A Novel Gene Encoding Ankyrin-Repeat Protein, SHG1, is Indispensable for Seed Germination under Moderate Salt Stress
Salt stress adversely affects plant growth at various stages of development including seed germination, seedling establishment, vegetative growth and finally reproduction. Because of their immobile nature, plants have evolved mechanisms to sense and respond to salt stress. Seed dormancy is an adaptive trait that enables seed germination to coincide with favorable environmental conditions. We identified a novel locus of Arabidopsis, designated SHG1 (salt hypersensitive germination 1), whose disruption leads to reduced germination rate under moderate salt stress conditions. SHG1 encodes a transmembrane protein with an ankyrin-repeat motif that has been implicated in diverse cellular processes such as signal transduction. The shg1-disrupted Arabidopsis mutant died at the cotyledon stage when sown on salt-containing medium, although wild-type plants could form true leaves under the same conditions. On the other hand, this mutant showed similar phenotypes to wild-type plants when sown on medium without salt and transferred to salt-containing medium at the vegetative stage. These results suggested that SHG1 played indispensable role in the seed germination and seedling establishment under moderate salt stress conditions. SHG1 may be involved in the release of seed dormancy.
[1] C. Chang, B. Wang, L. Shi, Y. Li, L. Duo, and W. Zhang, "Alleviation of Salt Stress-Induced Inhibition of Seed Germination in Cucumber (Cucumis sativus L.) by Ethylene and Glutamate,” J. Plant Phys., vol. 167, pp. 1152–1156, 2010.
[2] A. J. Vallejo, M. J. Yanovsky, and J. F. Botto, "Germination Variation in Arabidopsis thaliana Accessions under Moderate Osmotic and Salt Stresses,” Ann. Botany, vol. 106, pp.833-842, 2010.
[3] W. E. Finch-Savage, and G. Leubner-Metzger, "Seed Dormancy and the Control of Germination,” New Phytol., vol. 171, pp. 501-523, 2006.
[4] C. Becerra, T. Jahrmann, P. Puigdomènech, and C.M. Vicient, "Ankyrin Repeat- Containing Proteins in Arabidopsis: Characterization of a Novel and Abundant Group of Genes Coding ankyrin-transmembrane proteins,” Gene, vol. 340, pp. 111–121, 2004.
[5] J. Huang, X. Zhao, H. Yu, Y. Ouyang, L. Wang, and Q. Zhang, "The Ankyrin Repeat Gene Family in Rice. Genome-Wide Identification, Classification and Expression Profiling,” Plant Mol. Biol., vol. 71, pp. 207–226, 2009.
[6] H. Lu, D.N. Rate, J.T. Song, and J.T. Greenberg, "ACD6, a Novel Ankyrin Protein, is a Regulator and an Effector of Salicylic Acid Signaling in the Arabidopsis Defense Response,” Plant Cell, vol. 15, pp. 2408–2420, 2003.
[7] H. Lu, Y. Liu, and J.T. Greenberg, "Structure–Function Analysis of the Plasma Membrane-Localized Arabidopsis Defense Component ACD6,” Plant J., vol. 44, pp. 798–809, 2005.
[8] Y. Yang, Y. Zhang, P. Ding, K. Johnson, X. Li, and Y. Zhang, "The Ankyrin-Repeat Transmembrane Protein BDA1 Functions Downstream of the Receptor-Like Protein SNC2 to Regulate Plant Immunity,” Plant Physiol., vol. 159, pp. 1857–1865, 2012.
[9] H. Sakamoto, O. Matsuda, and K. Iba, "ITN1, a Novel Gene Encoding an Ankyrin-Repeat Protein that Affects the ABA-Mediated Production of Reactive Oxygen Species and Is Involved in Salt-Stress Tolerance in Arabidopsis thaliana,” Plant J., vol. 56, pp. 411–422, 2008.
[10] H. Sakamoto, K. Sakata, K. Kusumi, M. Kojima, H. Sakakibara, and K. Iba, "Interaction between a Plasma Membrane-Localized Ankyrin-Repeat Protein ITN1 and a Nuclear Protein RTV1,” Biochem. Biophys. Res. Commun., vol. 423, pp. 392–397, 2012.
[11] H. Sakamoto, Y. Nakagawara, and S. Oguri, "The Expression of a Novel Gene Encoding an Ankyrin-Repeat Protein, DRA1, is Regulated by Drought-Responsive Alternative Splicing,” Int. J. Biol. Life Sci. Eng.,vol. 7, pp. 81-84, 2013.
[12] T. Murashige, and F. Skoog, "A Revised Medium for Rapid Growth and Bioassays with Tobacco Tissue Culture,” Physiol. Plant., vol. 15, pp. 473–497, 1962.
[13] T. Nanjo, M. Kobayashi, Y. Yoshiba, Y. Kakubari, K. Yamaguchi-Shinozaki, and K. Shinozaki, "Antisense Suppression of Proline Degradation Improves Tolerance to Freezing and Salinity in Arabidopsis thaliana,” FEBS Lett., vol. 461, pp. 205–210, 1999.
[14] S. Mahajan, and N. Tuteja, "Cold, Salinity and Drought Stresses: An Overview,” Arch. Biochem. Biophys., vol. 444, pp. 139–158, 2005.
[15] J. Y. Kang, H. I. Choi, M. Y. Im, and S. Y. Kim, "Arabidopsis Basic Leucine Zipper Proteins That Mediate Stress-Responsive Abscisic Acid Signaling,” Plant Cell, vol. 14, pp. 343–357, 2002.
[1] C. Chang, B. Wang, L. Shi, Y. Li, L. Duo, and W. Zhang, "Alleviation of Salt Stress-Induced Inhibition of Seed Germination in Cucumber (Cucumis sativus L.) by Ethylene and Glutamate,” J. Plant Phys., vol. 167, pp. 1152–1156, 2010.
[2] A. J. Vallejo, M. J. Yanovsky, and J. F. Botto, "Germination Variation in Arabidopsis thaliana Accessions under Moderate Osmotic and Salt Stresses,” Ann. Botany, vol. 106, pp.833-842, 2010.
[3] W. E. Finch-Savage, and G. Leubner-Metzger, "Seed Dormancy and the Control of Germination,” New Phytol., vol. 171, pp. 501-523, 2006.
[4] C. Becerra, T. Jahrmann, P. Puigdomènech, and C.M. Vicient, "Ankyrin Repeat- Containing Proteins in Arabidopsis: Characterization of a Novel and Abundant Group of Genes Coding ankyrin-transmembrane proteins,” Gene, vol. 340, pp. 111–121, 2004.
[5] J. Huang, X. Zhao, H. Yu, Y. Ouyang, L. Wang, and Q. Zhang, "The Ankyrin Repeat Gene Family in Rice. Genome-Wide Identification, Classification and Expression Profiling,” Plant Mol. Biol., vol. 71, pp. 207–226, 2009.
[6] H. Lu, D.N. Rate, J.T. Song, and J.T. Greenberg, "ACD6, a Novel Ankyrin Protein, is a Regulator and an Effector of Salicylic Acid Signaling in the Arabidopsis Defense Response,” Plant Cell, vol. 15, pp. 2408–2420, 2003.
[7] H. Lu, Y. Liu, and J.T. Greenberg, "Structure–Function Analysis of the Plasma Membrane-Localized Arabidopsis Defense Component ACD6,” Plant J., vol. 44, pp. 798–809, 2005.
[8] Y. Yang, Y. Zhang, P. Ding, K. Johnson, X. Li, and Y. Zhang, "The Ankyrin-Repeat Transmembrane Protein BDA1 Functions Downstream of the Receptor-Like Protein SNC2 to Regulate Plant Immunity,” Plant Physiol., vol. 159, pp. 1857–1865, 2012.
[9] H. Sakamoto, O. Matsuda, and K. Iba, "ITN1, a Novel Gene Encoding an Ankyrin-Repeat Protein that Affects the ABA-Mediated Production of Reactive Oxygen Species and Is Involved in Salt-Stress Tolerance in Arabidopsis thaliana,” Plant J., vol. 56, pp. 411–422, 2008.
[10] H. Sakamoto, K. Sakata, K. Kusumi, M. Kojima, H. Sakakibara, and K. Iba, "Interaction between a Plasma Membrane-Localized Ankyrin-Repeat Protein ITN1 and a Nuclear Protein RTV1,” Biochem. Biophys. Res. Commun., vol. 423, pp. 392–397, 2012.
[11] H. Sakamoto, Y. Nakagawara, and S. Oguri, "The Expression of a Novel Gene Encoding an Ankyrin-Repeat Protein, DRA1, is Regulated by Drought-Responsive Alternative Splicing,” Int. J. Biol. Life Sci. Eng.,vol. 7, pp. 81-84, 2013.
[12] T. Murashige, and F. Skoog, "A Revised Medium for Rapid Growth and Bioassays with Tobacco Tissue Culture,” Physiol. Plant., vol. 15, pp. 473–497, 1962.
[13] T. Nanjo, M. Kobayashi, Y. Yoshiba, Y. Kakubari, K. Yamaguchi-Shinozaki, and K. Shinozaki, "Antisense Suppression of Proline Degradation Improves Tolerance to Freezing and Salinity in Arabidopsis thaliana,” FEBS Lett., vol. 461, pp. 205–210, 1999.
[14] S. Mahajan, and N. Tuteja, "Cold, Salinity and Drought Stresses: An Overview,” Arch. Biochem. Biophys., vol. 444, pp. 139–158, 2005.
[15] J. Y. Kang, H. I. Choi, M. Y. Im, and S. Y. Kim, "Arabidopsis Basic Leucine Zipper Proteins That Mediate Stress-Responsive Abscisic Acid Signaling,” Plant Cell, vol. 14, pp. 343–357, 2002.
@article{"International Journal of Biological, Life and Agricultural Sciences:66752", author = "H. Sakamoto and J. Tochimoto and S. Kurosawa and M. Suzuki and S. Oguri", title = "A Novel Gene Encoding Ankyrin-Repeat Protein, SHG1, is Indispensable for Seed Germination under Moderate Salt Stress", abstract = "Salt stress adversely affects plant growth at various stages of development including seed germination, seedling establishment, vegetative growth and finally reproduction. Because of their immobile nature, plants have evolved mechanisms to sense and respond to salt stress. Seed dormancy is an adaptive trait that enables seed germination to coincide with favorable environmental conditions. We identified a novel locus of Arabidopsis, designated SHG1 (salt hypersensitive germination 1), whose disruption leads to reduced germination rate under moderate salt stress conditions. SHG1 encodes a transmembrane protein with an ankyrin-repeat motif that has been implicated in diverse cellular processes such as signal transduction. The shg1-disrupted Arabidopsis mutant died at the cotyledon stage when sown on salt-containing medium, although wild-type plants could form true leaves under the same conditions. On the other hand, this mutant showed similar phenotypes to wild-type plants when sown on medium without salt and transferred to salt-containing medium at the vegetative stage. These results suggested that SHG1 played indispensable role in the seed germination and seedling establishment under moderate salt stress conditions. SHG1 may be involved in the release of seed dormancy.
", keywords = "Germination, ankyrin repeat, Arabidopsis, salt tolerance.", volume = "8", number = "3", pages = "244-4", }
