Plant Molecular Biology

, Volume 68, Issue 1–2, pp 119–129 | Cite as

Transcriptional and physiological study of the response of Burma mangrove (Bruguiera gymnorhiza) to salt and osmotic stress

  • Masashi Miyama
  • Yuichi TadaEmail author


We investigated the transcriptional response of Burma mangrove (Bruguiera gymnorhiza) to high salinity (salt stress; 500 mM NaCl) and hyperosmotic stress (osmotic stress; 1 M sorbitol) by microarray analysis. ANOVA (P < 0.05) and significant analysis of microarray (SAM; FDR < 5%) revealed that 865 of 11,997 genes showed significant differential expression under salt and osmotic stress. Scatter plot analysis revealed that the expression level of genes changed at 6 h after salt stress treatment, but recovered at 24 h, while the change at 6 h after osmotic stress treatment diverged at 24 h. Hierarchical clustering of the 865 genes showed that expression profiles under salt stress were distinctly different from those under osmotic stress. Comparison of gene ontology (GO) categories of differentially expressed genes under the stress conditions revealed that the adaptation of Burma mangrove to salt stress was accompanied by the up-regulation of genes categorized for “cell communication,” “signal transduction,” “lipid metabolic process,” “photosynthesis,” “multicellular organismal development,” and “transport,” and by down-regulation of genes categorized for “catabolic process.” Burma mangrove maintained its leaf water potential and recovered from its photosynthesis rate that declined temporarily under salt stress, but not under osmotic stress. These results demonstrated a fundamental difference between the response to salt and osmotic stress. Ion and sugar content analysis suggested that salt tolerance of Burma mangrove might be attributed to their ability to accumulate high concentrations of Na+ and Cl, even under non-stressed conditions; to uptake additional Na+ and Cl for use as osmolytes; and to maintain K+ homeostasis under salt stress.


Burma mangrove Gene ontology analysis Microarray Osmotic stress Salt tolerance Transcriptional response 



Analysis of variance


Expressed sequence tag


False discovery rate


Gene ontology


Significant analysis of microarray



We thank Noriko Someya for her excellent technical assistance. This work was supported by MEXT (the Ministry of Education, Culture, Sports, Science and Technology of Japan), “University-Industry Joint Research” Project 2003–2007.

Supplementary material

11103_2008_9356_MOESM1_ESM.xls (52.5 mb)
(XLS 53788 kb)


  1. Abebe T, Guenzi AC, Martin B, Cushman JC (2003) Tolerance of mannitol-accumulating transgenic wheat to water stress and salinity. Plant Physiol 131:1748–1755PubMedCrossRefGoogle Scholar
  2. Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285:1256–1258PubMedCrossRefGoogle Scholar
  3. Banzai T, Hershkovits G, Katcoff DJ, Hanagata N, Dubinsky Z, Karube I (2002a) Identification and characterization of mRNA transcripts differentially expressed in response to high salinity by means of differential display in the mangrove, Bruguiera gymnorrhiza. Plant Sci 162:499–505CrossRefGoogle Scholar
  4. Banzai T, Sumiya K, Hanagata N, Dubinsky Z, Karube I (2002b) Molecular cloning and characterization of genes encoding BURP domain-containing protein in the mangrove, Bruguiera gymnorrhiza. Trees 16:87–93CrossRefGoogle Scholar
  5. Banzai T, Hanagata N, Dubinsky Z, Karube I (2003) Fructose-2,6-bisphosphate contents were increased in response to salt, water and osmotic stress in leaves of Bruguiera gymnorhiza by differential changes in the activity of the bifunctional enzyme 6-phosphofructo-2-kinase/fructose-2,6-bisphosphate 2-phosphatase. Plant Mol Biol 53:51–59PubMedCrossRefGoogle Scholar
  6. Blumwald E (2000) Sodium transport and salt tolerance in plants. Curr Opin Cell Biol 12:431–434PubMedCrossRefGoogle Scholar
  7. Blumwald E, Aharon GS, Apse MP (2000) Sodium transport in plant cells. Biochim Biophys Acta 1465:140–151PubMedCrossRefGoogle Scholar
  8. Bolstad BM, Irizarry RA, Astrand M, Speed TP (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19:185–193PubMedCrossRefGoogle Scholar
  9. Cheng NH, Pittman JK, Zhu JK, Hirschi KD (2004) The protein kinase SOS2 activates the Arabidopsis H+/Ca2+ antiporter CAX1 to integrate calcium transport and salt tolerance. J Biol Chem 279:2922–2926PubMedCrossRefGoogle Scholar
  10. Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55:225–236PubMedCrossRefGoogle Scholar
  11. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95:14863–14868PubMedCrossRefGoogle Scholar
  12. FAO (2005) Global network on integrated soil management for sustainable use of salt-affected soils, vol 61. FAO Land and Plant Nutrition Management Service, Rome, Italy
  13. Flowers T, Troke PF, Yeo AR (1977) The mechanisms of salt tolerance in halophytes. Ann Rev Plant Physiol 29:89–121CrossRefGoogle Scholar
  14. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499PubMedCrossRefGoogle Scholar
  15. Huber W, von Heydebreck A, Sultmann H, Poustka A, Vingron M (2002) Variance stabilization applied to microarray data calibration and to the quantification of differential expression. Bioinformatics 18(Suppl 1):S96–104PubMedGoogle Scholar
  16. Knight H, Knight MR (2001) Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 6:262–267PubMedCrossRefGoogle Scholar
  17. Liu J, Zhu JK (1998) A calcium sensor homolog required for plant salt tolerance. Science 280:1943–1945PubMedCrossRefGoogle Scholar
  18. Miyama M, Hanagata N (2007a) Microarray analysis of 7029 gene expression patterns in burma mangrove under high-salinity stress. Plant Sci 172:948–957CrossRefGoogle Scholar
  19. Miyama M, Hanagata N (2007b) Microarray gene expression profiling for salt tolerant gene selection. Plant Stress 1:118–122Google Scholar
  20. Miyama M, Shimizu H, Sugiyama M, Hanagata N (2006) Sequencing and analysis of 14,842 expressed sequence tags of burma mangrove, Bruguiera gymnorrhiza. Plant Sci 171:234–241CrossRefGoogle Scholar
  21. Ohta M, Hayashi Y, Nakashima A, Hamada A, Tanaka A, Nakamura T, Hayakawa T (2002) Introduction of a Na+/H+ antiporter gene from Atriplex gmelini confers salt tolerance to rice. FEBS Lett 532:279–282PubMedCrossRefGoogle Scholar
  22. Ottow EA, Brinker M, Teichmann T, Fritz E, Kaiser W, Brosche M, Kangasjarvi J, Jiang X, Polle A (2005) Populus euphratica displays apoplastic sodium accumulation, osmotic adjustment by decreases in calcium and soluble carbohydrates, and develops leaf succulence under salt stress. Plant Physiol 139:1762–1772PubMedCrossRefGoogle Scholar
  23. Park JM, Park CJ, Lee SB, Ham BK, Shin R, Paek KH (2001) Overexpression of the tobacco Tsi1 gene encoding an EREBP/AP2-type transcription factor enhances resistance against pathogen attack and osmotic stress in tobacco. Plant Cell 13:1035–1046PubMedCrossRefGoogle Scholar
  24. Popp M, Larher F, Weigel P (1985) Osmotic adaption in Australian mangroves. Plant Ecol 61:247–253CrossRefGoogle Scholar
  25. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386PubMedGoogle Scholar
  26. 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
  27. Sakamoto A, Murata A, Murata N (1998) Metabolic engineering of rice leading to biosynthesis of glycinebetaine and tolerance to salt and cold. Plant Mol Biol 38:1011–1019PubMedCrossRefGoogle Scholar
  28. 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
  29. Sugihara K, Hanagata N, Dubinsky Z, Baba S, Karube I (2000) Molecular characterization of cDNA encoding oxygen evolving enhancer protein 1 increased by salt treatment in the mangrove Bruguiera gymnorrhiza. Plant Cell Physiol 41:1279–1285PubMedCrossRefGoogle Scholar
  30. Takemura T, Hanagata N, Sugihara K, Baba S, Karube I, Dubinsky Z (2000) Physiological and biochemical responses to salt stresses in the mangrove, Bruguriera gymnorrhiza. Aquat Bot 68:15–28CrossRefGoogle Scholar
  31. Takemura T, Hanagata N, Dubinsky Z, Karube I (2002) Molecular characterization and response to salt stress of mRNAs encoding cytosolic Cu/Zn superoxide dismutase and catalase from Bruguiera gymnorrhiza. Trees 16:94–99CrossRefGoogle Scholar
  32. Troyanskaya O, Cantor M, Sherlock G, Brown P, Hastie T, Tibshirani R, Botstein D, Altman RB (2001) Missing value estimation methods for DNA microarrays. Bioinformatics 17:520–525PubMedCrossRefGoogle Scholar
  33. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98:5116–5121PubMedCrossRefGoogle Scholar
  34. Xu D, Duan X, Wang B, Hong B, Ho T, Wu R (1996) Expression of a late embryogenesis abundant protein gene, hva1, from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol 110:249–257PubMedGoogle Scholar
  35. Yamaguchi T, Blumwald E (2005) Developing salt-tolerant crop plants: challenges and opportunities. Trends Plant Sci 10:615–620PubMedCrossRefGoogle Scholar
  36. Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71PubMedCrossRefGoogle Scholar
  37. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273PubMedCrossRefGoogle Scholar
  38. Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  1. 1.School of Bioscience and BiotechnologyTokyo University of TechnologyHachioji, TokyoJapan
  2. 2.Research Center of Advanced Bionics, Advanced Industrial Science and TechnologyHachiojiJapan

Personalised recommendations