Advertisement

Theoretical and Applied Genetics

, Volume 112, Issue 7, pp 1286–1294 | Cite as

Comparative transcriptome analyses of barley and rice under salt stress

  • Akihiro Ueda
  • Arumugam Kathiresan
  • John Bennett
  • Tetsuko TakabeEmail author
Original Paper

Abstract

Although barley and rice belong to the same family Poaceae, they differ in their ability to tolerate salt stress. In an attempt to understand the molecular bases of such differences, we compared changes in transcriptome between barley and rice in response to salt stress using barley cDNA microarrays. At 1 and 24 h after salt stress, many genes were up-regulated in barley, but not in rice. Leaf water potential declined in the first 10 h of stress in both species, but recovered in the period 24–48 h only in barley. In addition, we found that barley partitioned Na+ to the roots and away from the shoots more efficiently than rice. These differences in physiological responses were correlated with the differences in the steady-state abundance of transcripts for the genes related to adaptive functions. Transcripts for plasma membrane protein 3 and inorganic pyrophosphatase were up-regulated in both species, but only transiently in rice. This indicates that adaptive mechanisms for regulating ion homeostasis are partly conserved in the two species, but it seems that rice cannot sustain cellular ion homeostasis for a long time like barley. These results imply that genetic modification of regulatory controls of early salt-responsive genes might lead to development of the salt tolerance trait in rice.

Keywords

Salt Stress Salt Tolerance Leaf Water Potential Rice Root Glycinebetaine 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

This research was supported by a Grant “Research for future” to T.T. and Research Fellowship of JSPS for Young Scientists to A.U. We thank Dr. A.T. Jagendorf (Cornell University) for valuable suggestions on the manuscript. We are grateful to Dr. H. Koiwa (Texas A&M Univ.) for allowing to do a part of experiments.

Supplementary material

122_2006_231_MOESM1_ESM.xls (45 kb)
Supplementary material

References

  1. 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
  2. Close TJ, Wanamaker SI, Caldo RA, Turner SM, Ashlock DA, Dickerson JA, Wing RA, Muehlbauer GJ, Kleinhofs A, Wise RP (2004) A new resource for cereal genomics: 22K barley GeneChip comes of age. Plant Physiol 134: 960–968CrossRefPubMedGoogle Scholar
  3. Dubcovsky J, Ramakrishna W, SanMiguel PJ, Busso CS, Yan L, Shiloff BA, Bennetzen JL (2001) Comparative sequence analysis of collinear barley and rice bacterial artificial chromosomes. Plant Physiol 125: 1342–1353CrossRefPubMedGoogle Scholar
  4. Gale MD, Devos KM (1998) Comparative genetics in the grasses. Proc Natl Acad Sci USA 95:1971–1974CrossRefPubMedGoogle Scholar
  5. Gaxiola RA, Li J, Undurraga S, Dang LM, Allen GJ, Alper SL, Fink GR (2001) Drought- and salt-tolerant plants result from overexpression of the AVP1 H+-pump. Proc Natl Acad Sci USA 98:11444–11449PubMedCrossRefGoogle Scholar
  6. Glenn EP, Brown JJ (1998) Effects of soil salt levels on the growth and water use efficiency of Atriplex canescens (Chenopodiaceae) varieties in drying soil. Am J Bot 85:10–16CrossRefGoogle Scholar
  7. Hayashi H, Alia, Mustardy L, Deshnium P, Ida M, Murata N (1997) Transformation of Arabidopsis thaliana with the codA gene for choline oxidase; accumulation of glycinebetaine and enhanced tolerance to salt and cold stress. Plant J 12:133–142PubMedCrossRefGoogle Scholar
  8. Hölmstrom KO, Mantyla E, Welin B, Mandal A, Palva ET (1996) Drought tolerance in tobacco. Nature 379:683–684CrossRefGoogle Scholar
  9. Horvath DP, Schaffer R, West M, Wisman E (2003) Arabidopsis microarrays identify conserved and differentially expressed genes involved in shoot growth and development from distantly related plant species. Plant J 34:125–134PubMedCrossRefGoogle Scholar
  10. Huh GH, Damsz B, Matsumoto TK, Reddy MP, Rus AM, Ibeas JI, Narasimhan ML, Bressan RA, Hasegawa PM (2002) Salt causes ion disequilibrium-induced programmed cell death in yeast and plants. Plant J 29:649–659CrossRefPubMedGoogle Scholar
  11. Inada M, Ueda A, Shi W, Takabe T (2005) A stress-inducible plasma membrane protein 3 (AcPMP3) in a monocotyledonous halophyte, Aneurolepidium chinense, regulates cellular Na+ and K+ accumulation under salt stress. Planta 220:395–402CrossRefPubMedGoogle Scholar
  12. Ishitani M, Arakawa K, Mizuno K, Takabe T (1993) Betaine aldehyde dehydrogenase in the Gramineae: levels in leaves of both betaine-accumulating and non-accumulating cereal plants. Plant Cell Physiol 34:493–495Google Scholar
  13. Katsuhara M, Akiyama Y, Koshio K, Shibasaka M, Kasamo K (2002) Functional analysis of water channels in barley roots. Plant Cell Physiol 43:885–893PubMedCrossRefGoogle Scholar
  14. Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai K, Galbraith D, Bohnert HJ (2001) Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13:889–905CrossRefPubMedGoogle Scholar
  15. Kishor P, Hong Z, Miao GH, Hu C, Verma D (1995) Overexpression of [delta]-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol 108:1387–1394PubMedGoogle Scholar
  16. Maser P, Eckelman B, Vaidyanathan R, Horie T, Fairbairn DJ, Kubo M, Yamagami M, Yamaguchi K, Nishimura M, Uozumi N, Robertson W, Sussman MR, Schroeder JI (2002) Altered shoot/root Na+ distribution and bifurcating salt sensitivity in Arabidopsis by genetic disruption of the Na+ transporter AtHKT1. FEBS Lett 531:157–161CrossRefPubMedGoogle Scholar
  17. Moradi F, Ismail AM, Gregorio G, Egdane J (2003) Salinity tolerance of rice during reproductive development and association with tolerance at seedling stage. Indian J Plant Physiol 8:276–287Google Scholar
  18. Muramoto Y, Watanabe A, Nakamura T, Takabe T (1999) Enhanced expression of a nuclease gene in leaves of barley plants under salt stress. Gene 234:315–321CrossRefPubMedGoogle Scholar
  19. Nakamura T, Muramoto Y, Yokota S, Ueda A, Takabe T (2004) Structural and transcriptional characterization of a salt-responsive gene encoding ATP-dependent RNA helicase in barley. Plant Sci 167:63–70CrossRefGoogle Scholar
  20. Narita Y, Taguchi H, Nakamura T, Ueda A, Shi W, Takabe T (2004) Characterization of the salt-inducible methionine synthase from barley leaves. Plant Sci 167:1009–1016CrossRefGoogle Scholar
  21. Navarre C, Goffeau A (2000) Membrane hyperpolarization and salt sensitivity induced by deletion of PMP3, a highly conserved small protein of yeast plasma membrane. EMBO J 19:2515–2524CrossRefPubMedGoogle Scholar
  22. Negishi T, Nakanishi H, Yazaki J, Kishimoto N, Fujii F, Shimbo K, Yamamoto K, Sakata K, Sasaki T, Kikuchi S, Mori S, Nishizawa NK (2002) cDNA microarray analysis of gene expression during Fe-deficiency stress in barley suggests that polar transport of vesicles is implicated in phytosiderophore secretion in Fe-deficient barley roots. Plant J 30:83–94PubMedCrossRefGoogle Scholar
  23. Ozturk ZN, Talamé V, Deyholos M, Michalowski CB, Galbraith DW, Gozukirmizi N, Tuberosa R, Bohnert HJ (2002) Monitoring large-scale changes in transcript abundance in drought- and salt-stressed barley. Plant Mol Biol 48:551–573PubMedCrossRefGoogle Scholar
  24. Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292CrossRefPubMedGoogle Scholar
  25. Sheveleva E, Chmara W, Bohnert HJ, Jensen RG (1997) Increased salt and drought tolerance by D-ononitol production in transgenic Nicotiana tabacum L. Plant Physiol 115:1211–1219PubMedGoogle Scholar
  26. Shi H, Lee BH, Wu SJ, Zhu JK (2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nature Biotech 21:81–85CrossRefGoogle Scholar
  27. Taji T, Seki M, Satou M, Sakurai T, Kobayashi M, Ishiyama K, Narusaka Y, Narusaka M, Zhu JK, 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
  28. Takabe T, Nakamura T, Nomura M, Hayashi Y, Ishitani M, Muramoto Y, Tanaka A, Takabe T (1998) Glycinebetaine and the genetic engineering of salinity tolerance in plants. In: Satoh K, Murata N (eds) Stress reponses of photosynthesis organisms, Elsevier, Amsterdam, pp 115–131Google Scholar
  29. Ueda A, Shi W, Sanmiya K, Shono M, Takabe T (2001) Functional analysis of salt-inducible proline transporter of barley roots. Plant Cell Physiol 42:1282–1289PubMedCrossRefGoogle Scholar
  30. Ueda A, Shi W, Nakamura T, Takabe T (2002) Analysis of salt-inducible genes in barley roots by differential display. J Plant Res 115:119–130CrossRefPubMedGoogle Scholar
  31. Ueda A, Kathiresan A, Inada M, Narita Y, Nakamura T, Shi W, Takabe T, Bennett J (2004) Osmotic stress in barley regulates expression of a different set of genes than salt stress. J Exp Bot 55:2213–2218PubMedCrossRefGoogle Scholar
  32. Van Zyl L, Von Arnold S, Bozhkov P, Chen Y, Egertsdotter U, MacKay J, Sederoff R, Shen J, Zelena L, Clapham D (2002) Heterologous array analysis in Pinaceae: hybridization of high density arrays of Pinus taeda cDNA with cDNA from needles and embryogenic cultures of P. taeda, P. sylvestris, or Picea abies. Comp Funct Genome 3:306–318CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Akihiro Ueda
    • 1
  • Arumugam Kathiresan
    • 2
  • John Bennett
    • 2
  • Tetsuko Takabe
    • 1
    Email author
  1. 1.Graduate School of Bioagricultural SciencesNagoya UniversityChikusa, NagoyaJapan
  2. 2.Division of Plant Breeding, Genetics and BiochemistryInternational Rice Research InstituteMetro ManilaPhilippines

Personalised recommendations