev A, Popov D, Ryltsov A, Kostukovich E, Borisovsky I, Liu Z, Vinsavich A, Trush V, Quackenbush J (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34:374–378PubMedGoogle Scholar
  38. Schachtman DP, Kumar R, Schroeder JI, Marsh EL (1997) Molecular and functional characterization of a novel low-affinity cation transporter (LCT1) in higher plants. Proc Natl Acad Sci USA 94:11079–11084CrossRefPubMedGoogle Scholar
  39. Serrano R (1996) Salt tolerance in plants and microorganisms: toxicity targets and defense responses. Int Rev Cytol 165:1–52CrossRefPubMedGoogle Scholar
  40. Serrano R, Rodriguez PL (2002) Plants, genes and ions: workshop on the molecular basis of ionic homeostasis and salt tolerance in plants. EMBO Rep 3:116–119CrossRefPubMedGoogle Scholar
  41. Shabala S (2000) Ionic and osmotic components of salt stress specifically modulate net ion fluxes from bean leaf mesophyll. Plant Cell Environ 23:825–837CrossRefGoogle Scholar
  42. Shabala S, Cuin TA (2008) Cellular mechanisms of potassium transport in plants. Physiol Plant 133:651–669CrossRefPubMedGoogle Scholar
  43. Shabala S, Newman IA (2000) Salinity effects on the activity of plasma membrane H+ and Ca2+ transporters in bean leaf mesophyll: masking role of the cell wall. Ann Bot 85:681–686CrossRefGoogle Scholar
  44. Shi H, Lee BH, 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
  45. Stacklies W, Redestig H, Scholz M, Walther D, Selbig J (2007) pcaMethods—a bioconductor package providing PCA methods for incomplete data. Bioinformatics 23:1164–1167CrossRefPubMedGoogle Scholar
  46. Sudhakar C, Lakshmi A, Giridarakumar S (2001) Changes in the antioxidant enzyme efficacy in two high yielding genotypes of mulberry (Morus alba L.) under NaCl salinity. Plant Sci 161:613–619CrossRefGoogle Scholar
  47. 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 (2009a) Calcium mediates root K+/Na+ homeostasis in poplar species differing in salt tolerance. Tree Physiol 29:1175–1186CrossRefPubMedGoogle Scholar
  48. 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 (2009b) NaCl-induced alternations of cellular and tissue ion fluxes in roots of salt-resistant and salt-sensitive poplar species. Plant Physiol 149:1141–1153CrossRefPubMedGoogle Scholar
  49. Sun J, Wang M, Ding M, Deng S, Liu M, Lu C, Zhou X, Shen X, Zheng X, Zhang Z, Song J, Hu Z, Xu Y, Chen S (2010) 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 (doi:  10.1111/j.1365-3040.2010.02118.x)
  50. Taji T, Seki M, Satou M, Sakurai T, Kobayashi M, Ishiyama K, Narusaka Y, Narusaka M, Zhu J-K, Shinozaki K (2004) Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiol 135:1697–1709CrossRefPubMedGoogle Scholar
  51. Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527CrossRefPubMedGoogle Scholar
  52. Tsugane K, Kobayashi K, Niwa Y, Ohba Y, Wada K, Kobayashi H (1999) A recessive Arabidopsis mutant that grows photoautotrophically under salt stress shows enhanced active oxygen detoxification. Plant Cell 11:1195–1206CrossRefPubMedGoogle Scholar
  53. Wang R, Chen S, Ma H, Liu L, Li H, Weng H, Hao Z, Yang S (2006) Genotypic differences in anti-oxidative stress and salt tolerance of three poplars under saline conditions. Front For China 1:82–88CrossRefGoogle Scholar
  54. Wang R, Chen S, Deng L, Fritz E, Hüttermann A, Polle A (2007) Leaf photosynthesis, fluorescence response to salinity and the relevance to chloroplast salt compartmentation and anti-oxidative stress in two poplars. Trees 21:581–591CrossRefGoogle Scholar
  55. Wang R, Chen S, Zhou X, Shen X, Deng L, Zhu H, Shao J, Shi Y, Dai S, Fritz E, Hüttermann A, Polle A (2008) Ionic homeostasis and reactive oxygen species control in leaves and xylem sap of two poplars subjected to NaCl stress. Tree Physiol 28:947–957PubMedGoogle Scholar
  56. Ward JM, Hirschi KD, Sze H (2003) Plants pass the salt. Trends Plant Sci 8:200–201CrossRefPubMedGoogle Scholar
  57. Wong CE, Li Y, Labbe A, Guevara D, Nuin P, Whitty B, Diaz C, Golding GB, Gray GR, Weretilnyk EA, Griffith M, Moffatt BA (2006) Transcriptional profiling implicates novel interactions between abiotic stress and hormonal responses in Thellungiella, a close relative of Arabidopsis. Plant Physiol 140:1437–1450CrossRefPubMedGoogle Scholar
  58. Wu Y, Ding N, Zhao X, 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
  59. Xiong L, Zhu JK (2002) Molecular and genetic aspects of plant responses to osmotic stress. Plant Cell Environ 25:131–139CrossRefPubMedGoogle Scholar
  60. Xiong L, Schumaker KS, Zhu J-K (2002) Cell Signaling during cold, drought, and salt stress. Plant Cell 14:S165–S183CrossRefPubMedGoogle Scholar
  61. Yang Y, Zhang F, Zhao M, An L, Zhang L, Chen N (2007) Properties of plasma membrane H+-ATPase in salt-treated Populus euphratica callus. Plant Cell Rep 26:229–235CrossRefPubMedGoogle Scholar
  62. Zhang HX, Blumwald E (2001) Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nat Biotechnol 19:765–768CrossRefPubMedGoogle Scholar
  63. Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71CrossRefPubMedGoogle Scholar
  64. Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:1–5CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Mingquan Ding
    • 1
  • Peichen Hou
    • 1
  • Xin Shen
    • 1
  • Meijuan Wang
    • 1
  • Shurong Deng
    • 1
  • Jian Sun
    • 1
  • Fei Xiao
    • 1
  • Ruigang Wang
    • 1
  • Xiaoyang Zhou
    • 1
  • Cunfu Lu
    • 1
  • Deqiang Zhang
    • 1
  • Xiaojiang Zheng
    • 2
  • Zanmin Hu
    • 3
  • Shaoliang Chen
    • 1
    • 2
  1. 1.College of Biological Sciences and Technology, National Engineering Laboratory for Tree BreedingBeijing Forestry UniversityBeijingPeople’s Republic of China
  2. 2.Key Laboratory of Biological Resources Protection and Utilization in Hubei ProvinceHubei University for NationalitiesEnshiPeople’s Republic of China
  3. 3.Institute of Genetics and Developmental BiologyChinese Academy of SciencesBeijingPeople’s Republic of China

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