Hostname: page-component-848d4c4894-mwx4w Total loading time: 0 Render date: 2024-06-19T01:52:20.645Z Has data issue: false hasContentIssue false

The regulation of post-germinative transition from the cotyledon- to vegetative-leaf stages by microRNA-targeted SQUAMOSA PROMOTER-BINDING PROTEIN LIKE13 in Arabidopsis

Published online by Cambridge University Press:  18 March 2010

Ruth C. Martin
Affiliation:
USDA-ARS, National Forage Seed Production Research Center, Corvallis, Oregon97331, USA
Masashi Asahina
Affiliation:
Department of Horticulture, Oregon State University, Corvallis, OR97331, USA
Po-Pu Liu
Affiliation:
Department of Horticulture, Oregon State University, Corvallis, OR97331, USA
Jessica R. Kristof
Affiliation:
Department of Horticulture, Oregon State University, Corvallis, OR97331, USA
Jennifer L. Coppersmith
Affiliation:
Department of Horticulture, Oregon State University, Corvallis, OR97331, USA
Wioletta E. Pluskota
Affiliation:
Department of Horticulture, Oregon State University, Corvallis, OR97331, USA
George W. Bassel
Affiliation:
Department of Horticulture, Oregon State University, Corvallis, OR97331, USA
Natalya A. Goloviznina
Affiliation:
Department of Horticulture, Oregon State University, Corvallis, OR97331, USA
Theresa T. Nguyen
Affiliation:
Department of Horticulture, Oregon State University, Corvallis, OR97331, USA
Cristina Martínez-Andújar
Affiliation:
Department of Horticulture, Oregon State University, Corvallis, OR97331, USA
M.B. Arun Kumar
Affiliation:
Department of Horticulture, Oregon State University, Corvallis, OR97331, USA
Piotr Pupel
Affiliation:
Department of Horticulture, Oregon State University, Corvallis, OR97331, USA
Hiroyuki Nonogaki*
Affiliation:
Department of Horticulture, Oregon State University, Corvallis, OR97331, USA
*
*Correspondence Fax: +1 (541) 737-3479 Email: hiro.nonogaki@oregonstate.edu

Abstract

Germination and early seedling development are critical for successful stand establishment of plants. Following germination, the cotyledons, which are derived from embryonic tissue, emerge from the seed. Arabidopsis seedlings at post-germinative stages are supported mainly by the supply of nutrition from the cotyledons until vegetative leaves emerge and initiate photosynthesis. The switch to autotrophic growth is a significant transition at the post-germinative stage. Here, we provide evidence that down-regulation of SQUAMOSA PROMOTER-BINDING PROTEIN LIKE13 (SPL13) by microRNA156 (miR156) plays an important role in the regulation of the post-germinative switch from the cotyledon stage to the vegetative-leaf stage. Silent mutations created in the SPL13 sequence in the region that is complementary to the miR156 sequence caused the deregulation of the mutant form of SPL13 (mSPL13) mRNA from miR156. Mutant seedlings over-accumulated miRNA-resistant messages and exhibited a delay in the emergence of vegetative leaves compared to wild-type seedlings. The delay was not observed in control transgenic plants expressing non-mutated SPL13, indicating that the phenotype was caused specifically by the silent mutations and deregulation of SPL13 from miR156. Characterization of the SPL13 promoter indicated that this gene is expressed mainly in the hypocotyl and affects leaf primordium development. These results suggest that the repression of SPL13 by miR156 is essential for normal post-germinative growth in Arabidopsis.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ariizumi, T., Murase, K., Sun, T.-P. and Steber, C.M. (2008) Proteolysis-independent downregulation of DELLA repression in Arabidopsis by the gibberellin receptor GIBBERELLIN INSENSITIVE DWARF1. The Plant Cell 20, 24472459.CrossRefGoogle ScholarPubMed
Becker, D., Kemper, E., Schell, J. and Masterson, R. (1992) New plant binary vectors with selectable markers located proximal to the left T-DNA border. Plant Molecular Biology 20, 11951197.CrossRefGoogle Scholar
Cardon, G.H., Hohmann, S., Nettesheim, K., Saedler, H. and Huijser, P. (1997) Functional analysis of the Arabidopsis thaliana SBP-box gene SPL3: a novel gene involved in the floral transition. The Plant Journal 12, 367377.CrossRefGoogle ScholarPubMed
Cardon, G., Hohmann, S., Klein, J., Nettesheim, K., Saedler, H. and Huijser, P. (1999) Molecular characterisation of the Arabidopsis SBP-box genes. Gene 237, 91104.CrossRefGoogle ScholarPubMed
Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735743.CrossRefGoogle Scholar
Grebenok, R.J., Pierson, E., Lambert, G.M., Gong, F.C., Afonso, C.L., Haldeman-Cahill, R., Carrington, J.C. and Galbraith, D.W. (1997) Green-fluorescent protein fusions for efficient characterization of nuclear targeting. The Plant Journal 11, 573586.Google ScholarPubMed
Ho, S.N., Hunt, H.D., Horton, R.M., Pullen, J.K. and Pease, L.R. (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77, 5159.CrossRefGoogle ScholarPubMed
Huijser, P., Klein, J., Lonnig, W.E., Meijer, H., Saedler, H. and Sommer, H. (1992) Bracteomania, an inflorescence anomaly, is caused by the loss of function of the MADS-box gene squamosa in Antirrhinum majus. EMBO Journal 11, 12391249.CrossRefGoogle ScholarPubMed
Klein, J., Saedler, H. and Huijser, P. (1996) A new family of DNA binding proteins includes putative transcriptional regulators of the Antirrhinum majus floral meristem identity gene SQUAMOSA. Molecular and General Genetics 250, 716.Google ScholarPubMed
Kropat, J., Tottey, S., Birkenbihl, R.P., Depege, N., Huijser, P. and Merchant, S. (2005) A regulator of nutritional copper signaling in Chlamydomonas is an SBP domain protein that recognizes the GTAC core of copper response element. Proceedings of the National Academy of Sciences, USA 102, 1873018735.CrossRefGoogle ScholarPubMed
Liu, P.-P., Montgomery, T.A., Fahlgren, N., Kasschau, K.D., Nonogaki, H. and Carrington, J.C. (2007) Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. The Plant Journal 52, 133146.CrossRefGoogle ScholarPubMed
Mandel, M.A. and Yanofsky, M.F. (1995) A gene triggering flower formation in Arabidopsis. Nature 377, 522524.CrossRefGoogle ScholarPubMed
Mandel, A.M., Gustafson-Brown, C., Savidge, B. and Yanofsky, M.F. (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360, 273277.CrossRefGoogle ScholarPubMed
Martin, R.C., Liu, P.-P. and Nonogaki, H. (2005) Simple purification of small RNAs from seeds and efficient detection of multiple microRNAs expressed in Arabidopsis thaliana and tomato (Lycopersicon esculentum) seeds. Seed Science Research 15, 319328.CrossRefGoogle Scholar
Martin, R.C., Liu, P.-P. and Nonogaki, H. (2006) microRNAs in seeds: modified detection techniques and potential applications. Canadian Journal of Botany 84, 189198.CrossRefGoogle Scholar
Martin, R.C., Asahina, M., Liu, P.-P., Kristof, J.R., Coppersmith, J.L., Pluskota, W.E., Bassel, G.W., Goloviznina, N.A., Nguyen, T.T., Martínez-Andújar, C., Kumar, M.B.A., Pupel, P. and Nonogaki, H. (2010) The microRNA156 and microRNA172 gene regulation cascades at post-germinative stages in Arabidopsis. Seed Science Research 20, 7987.CrossRefGoogle Scholar
Nonogaki, H., Liu, P.-P., Hewitt, J.R. and Martin, R.C. (2007) Regulation of seed germination and stand establishment – importance of repression of developmental programs. Acta Horticulture 782, 5157.Google Scholar
Seo, M., Nambara, E., Choi, G. and Yamaguchi, S. (2009) Interaction of light and hormone signals in germinating seeds. Plant Molecular Biology 69, 463472.CrossRefGoogle ScholarPubMed
Steber, C.M. (2007) De-repression of seed germination by GA signaling. pp. 248263in Bradford, K.J.; Nonogaki, H. (Eds) Seed development, dormancy and germination. Oxford, Blackwell Publishing.CrossRefGoogle Scholar
Unte, U.S., Sorensen, A.M., Pesaresi, P., Gandikota, M., Leister, D., Saedler, H. and Huijser, P. (2003) SPL8, an SBP-box gene that affects pollen sac development in Arabidopsis. The Plant Cell 15, 10091019.CrossRefGoogle ScholarPubMed
Weigel, D. and Glazebrook, J. (2002) Arabidopsis: a laboratory manual. New York, Cold Spring Harbor Laboratory Press.Google Scholar
Xie, K., Wu, C. and Xiong, L. (2006) Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiology 142, 280293.CrossRefGoogle ScholarPubMed
Yamaguchi, S., Kamiya, Y. and Nambara, E. (2007) Regulation of ABA and GA levels during seed development and germination in Arabidopsis. pp. 224247in Bradford, K.J.; Nonogaki, H. (Eds) Seed development, dormancy and germination. Oxford, Blackwell Publishing.CrossRefGoogle Scholar
Zhang, Y., Schwarz, S., Saedler, H. and Huijser, P. (2006) SPL8, a local regulator in a subset of gibberellin-mediated developmental processes in Arabidopsis. Plant Molecular Biology 63, 429439.Google Scholar