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The microRNA156 and microRNA172 gene regulation cascades at post-germinative stages in Arabidopsis

Published online by Cambridge University Press:  17 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

MicroRNAs (miRNAs) are involved in developmental programmes of plants, including seed germination and post-germination. Here, we provide evidence that two different miRNA pathways, miR156 and miR172, interact during the post-germination stages in Arabidopsis. Mutant seedlings expressing miR156-resistant SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE13 (mSPL13), which has silent mutations in the miR156 complementary sequence, over-accumulated SPL13 mRNA and exhibited a delay in seedling development. Microarray analysis indicated that SCHNARCHZAPFEN (SNZ), an AP2-like gene targeted by miR172, was down-regulated in these mutants. Quantitative reverse transcription-polymerase chain reaction (RT-PCR) and miRNA gel blot analyses showed that the MIR172 genes were up-regulated in mSPL13 mutants. These results suggest that the miRNA regulation cascades (miR156⊣SPL13 → miR172⊣SNZ) play a critical role during the post-germination developmental stages in Arabidopsis.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2010

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References

Arazi, T., Talmor-Neiman, M., Stav, R., Riese, M., Huijser, P. and Baulcombe, D.C. (2005) Cloning and characterization of micro-RNAs from moss. The Plant Journal 43, 837848.CrossRefGoogle ScholarPubMed
Aukerman, M.J. and Sakai, H. (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. The Plant Cell 15, 27302741.CrossRefGoogle ScholarPubMed
Birkenbihl, R.P., Jach, G., Saedler, H. and Huijser, P. (2005) Functional dissection of the plant-specific SBP-domain: Overlap of the DNA-binding and nuclear localization domains. Journal of Molecular Biology 352, 585596.CrossRefGoogle ScholarPubMed
Brodersen, P., Sakvarelidze-Achard, L., Bruun-Rasmussen, M., Dunoyer, P., Yamamoto, Y.Y., Sieburth, L. and Voinnet, O. (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320, 11851190.CrossRefGoogle ScholarPubMed
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
Chen, J., Li, W.X., Xie, D., Peng, J.R. and Ding, S.W. (2004) Viral virulence protein suppresses RNA silencing-mediated defense but upregulates the role of microRNA in host gene expression. The Plant Cell 16, 13021313.Google Scholar
Chen, X. (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303, 20222025.CrossRefGoogle ScholarPubMed
Chuck, G., Cigan, A.M., Saeteurn, K. and Hake, S. (2007) The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nature Genetics 39, 544549.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
Evans, M.M., Passas, H.J. and Poethig, R.S. (1994) Heterochronic effects of glossy15 mutations on epidermal cell identity in maize. Development 120, 19711981.Google Scholar
Gandikota, M., Birkenbihl, R.P., Hohmann, S., Cardon, G.H., Saedler, H. and Huijser, P. (2007) The miRNA156/157 recognition element in the 3′ UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. The Plant Journal 49, 683693.Google Scholar
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.Google Scholar
Holland, P.M., Abramson, R.D., Watson, R. and Gelfand, D.H. (1991) Detection of specific polymerase chain reaction product by utilizing the 5′ → 3′ exonuclease activity of Thermus aquaticus DNA polymerase. Proceedings of the National Academy of Sciences, USA, 88, 72767280.Google Scholar
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
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., 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 regulation of post-germinative transition from the cotyledon- to vegetative-leaf stages by microRNA-targeted SQUAMOSA PROMOTER-BINDING PROTEIN LIKE13 in Arabidopsis. Seed Science Research 20, 8996.CrossRefGoogle Scholar
Moose, S.P. and Sisco, P.H. (1994) Glossy15 controls the epidermal juvenile-to-adult phase transition in maize. The Plant Cell 6, 13431355.Google Scholar
Moose, S.P. and Sisco, P.H. (1996) Glossy15, an APETALA2-like gene from maize that regulates leaf epidermal cell identity. Genes & Development 10, 30183027.Google Scholar
Motchoulski, A. and Liscum, E. (1999) Arabidopsis NPH3: A NPH1 photoreceptor-interacting protein essential for phototropism. Science 286, 961964.Google Scholar
Rhoades, M.W., Reinhart, B.J., Lim, L.P., Burge, C.B., Bartel, B. and Bartel, D.P. (2002) Prediction of plant microRNA targets. Cell 110, 513520.CrossRefGoogle ScholarPubMed
Riese, M., Hohmann, S., Saedler, H., Munster, T. and Huijser, P. (2007) Comparative analysis of the SBP-box gene families in P. patens and seed plants. Gene 401, 2837.CrossRefGoogle Scholar
Schmid, M., Uhlenhaut, N.H., Godard, F., Demar, M., Bressan, R., Weigel, D. and Lohmann, J.U. (2003) Dissection of floral induction pathways using global expression analysis. Development 130, 60016012.CrossRefGoogle ScholarPubMed
Schwab, R., Palatnik, J.F., Riester, M., Schommer, C., Schmid, M. and Weigel, D. (2005) Specific effects of microRNAs on the plant transcriptome. Developmental Cell 8, 517527.Google 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
Wang, H., Nussbaum-Wagler, T., Li, B., Zhao, Q., Vigouroux, Y., Faller, M., Bomblies, K., Lukens, L. and Doebley, J.F. (2005) The origin of the naked grains of maize. Nature 436, 714719.Google Scholar
Wu, G. and Poethig, R.S. (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133, 35393547.CrossRefGoogle ScholarPubMed
Wu, G., Park, M.Y., Conway, S.R., Wang, J.-W., Weigel, D. and Poethig, R.S. (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138, 750759.CrossRefGoogle ScholarPubMed
Wurschum, T., Gross-Hardt, R. and Laux, T. (2006) APETALA2 regulates the stem cell niche in the Arabidopsis shoot meristem. The Plant Cell 18, 295307.Google Scholar
Xie, Z., Allen, E., Fahlgren, N., Calamar, A., Givan, S.A. and Carrington, J.C. (2005) Expression of Arabidopsis MIRNA genes. Plant Physiology 138, 21452154.CrossRefGoogle ScholarPubMed
Yamauchi, Y., Ogawa, M., Kuwahara, A., Hanada, A., Kamiya, Y. and Yamaguchi, S. (2004) Activation of gibberellin biosynthesis and response pathways by low temperature during imbibition of Arabidopsis thaliana seeds. The Plant Cell 16, 367378.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar