biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 60:269-278, 2016 | DOI: 10.1007/s10535-016-0586-6

Characterization of S-adenosylmethionine synthetases in soybean under flooding and drought stresses

X. Wang1,2, M. W. Oh1,2, S. Komatsu1,2,*
1 Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Japan
2 National Institute of Crop Science, National Agriculture and Food Research Organization, Tsukuba, Japan

Soybean is stress-sensitive crop that exhibits markedly reduced growth under flooding and drought conditions. Three S-adenosylmethionine synthetases (SAMs) proteins were identified as flooding and drought responsive proteins in soybean using a proteomic technique. To better understand the role of these SAMs proteins in soybean under flooding and drought stresses, temporal, organ, and stress specificities were examined at mRNA and enzyme activity levels. The activity of SAMs decreased in response to the flooding, however, it was not significantly changed by NaCl, cold, gibberellic acid, and calcium in soybean roots. The activity of SAMs was induced in roots and hypocotyls under drought. The mRNA expression of the S-adenosylmethionine synthetase (SAMs) family was down-regulated in root tips and roots under the flooding and the drought, and SAMs 1 and SAMs 2 were down-regulated in roots under both stresses. A gene 1-aminocyclopropane-1-carboxylate synthase was up-regulated in root tips, roots, and hypocotyls under drought, however, it was not changed in root tips and roots under the flooding. In addition, 1-aminocyclopropane-1-carboxylate oxidase was induced in root tips under flooding and drought. These results suggest that SAMs was involved in the response to the flooding and drought and it might affect ethylene biosynthesis in soybean.

Keywords: 1-aminocyclopropane-1-carboxylate synthase; 1-aminocyclopropane-1-carboxylate oxidase
Subjects: S-adenosylmethionine synthetase; flooding; drought; amino acid sequence; phylogenetic analysis; soybean

Received: March 26, 2015; Revised: September 29, 2015; Accepted: October 5, 2015; Published: June 1, 2016  Show citation

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Wang, X., Oh, M.W., & Komatsu, S. (2016). Characterization of S-adenosylmethionine synthetases in soybean under flooding and drought stresses. Biologia plantarum60(2), 269-278. doi: 10.1007/s10535-016-0586-6
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References

  1. Abeles, F.B., Morgan, P.W., Saltveit, M.E., Jr.: Ethylene in Plant Biology. - Academic Press. New York 1992.
  2. Alam, I., Sharmin, S.A., Kim, K.H., Yang, J.K., Choi, M.S., Lee, B.H.: Proteome analysis of soybean roots subjected to short-term drought stress. - Plant Soil 333: 491-505, 2010. Go to original source...
  3. Arimura, G., Ozawa, R., Nishioka, T., Boland, W., Koch, T., Kuhnemann, F., Takabayashi, J.: Herbivore-induced volatiles induce the emission of ethylene in neighboring lima bean plants. - Plant J. 29: 87-98, 2002. Go to original source...
  4. Bairoch, A.: The PROSITE dictionary of sites and patterns in proteins, its current status. - Nucl. Acids Res. 21: 3097-3103, 1993. Go to original source...
  5. Bleecker, A.B., Kende, H.: Ethylene: a gaseous signal molecule in plants. - Annu. Rev. cell. dev. Biol. 16: 1-18, 2000. Go to original source...
  6. Bradford, M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. - Anal. Biochem. 72: 248-254, 1976. Go to original source...
  7. Chang, S., Puryear, J.D., Dias, D.L., Funkhouser, E.A., Newton, R.J., Cairney, J.: Gene expression under water deficit in loblolly pine (Pinus taeda): isolation and characterization of cDNA clones. - Physiol. Plant. 97: 139-148, 1996. Go to original source...
  8. Chevenet, F., Brun, C., Banuls, A.-L., Jacq, B., Chisten, R.: TreeDyn: towards dynamic graphics and annotations for analyses of trees. - BMC Bioinformatics 7: 439, 2006. Go to original source...
  9. Cui, S., Huang, F., Wang, J., Ma, X., Cheng, Y., Liu, J.: A proteomic analysis of cold stress responses in rice seedlings. - Proteomics 5: 3162-3172, 2005. Go to original source...
  10. Espartero, J., Pintor-Toro, J.A., Pardo, J.M.: Differential accumulation of S-adenosylmethionine synthetase transcripts in response to salt stress. - Plant mol. Biol. 25: 217-227. 1994. Go to original source...
  11. Evans, J.M., Malmberg, R.L.: Do polyamines have roles in plant development? - Annu. Rev. Plant Physiol. Plant mol. Biol. 40: 235-269, 1989. Go to original source...
  12. Fan, R., Wang, H., Wang, Y., Yu, D.: Proteomic analysis of soybean defense response induced by cotton worm (Prodenia litura Fabricius) feeding. - Proteome Sci. 10: 16, 2012. Go to original source...
  13. Frederick, J.R., Camp, C.R., Bauer, P.J.: Drought-stress effects on branch and mainstem seed yield and yield components of determinate soybean. - Crop Sci. 41: 759-763, 2001. Go to original source...
  14. Fukuda, T., Saito, A., Wasaki, J., Shinano, T., Osaki, M.: Metabolic alterations proposed by proteome in rice roots grown under low P and high Al concentration under pH. - Plant Sci. 172: 1157-1165, 2007. Go to original source...
  15. Githiri, S.M., Watanabe, S., Harada, K., Takahashi, R.: QTL analysis of flooding tolerance in soybean at an early vegetative growth stage. - Plant Breed. 8: 2058-2069, 2006. Go to original source...
  16. Guo, Z., Tan, J., Zhuo, C., Wang, C., Xiang, B., Wang, Z.: Abscisic acid, H2O2 and nitric oxide interactions mediated cold-induced S-adenosylmethionine synthetase in Medicago sativa subsp. falcata that confers cold tolerance through up-regulating polyamine oxidation. - Plant Biotechnol. J. 12: 601-612, 2014. Go to original source...
  17. Hashiguchi, A., Sakata, K., Komatsu, S.: Proteome analysis of early-stage soybean seedlings under flooding stress. - J. Proteome Res. 8: 2058-2069, 2009. Go to original source...
  18. Kausar, R., Hossain, Z., Makino, T., Komatsu, S.: Characterization of ascorbate peroxidase in soybean under flooding and drought stresses. - Mol. Biol. Rep. 39: 10573-10579, 2012. Go to original source...
  19. Kende, H.: Ethylene biosynthesis. - Annu. Rev. Plant Physiol. Plant mol. Biol. 44: 283-307, 1993. Go to original source...
  20. Khatoon, A., Rehman, S., Hiraga, S., Makino, T., Komatsu, S.: Organ-specific proteomics analysis for response mechanism in soybean seedlings under flooding stress. - J. Proteomics 75: 5706-5723, 2012. Go to original source...
  21. Khan, M.N., Sakata, K., Hiraga, S., Komatsu, S.: Quantitative proteomics reveals that peroxidases play key roles in post-flooding recovery in soybean roots. - J. Proteome Res. 13: 5812-5828, 2014. Go to original source...
  22. Kim, H.J., Balcezak, T.J., Nathin, S.J., McMullen, H.F., Hansen, D.E.: The use of a spectrometric assay to study the interaction of S-adenosylmethionine synthetase with methionine analogues. - Anal. Biochem. 207: 68-72, 1992. Go to original source...
  23. Kim, J.Y.: Identification and functional analysis of S-adenosylmethionine synthetase (HvSAMS) genes in early maturing barley (Hordeum vulgare subsp. vulgare). - Plant Breed. Biotechnol. 1: 178-195, 2013. Go to original source...
  24. Kim, S.H., Kim, S.H., Palaniyandi, S.A., Yang, S.H., Suh, J.W.: Expression of potato S-adenosyl-L-methionine synthase (SbSAMS) gene altered developmental characteristics and stress responses in transgenic Arabidopsis plants. - Plant Physiol. Biochem. 87: 84-91, 2015. Go to original source...
  25. Komatsu, S., Yamamoto, R., Nanjo, Y., Mikami, Y., Yunokawa, H., Sakata, K.: A comprehensive analysis of the soybean genes and proteins expressed under flooding stress using transcriptome and proteome techniques. - J. Proteome Res. 8: 4766-4778, 2009. Go to original source...
  26. Korte, L.L., Williams, J.H., Specht, J.E., Sorense, R.C.: Irrigation of soybean genotypes during reproductive ontogeny. I. Agronomic responses. - Crop Sci. 23: 521-527, 1983. Go to original source...
  27. Lamblin, F., Saladin, G., Dehorter, B., Cronier, D., Grenier, E., Lacoux, J., Bruyant, P., Laine, E., Chabbert, B., Girault, F., Monties, B., Morvan, C., David, H., David, A.: Overexpression of a heterologous sam gene encoding S-adenosylmethionine synthetase in flax (Linum usitatissimum) cells: consequences on methylation of lignin precursors and pectins. - Physiol. Plant. 112: 223-232, 2001. Go to original source...
  28. Li, X.D., Xia, B., Wang, R., Xu, S., Jiang, Y.M., Yu, F.B., Peng F.: Molecular cloning and characterization of S-adenosylmethionine synthetase gene from Lycoris radiata. - Mol. Biol. Rep. 40: 1255-1263, 2013. Go to original source...
  29. Lim, C.C., Liu, J.Z., Pua, E.C.: Characterization of S-adenosylmethionine synthetase genes and its expression is associated with ethylene synthesis in mustard (Brassica juncea). - Physiol. Plant. 116: 522-530, 2002. Go to original source...
  30. Lindroth, A.M., Saarikoski, P., Flygh, G., Clapham, D., Gronroos, R., Thelander, M., Ronne, H., Von Arnold, S.: Two S-adenosylmethionine synthetase-encoding genes differentially expressed using adventitious root development in Pinus contorta. - Plant mol. Biol. 46: 335-346, 2001. Go to original source...
  31. Liu, F., Jensen, C.R., Andersen, M.N.: Drought stress effect on carbohydrate concentration in soybean leaves and pods during early reproductive development: its implication in altering pod set. - Field Crops Res. 86: 1-13, 2004. Go to original source...
  32. Liu, K.: Food use of whole soybeans. - In: Johnson, L.A., White, P.J., Galloway, R., (ed.): Soybeans: Chemistry, Production, Processing, and Utilization. Pp. 441-482. American Oil Chemists' Society. Urbana 2008. Go to original source...
  33. Livak, K.J., Schmittgen, T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2-Delta Delta C(T) method. - Methods 25: 402-408, 2001. Go to original source...
  34. Mayne, M.B., Coleman, J.R., Blumwald, E.: Differential expression during drought conditioning of a root-specific S-adenosylmethionine synthetase from jack pine (Pinus banksiana Lamb.) seedlings. - Plant Cell Environ. 19: 958-966, 1996. Go to original source...
  35. Miao, S., Shi, H., Jin, J., Liu, J., Liu, X., Wang, G.: Effects of short-term drought and flooding on soybean nodulation and yield at key nodulation stage under pot culture. - J. Food Agr. Environ. 10: 819-824, 2012.
  36. Mohammadi, P.P., Moieni, A., Hiraga, S., Komatsu, S.: Organ-specific proteomic analysis of drought-stressed soybean seedlings. - J. Proteomics 75: 1906-1923, 2012. Go to original source...
  37. Nanjo, Y., Skultety, L., Asraf, Y., Komatsu, S.: Comparative proteomic analysis of early-stage soybean seedlings responses to flooding by using gel and gel-free techniques. - J. Proteome Res. 9: 3989-4002, 2010. Go to original source...
  38. Oh, M.W., Komatsu, S.: Characterization of proteins in soybean roots under flooding and drought stresses. - J. Proteomics 114: 161-181, 2015. Go to original source...
  39. Peleman, J., Saito, K., Cottyn, B., Engler, G., Seurinck, J., Van Montagu, M., Inze, D.: Structure and expression analyses of the S-adenosylmethionine synthetase gene family in Arabidopsis thaliana. - Gene 84: 359-369, 1989a. Go to original source...
  40. Peleman, J., Boerjan, W., Engler, G., Seurinck, J., Botterman, J., Alliotte, T., Van Montagu, M., Inze, D.: Strong cellular preference in the expression of a housekeeping gene of Arabidopsis thaliana encoding S-adenosylmethionine synthetase. - Plant Cell 1: 81-93, 1989b. Go to original source...
  41. Pulla, P.K., Kim, Y.J., Parvin, S., Shim, J.S., Lee, J.H., Kim, Y.J., In, J.G., Senthil, K.S., Yang, D.C.: Isolation of S-adenosyl-L-methionine synthetase gene from Panax ginseng C. A. Meyer and analysis of its response to abiotic stresses. - Physiol. mol. Biol. Plants 15: 267-275, 2009. Go to original source...
  42. Ribas-Carbo, M., Taylor, N.L., Giles, L., Busquets, S., Finnegan, P.M., Day, D.A., Lamber, H., Medrano, H., Berry, J.A., Flexas, J.: Effects of water stress on respiration in soybean leaves. - Plant Physiol. 139: 466-473, 2005. Go to original source...
  43. Roeder, S., Dreschler, K., Wirtz, M., Cristescu, S.M., Van Harren, F.J., Hell, R., Piechulla, B.: SAM levels, gene expression of SAM synthetase, methionine synthase and ACC oxidase, and ethylene emission from N. suaveolens flowers. - Plant mol. Biol. 70: 535-546, 2009. Go to original source...
  44. Rozen, S., Skaletsky, H.J.: Primer3 on the www for general users and for biologist programmers. - In: Misener, S., Krawetz, S.A. (ed.): Bioinformatics Methods and Protocols. Pp. 365-386. Humana Press, Towata 2000. Go to original source...
  45. Russell, D.A., Wong, D.M., Sachs, M.M.: The anaerobic response of soybean. - Plant Physiol. 92: 401-407, 1990. Go to original source...
  46. Sallam, A., Scott, H.D.: Effects of prolonged flooding on soybean at the R2 growth stage I. Dry matter and N and P accumulation. - J. Plant Nutr. 10: 567-592, 1987. Go to original source...
  47. Sanchez-Aguayo, I., Rodriguez-Galan, J.M., Garcia, R., Torreblanca, J., Pardo, J.M.: Salt stress enhances xylem development and expression of S-adenosyl-L-methionine synthetase in lignifying tissues of tomato plants. - Planta 220: 278-285, 2004. Go to original source...
  48. Schmutz, J., Cannon, S.B., Schlueter, J., Ma, J., Mitros, T., Nelson, W., Hyten, D.L., Song, Q., Thelen, J.J., Cheng, J., Xu, D., Hellsten, U., May, G.D., Yu, Y., Sakurai, T., Umezawa, T., Bhattacharyya, T.U., Sandhu, D., Valliyodan, B., Lindquist, E., Peto, M., Grant, D., Shu, S., Goodstein, D., Barry, K., Futrell-Griggs, M., Abemathy, B., Du, J., Tian, Z., Zhu, L., Gill, N., Joshi, T., Libault, M., Sethuraman, A., Zhang, X.C., Shinozaki, K., Nguyen, H.T., Wing, R.A., Cregan, P., Specht, J., Grimwood, J., Rokhsar, D., Shoemaker, R.C., Jackson, S.A.: Genome sequence of the palaeopolyploid soybean. - Nature 463: 178-183, 2010. Go to original source...
  49. Schroder, G., Eichel, J., Breinig, S., Schroder, J.: Three differentially expressed S-adenosylmethionine synthetases from Catharanthus roseus: molecular and functional characterization. - Plant mol. Biol. 33: 211-222, 1997. Go to original source...
  50. Singh, B., Bohra, A., Mishra, S., Joshi, R., Pandey, S.: Embracing new-generation 'omics' tools to improve drought tolerance in cereal and food-legume crops. - Biol. Plant. 59: 413-428, 2015. Go to original source...
  51. Sung, F.J.M.: Waterlogging effects on nodule nitrogenase and leaf nitrate reductase activities in soybean. - Field Crops Res. 35: 183-189, 1993. Go to original source...
  52. Tabor, C.W., Tabor, H.: Methionine adenosyltransferase (S-adenosylmethionine synthetase) and S-adenosylmethionine decarboxylase. - Adv. Enzymol. Relat. Areas mol. Biol. 56: 251-282, 1984. Go to original source...
  53. Van Breusegem, F., Dekeyser, R., Giele, J., Van Montagu, M., Caplan, A.: Characterization of a S-adenosylmethionine synthetase gene in rice. - Plant Physiol. 105: 1463-1464, 1994. Go to original source...
  54. Van Doorsselaere, J., Gielen, J., Van Montagu, M., Inzé, D.: A cDNA encoding S-adenosyl-L-methionine synthetase from poplar. - Plant Physiol. 102: 1365-1366, 1993. Go to original source...
  55. Van Toai, T.T., Lee, J.D., Goulart, P.F.P., Shannon, J.G., Alves, J.D., Nguyen, H.T., Yu, O., Rahman, M., Islam, R.: Soybean (Glycine max L. Merr.) seed composition response to soil flooding stress. - J. Food Agr. Environ. 10: 795-801, 2012.
  56. Vriezen, W.H., Hulzink, R., Mariani, C., Voesenek, L.A.C.J.: 1-aminocyclopropane-1-carboxylate oxidase activity limits ethylene biosynthesis in Rumex palustris during submergence. - Plant Physiol. 121: 185-195, 1999. Go to original source...
  57. Wang, K.L.C., Li, H., Ecker, J.R.: Ethylene biosynthesis and signaling networks. - Plant Cell 14: S131-S151, 2002. Go to original source...
  58. Witzel, K., Weinder, A., Surabhi, G.-K., Borner, A., Mock, H.-P.: Salt stress-induced alterations in the root proteome of barley genotypes with contrasting response towards salinity. - J. exp. Bot. 60: 3545-3557, 2009. Go to original source...
  59. Yang, S.F., Hoffman, N.E.: Ethylene biosynthesis and its regulation in higher plants. - Annu. Rev. Plant Physiol. 35: 155-189, 1984. Go to original source...