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Molecular Breeding

, Volume 34, Issue 3, pp 1055–1064 | Cite as

OsMsr9, a novel putative rice F-box containing protein, confers enhanced salt tolerance in transgenic rice and Arabidopsis

  • Guoyun Xu
  • Yanchun Cui
  • Manling Wang
  • Mingjuan Li
  • Xuming Yin
  • Xinjie Xia
Article

Abstract

Salinity is a major environmental stress that limits agricultural production and geographical distribution of plants. In a previous study, it has been shown that OsMsr9 was induced by cold, drought and heat stresses. However, functions of OsMsr9 at physiological and molecular levels are still unknown. Here, we report that OsMsr9 plays roles in salt tolerance in plants. Quantitative real-time PCR (qPCR) analysis revealed that OsMsr9 was also rapidly and strongly induced by salt stress. Overexpression of OsMsr9 in Arabidopsis and rice showed enhanced salt stress tolerance displaying increased shoot and root elongation, higher survival rates in transgenic plants compared with wild type. OsMsr9 might act as a positive regulator of plant salt tolerance with reinforced expression of stress-related genes, such as RD29A, DREB2A and RAB18 in transgenic plants under salt conditions. Furthermore, transgenic plants accumulated more compatible solutes (proline and soluble sugar) and low level of malondialdehyde, alleviating the changes in reactive oxygen species. These results indicate that OsMsr9 could be a useful gene in developing transgenic crops with enhanced salt tolerance.

Keywords

F-box Salt tolerance Overexpression Rice Arabidopsis 

Notes

Acknowledgments

This research was supported by National Natural Science Foundation of China (31171536, 31301253).

Supplementary material

11032_2014_96_MOESM1_ESM.doc (678 kb)
Supplementary material 1 (DOC 678 kb)

References

  1. Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59(2):206–216CrossRefGoogle Scholar
  2. Bai C, Sen P, Hofmann K, Ma L, Goebl M, Harper JW, Elledge SJ (1996) SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell 86:263–274PubMedCrossRefGoogle Scholar
  3. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743PubMedCrossRefGoogle Scholar
  4. Cui YC, Xu GY, Wang ML, Yu Y, Li MJ, Pedro R, Xia XJ (2013) Expression of OsMSR3 in Arabidopsis enhances tolerance to cadmium stress. Plant Cell Tiss Org 113:331–340CrossRefGoogle Scholar
  5. Dill A, Thomas SG, Hu J, Steber CM, Sun TP (2004) The Arabidopsis F-Box protein SLEEPY1 targets gibberellin signaling repressors for gibberellin-induced degradation. Plant Cell 16:1392–1405PubMedCrossRefPubMedCentralGoogle Scholar
  6. Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci USA 99:15898–15903PubMedCrossRefPubMedCentralGoogle Scholar
  7. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198PubMedCrossRefGoogle Scholar
  8. Hmida-Sayari A, Gargouri-Bouzid R, Bidani A, Jaoua L, Savouré A, Jaoua S (2005) Overexpression of Δ1-pyrroline-5-carboxylate synthetase increases proline production and confers salt tolerance in transgenic potato plants. Plant Sci 169:746–752CrossRefGoogle Scholar
  9. Jain M, Nijhawan A, Arora R, Agarwal P, Ray S, Sharma P, Kapoor S, Tyagi AK, Khurana JP (2007) F-Box proteins in rice. Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress. Plant Physiol 143:1467–1483PubMedCrossRefPubMedCentralGoogle Scholar
  10. Kim JB, Kang JY, Kim SY (2004) Over-expression of a transcription factor regulating ABA-responsive gene expression confers multiple stress tolerance. Plant Biotechnol J 2:459–466PubMedCrossRefGoogle Scholar
  11. Kramer GF, Norman HA, Krizek DT, Mirecki RM (1991) Influence of UV-B radiation on polyamines, lipid peroxidation and membrane lipids in cucumber. Phytochemistry 30:2101–2108CrossRefGoogle Scholar
  12. Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406PubMedCrossRefPubMedCentralGoogle Scholar
  13. Liu K, Wang L, Xu Y, Chen N, Ma Q, Li F, Chong K (2007) Overexpression of OsCOIN, a putative cold inducible zinc finger protein, increased tolerance to chilling, salt and drought, and enhanced proline level in rice. Planta 226:1007–1016PubMedCrossRefGoogle Scholar
  14. Lu XD, Song SF, Li LY, Wang ML, Xia XJ (2010) Expression and cloning of a novel stress-responsive gene OsMsr9 in rice. Res Agr Moder 31:228–232Google Scholar
  15. Maldonado-Calderón MT, Sepúlveda-García E, Rocha-Sosa M (2012) Characterization of novel F-box proteins in plants induced by biotic and abiotic stress. Plant Sci 185–186:208–217PubMedCrossRefGoogle Scholar
  16. Msanne J, Lin JS, Stone JM, Awada T (2011) Characterization of abiotic stress-responsive Arabidopsis thaliana RD29A and RD29B genes and evaluation of transgenes. Planta 234:97–107PubMedCrossRefGoogle Scholar
  17. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681PubMedCrossRefGoogle Scholar
  18. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco cultures. Physiol Plant 15:473–497CrossRefGoogle Scholar
  19. Niu CF, Wei W, Zhou QY, Tian AG, Hao YJ, Zhang WK, Ma B, Liu Q, Zhang ZB, Zhang JS, Chen SY (2012) Wheat WRKY genes TaWRKY2 and TaWRKY19 regulate abiotic stress tolerance in transgenic Arabidopsis plants. Plant, Cell Environ 35:1156–1170CrossRefGoogle Scholar
  20. Ruan SL, Ma HS, Wang SH, Fu YP, Xin Y, Liu WZ, Wang F, Tong JX, Wang SZ, Chen HZ (2011) Proteomic identification of OsCYP2, a rice cyclophilin that confers salt tolerance in rice (Oryza sativa L.) seedlings when overexpressed. BMC Plant Biol 11:34PubMedCrossRefPubMedCentralGoogle Scholar
  21. Sakamoto H, Maruyama K, Sakuma Y, Meshi T, Iwabuchi M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions. Plant Physiol 136:2734–2746PubMedCrossRefPubMedCentralGoogle Scholar
  22. Schwager KM, Calderon-Villalobos LIA, Dohmann EMN, Willige BC, Knierer S, Nill C, Schwechheimer C (2007) Characterization of the VIER F-BOX PROTEINE genes from Arabidopsis reveals their importance for plant growth and development. Plant Cell 19:1163–1178PubMedCrossRefPubMedCentralGoogle Scholar
  23. Shinozaki K, Yamaguchi-Shinozaki K (1997) Gene expression and signal transduction in water-stress response. Plant Physiol 115:327–334PubMedCrossRefPubMedCentralGoogle Scholar
  24. Song SY, Dai XY, Zhang WH (2012) A rice F-box gene, OsFbx352, is involved in glucose-delayed seed germination in rice. J Exp Bot 63(5):5559–5568PubMedCrossRefPubMedCentralGoogle Scholar
  25. Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97PubMedCrossRefGoogle Scholar
  26. Székely G, Abrahám E, Cséplo A, Rigó G, Zsigmond L, Csiszár J, Ayaydin F, Strizhov N, Jásik J, Schmelzer E, Koncz C, Szabados L (2008) Duplicated P5CS genes of Arabidopsis play distinct oles in stress regulation and developmental control of proline bio-synthesis. Plant J 53:11–28PubMedCrossRefGoogle Scholar
  27. Troll W, Lindsley J (1955) A photometric method for the determination of proline. J Biol Chem 215:655–660PubMedGoogle Scholar
  28. Van den Burg HA, Tsitsigiannis DI, Rowland O, Lo J, Rallapalli G, Maclean D, Takken FL, Jones JD (2008) The F-box protein ACRE189/ACIF1 regulates cell death and defense responses activated during pathogen recognition in tobacco and tomato. Plant Cell 20:697–719PubMedCrossRefPubMedCentralGoogle Scholar
  29. Verslues PE, Kim Y, Zhu J (2007) Altered ABA, proline and hydrogen peroxide in an Arabidopsis glutamate: glyoxylate aminotransferase mutant. Plant Mol Biol 64:205–217PubMedCrossRefGoogle Scholar
  30. Woo HR, Chung KM, Park JH, Oh SA, Ahn T, Hong SH, Jang SK, Nam HG (2001) ORE9, an F-box protein that regulates leaf senescence in Arabidopsis. Plant Cell 13:1779–1790PubMedCrossRefPubMedCentralGoogle Scholar
  31. Xiang Y, Tang N, Du H, Ye H, Xiong L (2008) Characterization of OsbZIP23 as a key player of bZIP transcription factor family for conferring ABA sensitivity and salinity and drought tolerance in rice. Plant Physiol 148:1938–1952PubMedCrossRefPubMedCentralGoogle Scholar
  32. Xiong L, Zhu JK (2002) Molecular and genetic aspects of plant responses to osmotic stress. Plant, Cell Environ 25:131–139CrossRefGoogle Scholar
  33. Xu GX, Ma H, Nei M, Kong HZ (2009) Evolution of F-box genes in plants: different modes of sequence divergence and their relationships with functional diversification. Proc Natl Acad Sci USA 106:835–840PubMedCrossRefPubMedCentralGoogle Scholar
  34. Xu GY, Pedro R, Wang ML, Xu ML, Cui YC, Li LY, Zhu YX, Xia XJ (2011) A novel rice calmodulin-like gene, OsMSR2, confers improved drought, salt tolerance and enhanced ABA sensitivity in Arabidopsis. Planta 234:47–59PubMedCrossRefGoogle Scholar
  35. Xu GY, Cui YC, Li MJ, Wang ML, Yu Y, Zhang B, Huang LF, Xia XJ (2013) OsMSR2, a novel rice calmodulin-like gene, confers enhanced salt tolerance in rice (Oryza sativa L.). Aust J Crop Sci 7(3):368–373Google Scholar
  36. Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6:251–264PubMedCrossRefPubMedCentralGoogle Scholar
  37. Yan YS, Chen XY, Yang K, Sun ZX, Fu YP, Zhang YM, Fang RX (2011) Overexpression of an F-box protein gene reduces abiotic stress tolerance and promotes root growth in rice. Mol Plant 4(1):190–197PubMedCrossRefGoogle Scholar
  38. Yang CW, Deng W, Tang N, Li ZG (2013) Overexpression of ZmAFB2, a maize homologue of AFB2 gene, enhances salt tolerance in transgenic tobacco. Plant Cell Tiss Org 112:171–179CrossRefGoogle Scholar
  39. Yoshiba Y, Nanjo T, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Stress-responsive and developmental regulation of Delta(1)-pyrroline-5-carboxylate synthetase 1 (P5CS1) gene expression in Arabidopsis thaliana. Biochem Biophys Res Commun 261:766–772PubMedCrossRefGoogle Scholar
  40. Zhang Y, Xu W, Li Z, Deng XW, Wu W, Xue Y (2008) F-box protein DOR functions as a novel inhibitory factor for abscisic acid-induced stomatal closure under drought stress in Arabidopsis. Plant Physiol 148:2121–2133PubMedCrossRefPubMedCentralGoogle Scholar
  41. Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Guoyun Xu
    • 1
  • Yanchun Cui
    • 1
  • Manling Wang
    • 1
  • Mingjuan Li
    • 1
  • Xuming Yin
    • 1
  • Xinjie Xia
    • 1
  1. 1.Key Laboratory for Agro-Ecological Process in Subtropical Region, Institute of Subtropical AgricultureChinese Academy of SciencesChangshaChina

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