Department of Biology

Program

Molecular, Cellular & Developmental Biology

Research Areas

• Chromatin, Chromosomes, and Genome Integrity
• Developmental Mechanisms and Regulation in Eukaryotic Systems
• Plant Molecular Biology

Education

Ph.D. University of Wisconsin-Madison, 1999
Postdoctoral Fellow, University of Wisconsin-Madison, 1999-2003

Awards

Outstanding Junior Faculty Award
NSF CAREER Award

Research Description

REGULATION OF CHROMATIN STRUCTURE AND GENE EXPRESSION BY EPIGENETIC MODIFICATIONS

Chromatin is the term used to describe DNA and associated packaging proteins (e.g. histones). Modifications of histones, such as methylation and acetylation at specific positions can cause the DNA to be packaged more tightly and become less transcriptionally active (heterochromatin), whereas other histone modifications can increase transcriptional activity by opening up the chromatin structure (euchromatin). These modifications are sometimes referred to as the "histone code" and play an important role in the regulation of gene expression in all eukaryotes. The sequences of histones, and in many cases histone-modifying enzymes, are highly conserved. Therefore, there is a high likelihood that the knowledge gained from research in model systems will have broad applications in all eukaryotes.

In our laboratory, we use two different models to study the links between histone modifications, chromatin structure, and gene expression. The first model is the constitutive heterochromatin present in Arabidopsis nuclei. In wild-type nuclei, 8-10 spots of highly compacted heterochromatin are visible (Fig 1). These spots are called chromocenters and contain repetitive sequences, transposons, and rDNA genes. Histones in chromocenters are marked by modifications that are known to repress gene expression, such as histone H3 monomethylation at lysine 27 (H3K27me1). Our laboratory has identified ATXR5 and ATXR6 as the enzymes that are responsible for H3K27me1 at chromocenters and the loss of these enzymes leads to loss of gene silencing and decondensation of heterochromatin (Fig 1). Ongoing work in our lab is elucidating the mechanisms by which the activity of ATXR5 and ATXR6 is targeted to heterochromatin and how H3K27 methylation leads to gene silencing.

The second model that we use is an epigenetic switch that is triggered by signals from the environment. To ensure that flowering occurs at a favorable time of year, many plants growing in temperate climates have adopted a biennial growth habit. These plants contain a block to flowering that is eliminated by the prolonged cold temperatures of winter; thus flowering is prevented prior to winter and promoted in the favorable conditions of spring. In biennial-like, winter-annual accessions of Arabidopsis, this block to flowering is created by the floral repressor FLOWERING LOCUS C (FLC). Prior to winter, FLC is highly expressed and prevents flowering. Cold treatment, in turn, causes a permanent epigenetic shut off of FLC expression that is mediated by repressive histone modifications at the FLC locus. Our laboratory is actively involved in determining that molecular mechanisms that control this epigenetic switch.

Select Publications

Benjamin K. Blackman, Jared L. Strasburg, Andrew R. Raduski, Scott D. Michaels, Loren H. Rieseberg. 2010. The Role of Recently Derived FT Paralogs in Sunflower Domestication. Current Biology, in press.

Michaels, S.D. 2009. Flowering time regulation produces much fruit. Current Opinion in Plant Biology, 12: 75-80.

Jacob, Y. and Michaels, S.D. 2009. H3K27me1 is E(z) in animals, but not in plants. Epigenetics, 4: 266-269.

Jacob, Y., Feng, S., LeBlanc, C.A., Bernatavichute, Y.V., Stroud, H., Cokus, S., Johnson, L.M., Pellegrini, M., Jacobsen, S.E., and Michaels, S.D. 2009. ATXR5 and ATXR6 are H3K27 monomethyltransferases required for chromatin structure and gene silencing. Nature Structural and Molecular Biology, 16: 763-768.

Bonnie M. Weasner, Brandon Weasner, Stephanie M. DeYoung, Scott D. Michaels and Justin P. Kumar. 2009. Transcriptional activities of the Pax6 gene eyeless regulate tissue specificity of ectopic eye formation in Drosophila. Developmental Biology, 492-502.

Michaels, S.D. 2009. Integration of photoperiodic timing and vernalization. In: Photoperiodism: Seasonal Time Measurement. Edited by Randy J. Nelson, David Denlinger and David Somers. Oxford University Press.

Veley, K.M. and Michaels, S.D. 2008. Functional redundancy and new roles for genes of the autonomous floral-promotion pathway. Plant Physiology 147 (2): 682-695.

Jacob, Y. and Michaels, S.D. 2008. Peering through the pore; the role of AtTPR in nuclear transport and development. Plant Signaling and Behavior 3 (1): 62-64.

Kim, S.Y., Yu, X., and Michaels, S.D. 2008. Regulation CONSTANS and FT expression in response to changing light quality. Plant Physiology 148: 269-279 .

Jacob, Y., Mongkolsiriwatana, C., Veley, K., Kim, S.Y., and Michaels, S.D. 2007. The nuclear pore protein AtTPR is required for RNA homeostasis, flowering time, and auxin signaling. Plant Physiology 144(3): 1383-90.

Kim, S.Y. and Michaels, S.D. 2006. SUPPRESSOR OF FRI 4 encodes a nuclear-localized protein that is required for delayed flowering in winter-annual Arabidopsis. Development, 133(23): 4699-707.

Salathia, N., Davis, S.J., Lynn, J.R., Michaels, S.D., Amasino, R.M., and Millar, A.J. 2006. FLOWERING LOCUS C -dependent and -independent regulation of the circadian clock by the autonomous and vernalization pathways. BMC Plant Biology 6:10.

Doyle, M.R., Bizzell, C.M., Keller, M.R, Michaels, S.D., Song, J., Noh, Y.S., and Amasino, R.M. 2005. HUA2 is required for the expression of floral repressors in Arabidopsis thaliana. Plant Journal 41: 376-385.

Michaels, S.D., Himelblau, E., Kim, S.Y., Schomburg, F.M., and Amasino, R.M. 2005. Integration of flowering signals in winter-annual Arabidopsis. Plant Physiology 137: 149-156.

Schmitz, R.J., Hong, L., Michaels, S.D., and Amasino, R.M. 2005. FRIGIDA-ESSENTIAL 1 interacts genetically with FRIGIDA and FRIGIDA-LIKE 1 to promote the winter-annual habit of Arabidopsis thaliana. Development 132: 5471-5478.

Kim, S.Y., He, Y., Jacob, Y., Noh, Y.S., Michaels, S.D., and Amasino, R.M. 2005. Establishment of the vernalization-responsive, winter-annual habit in Arabidopsis requires a putative histone H3 methyl transferase. Plant Cell 17: 3301-10.

Choi K., Kim S., Kim S.Y., Kim M., Hyun Y., Lee H., Choe S., Kim S.G., Michaels S., Lee I. 2005. SUPPRESSOR OF FRIGIDA3 encodes a nuclear ACTIN-RELATED PROTEIN6 required for floral repression in Arabidopsis. Plant Cell 17: 2647-2660.

Michaels, S.D., Bezzerra, I.C., and Amasino, R.M. 2004. FRIGIDA-related genes are required for the winter-annual habit in Arabidopsis. PNAS 101: 3281-5.

Bezerra, I.C., Michaels, S.D., Schomburg, F., and Amasino, R.M. 2004. Lesions in the mRNA cap-binding gene ABA HYPERSENSITIVE 1 suppress FRIGIDA-mediated delayed flowering. Plant Journal 40: 112-119.

He, Y., Michaels, S.D., and Amasino, R.M. 2003. Regulation of flowering time by histone acetylation in Arabidopsis. Science 305: 1751-1754.

Michaels, S.D., He, Y., Scortecci, K.C., and Amasino, R.M.  2003. Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis. PNAS 100: 10102-7.

Scortecci, K.C., Michaels, S.D., and Amasino, R.M.  2003. Genetic interactions between FLM and other flowering-time genes in Arabidopsis thaliana. Plant Molecular Biology 52: 915-22.

Michaels, S.D., Ditta, G., Gustafson-Brown, C., Soraya, P., Yanofsky, M., and Amasino, R.M.  2003. AGL24 acts as a promoter of flowering in Arabidopsis and is positively regulated by vernalization. Plant Journal 33: 867-874.

Kole, C., Quijada, P., Michaels, S.D., Amasino, R.M., and Osborn, T.C.  2001. Evidence for homology of flowering-time genes VFR2 from Brassica rapa and FLC from Arabidopsis thaliana. Theoretical and Applied Genetics 102: 425-430.

Michaels, S. and Amasino, R.  2001. High throughput isolation of DNA and RNA in 96-well format using a paint shaker. Plant Molecular Biology Reporter 19: 227-233.

Michaels, S., and Amasino, R.  2001. Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous-pathway mutations, but not responsiveness to vernalization. Plant Cell 13: 935-942.

Scortecci, K.C., Michaels, S.D., Amasino, R.M.  2001. Identification of a MADS-box gene, FLOWERING LOCUS M, that represses flowering. Plant Journal 26: 229-236.

Michaels, S., and Amasino, R.  2000. Memories of winter: vernalization and the competence to flower. Plant Cell and Environment 23: 1145-1154.

Johanson, U., West, J., Lister, C., Michaels, S., Amasino, R., and Dean, C.  2000. Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290: 344-347

Michaels, S.D. and Amasino, R.M.  1999. The gibberellic acid biosynthesis mutant ga1-3 of Arabidopsis thaliana is responsive to vernalization. Developmental Genetics 25: 194-198.

Michaels, S.D. and Amasino, R.M.  1999. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11: 949-956.

Swarup K., Alonso-Blanco C., Lynn J.R., Michaels S.D., Amasino R.M., Koornneef M., and Millar A.J. 1999. Natural allelic variation identifies new genes in the Arabidopsis circadian system. Plant Journal 20:67-78.

Michaels, S.D. and Amasino, R.M. 1998. A robust method for detecting single-nucleotide changes as polymorphic markers by PCR. The Plant Journal 14: 381-385.