Advertisement

Plant Molecular Biology

, Volume 58, Issue 4, pp 561–574 | Cite as

Expressed sequence tags from the Yukon ecotype of Thellungiella reveal that gene expression in response to cold, drought and salinity shows little overlap

  • C.E. Wong
  • Y. Li
  • B.R. Whitty
  • C. Díaz-Camino
  • S.R. Akhter
  • J.E. Brandle
  • G.B. Golding
  • E.A. Weretilnyk
  • B.A. Moffatt
  • M. Griffith
Article

Abstract

Thellungiella salsuginea (also known as T. halophila) is a close relative of Arabidopsis that is very tolerant of drought, freezing, and salinity and may be an appropriate model to identify the molecular mechanisms underlying abiotic stress tolerance in plants. We produced 6578 ESTs, which represented 3628 unique genes (unigenes), from cDNA libraries of cold-, drought-, and salinity-stressed plants from the Yukon ecotype of Thellungiella. Among the unigenes, 94.1% encoded products that were most similar in amino acid sequence to Arabidopsis and 1.5% had no match with a member of the family Brassicaceae. Unigenes from the cold library were more similar to Arabidopsis sequences than either drought- or salinity-induced sequences, indicating that latter responses may be more divergent between Thellungiella and Arabidopsis. Analysis of gene ontology using the best matched Arabidopsis locus showed that the Thellungiella unigenes represented all biological processes and all cellular components, with the highest number of sequences attributed to the chloroplast and mitochondria. Only 140 of the unigenes were found in all three abiotic stress cDNA libraries. Of these common unigenes, 70% have no known function, which demonstrates that Thellungiella can be a rich resource of genetic information about environmental responses. Some of the ESTs in this collection have low sequence similarity with those in Genbank suggesting that they may encode functions that may contribute to Thellungiella’s high degree of stress tolerance when compared with Arabidopsis. Moreover, Thellungiella is a closer relative of agriculturally important Brassica spp. than Arabidopsis, which may prove valuable in transferring information to crop improvement programs.

Keywords

abiotic stress acclimation Arabidopsis Brassicaceae canola desiccation EST freezing salt tolerance 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Al-Shehbaz, I.A., O’Kane, S.L.,Jr., Price, R.A. 1999Generic placement of species excluded from Arabidopsis (Brassicaceae)Novon9296307Google Scholar
  2. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., Lipman, D.J. 1997Gapped BLAST and PSI-BLAST: a new generation of protein database search programsNucleic Acids Res.2533893402Google Scholar
  3. Audic, S., Claverie, J.M. 1997The significance of digital gene expression profilesGenome Res.7986995Google Scholar
  4. Baranowskij, N., Frohberg, C., Prat, S., Willmitzer, L. 1994A novel DNA binding protein with homology to Myb oncoproteins containing only one repeat can function as a transcriptional activatorEMBO J.1353835392Google Scholar
  5. Berardini, T.Z., Mundodi, S., Reiser, L., Huala, E., Garcia-Hernandez, M., Zhang, P., Mueller, L.A., Yoon, J., Doyle, A., Lander, G., Moseyko, N., Yoo, D., Xu, I., Zoeckler, B., Montoya, M., Miller, N., Weems, D., Rhee, S.Y. 2004Functional annotation of the Arabidopsis genome using controlled vocabulariesPlant Physiol.135745755Google Scholar
  6. Bray, E.A., Bailey-Serres, J., Weretilnyk, E. 2000Responses to abiotic stressGruissem, W.Buchannan, B.Jones, R. eds. Biochemistry and Molecular Biology of PlantsAmerican Society of Plant PhysiologistsRockville, MD11581249Google Scholar
  7. Bressan, R.A., Zhang, C., Zhang, H., Hasegawa, P., Bohnert, H., Zhu, J.K. 2001Learning from the Arabidopsis experience. The next gene search paradigmPlant Physiol.12713541360Google Scholar
  8. Chinnusamy, V., Schumaker, K., Zhu, J.K. 2004Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plantsJ. Exp.Bot.55225236Google Scholar
  9. Cody, W.J. 2000Flora of the Yukon Territory2NRC Research PressOttawa, Canada669Google Scholar
  10. Danyluk, J., Sarhan, F. 1990Differential messenger-RNA transcription during the induction of freezing tolerance in spring and winter wheatPlant Cell Physiol.31609619Google Scholar
  11. Ewing, B., Green, P. 1998Base-calling of automated sequencer traces using phred. II. Error probabilitiesGenome Res.8186194Google Scholar
  12. Ewing, B., Hillier, L., Wendl, M.C., Green, P. 1998Base-calling of automated sequencer traces using phred. I. Accuracy assessmentGenome Res.8175185Google Scholar
  13. Fowler, S., Thomashow, M.F. 2002Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathwayPlant Cell1416751690Google Scholar
  14. Galloway, G.L., Malmberg, R.L., Price, R.A. 1998Phylogenetic utility of the nuclear gene arginine decarboxylase: an example from BrassicaceaeMol. Biol. Evol.1513121320Google Scholar
  15. Hasegawa, P.M., Bressan, R.A., Zhu, J.K., Bohnert, H.J. 2000Plant cellular and molecular responses to high salinityAnnu. Rev. Plant Physiol. Plant Mol. Biol.51463499Google Scholar
  16. Hondred, D., Wadle, D-W., Titus, D.E., Becker, W.M. 1987Light-stimulated accumulation of the proxisomal enzymes hydroxypyruvate reductase and serine:glyoxylate aminotransferase and their translatable mRNAs in cotyledons of cucumber seedlingsPlant Mol. Biol.9259275Google Scholar
  17. Hu, W., Wang, Y., Bowers, C., Ma, H. 2003Isolation, sequence analysis, and expression studies of florally expressed cDNAs in ArabidopsisPlant Mol. Biol.53545563Google Scholar
  18. Huelsenbeck, J.P., Ronquist, F. 2001MRBAYES: Bayesian inference of phylogenetic treesBioinformatics17754755Google Scholar
  19. Huh, G.H., Damez, B., Matsumoto, T.K., Reddy, M.P., Rus, A.M., Ibeas, J.I., Narasimhan, M.L., Bressan, R.A., Hasegawa, P.M. 2002Salt causes ion disequilibrium-induced programmed cell death in yeast and plantsPlant J.29649659Google Scholar
  20. Inan, G., Zhang, Q., Li, P.H., Wang, Z.L., Cao, Z.Y., Zhang, H., Zhang, C.Q., Quist, T.M., Goodwin, S.M., Zhu, J.H., Shi, H.H., Damsz, B., Charbaji, T., Gong, Q.Q., Ma, S.S., Fredricksen, M., Galbraith, D.W., Jenks, M.A., Rhodes, D., Hasegawa, P.M., Bohnert, H.J., Joly, R.J., Bressan, R.A., Zhu, J.K. 2004Salt cress. A halophyte and cryophyte Arabidopsis relative model system and its applicability to molecular genetic analyses of growth and development of extremophilesPlant Physiol.13517181737Google Scholar
  21. Kacperska, A. 2004Sensor types in signal transduction pathways in plant cells responding to abiotic stressors: do they depend on stress intensity?Physiol. Plant.122159168Google Scholar
  22. Kreps, J.A., Wu, Y., Chang, H.S., Zhu, T., Wang, X., Harper, J. 2002Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stressPlant Physiol.13021292141Google Scholar
  23. Mittler, R., Hallak-Herr, E., Orvar, B.L., Camp, W., Willekens, H., Inze, D., Ellis, B. 1999Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyper-responsive to pathogen infectionProc. Natl. Acad. Sci. USA961416514170Google Scholar
  24. Murray, M.G., Peters, D.L., Thompson, W.F. 1981Ancient repeated sequences in the pea and mung bean genomes and implications for genome evolutionJ. Mol. Evol.173142Google Scholar
  25. Orvar, B.L., Ellis, B.E. 1997Transgenic tobacco plants expressing antisense RNA for cytosolic ascorbate peroxidase show increased susceptibility to ozone injuryPlant J.1112971305Google Scholar
  26. Pastori, G.M., Foyer, C.H. 2002Common components, networks, and pathways of cross-tolerance to stress. The central role of “redox” and abscisic acid-mediated controlsPlant Physiol.129460468Google Scholar
  27. Pertea, G., Huang, X., Liang, F., Antonescu, V., Sultana, R., Karamycheva, S., Lee, Y., White, J., Cheung, F., Parvizi, B., Tsai, J., Quackenbush, J. 2003TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST datasetsBioinformatics19651652Google Scholar
  28. Rhee, S.Y., Beavis, W., Berardini, T.Z., Chen, G., Dixon, D., Doyle, A., Garcia-Hernandez, M., Huala, E., Lander, G., Montoya, M., Miller, N., Mueller, L.A., Mundodi, S., Reiser, L., Tacklind, J., Weems, D.C., Wu, Y., Xu, I., Yoo, D., Yoon, J., Zhang, P. 2003The Arabidopsis Information Resource (TAIR): a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and communityNucleic Acids Res.31224228Google Scholar
  29. Roxas, V.P., Lodhi, S.A., Garrett, D.K., Mahan, J.R., Allen, R.D. 2000Stress tolerance in transgenic tobacco seedlings that overexpress glutathione S-transferase/glutathione peroxidasePlant Cell Physiol.4112291234Google Scholar
  30. 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. 2002Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high salinity stresses using a full-length cDNA microarrayPlant J.31279292Google Scholar
  31. Staden, R., Beal, K.F., Bonfield, J.K. 2000The Staden package, 1998Methods Mol. Biol.132115130Google Scholar
  32. Stoop, J.M.H., Wichers, H.J., Mooibroek, H. 1996Mannitol metabolism in salt stressed Agaricus bisporus Acta Bot. Neerl.45572572Google Scholar
  33. Teusink, R.S., Rahman, M., Bressan, R.A., Jenks, M.A. 2002Cuticular waxes on Arabidopsis thaliana close relatives Thellungiella halophila and Thellungiella parvula Internat. J.␣Plant Sci.163309315Google Scholar
  34. Thomas, H., Stoddart, J.L. 1980Leaf senescenceAnnu. Rev. Plant Physiol.3183111Google Scholar
  35. Thomashow, M.F. 1999Plant cold acclimation: freezing tolerance genes and cold acclimationPhysiol. Plant Mol. Biol.50571599Google Scholar
  36. Thompson, J.D., Higgins, D.G., Gibson, T.J. 1994CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choiceNucleic Acids Res.2246734680Google Scholar
  37. Volkov, V., Wang, B., Dominy, P.J., Fricke, W., Amtmann, A. 2004Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana, possesses effective mechanisms to discriminate between potassium and sodiumPlant Cell Environ.27114Google Scholar
  38. Wang, Z.I., Li, P.H., Fredricksen, M., Gong, Z.H., Kim, C.S., Zhang, C.Q., Bohnert, H.J., Zhu, J.K., Bressan, R.A., Hasegawa, P.M., Zhao, Y.X., Zhang, H. 2004Expressed sequence tags from Thellungiella halophila, a new model to study plant salt-tolerancePlant Sci.166609616Google Scholar
  39. Wang, W., Vinocur, B., Altman, A. 2003Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerancePlanta218114Google Scholar
  40. Willekens, H., Chamnongpol, S., Davey, M., Schraudner, M., Langebartels, C., Montagu, M., Inze, D., Camp, W. 1997Catalase is a sink for H2O2 and is indispensable for stress defence in C-3 plantsEMBO J.1648064816Google Scholar
  41. Yan Wang, J., Tissue, D., Holaday, A.S., Allen, R., Zhang, H. 2003Photosynthesis and seed production under water-deficit conditions in transgenic tobacco plants that overexpress an Arabidopsis ascorbate peroxidase geneCrop Sci.4314771483Google Scholar
  42. Zhu, J.K. 2001Plant salt toleranceTrends Plant Sci.66671Google Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • C.E. Wong
    • 1
  • Y. Li
    • 1
  • B.R. Whitty
    • 2
  • C. Díaz-Camino
    • 1
  • S.R. Akhter
    • 1
  • J.E. Brandle
    • 3
  • G.B. Golding
    • 2
  • E.A. Weretilnyk
    • 2
  • B.A. Moffatt
    • 1
  • M. Griffith
    • 1
  1. 1.Department of BiologyUniversity of WaterlooWaterloo ONCanada
  2. 2.Department of BiologyMcMaster UniversityHamilton ONCanada
  3. 3.Agriculture and Agri-Food Canada (AAFC) LondonLondon ONCanada

Personalised recommendations