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.
Similar content being viewed by others
References
Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285:1256–1258
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: 960–968
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: 1342–1353
Gale MD, Devos KM (1998) Comparative genetics in the grasses. Proc Natl Acad Sci USA 95:1971–1974
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 98:11444–11449
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 85:10–16
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 12:133–142
Hölmstrom KO, Mantyla E, Welin B, Mandal A, Palva ET (1996) Drought tolerance in tobacco. Nature 379:683–684
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 34:125–134
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 29:649–659
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 220:395–402
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 34:493–495
Katsuhara M, Akiyama Y, Koshio K, Shibasaka M, Kasamo K (2002) Functional analysis of water channels in barley roots. Plant Cell Physiol 43:885–893
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 13:889–905
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 108:1387–1394
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 531:157–161
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 8:276–287
Muramoto Y, Watanabe A, Nakamura T, Takabe T (1999) Enhanced expression of a nuclease gene in leaves of barley plants under salt stress. Gene 234:315–321
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 167:63–70
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 167:1009–1016
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 19:2515–2524
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 30:83–94
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 48:551–573
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 31:279–292
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 115:1211–1219
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 21:81–85
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 135:1697–1709
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 115–131
Ueda A, Shi W, Sanmiya K, Shono M, Takabe T (2001) Functional analysis of salt-inducible proline transporter of barley roots. Plant Cell Physiol 42:1282–1289
Ueda A, Shi W, Nakamura T, Takabe T (2002) Analysis of salt-inducible genes in barley roots by differential display. J Plant Res 115:119–130
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 55:2213–2218
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 3:306–318
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by E. Guiderdoni
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Ueda, A., Kathiresan, A., Bennett, J. et al. Comparative transcriptome analyses of barley and rice under salt stress. Theor Appl Genet 112, 1286–1294 (2006). https://doi.org/10.1007/s00122-006-0231-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-006-0231-4