The transition from vegetative development to flowering is a major event in the life cycle of plants. Stem cells in the shoot apical meristem switch from producing primordia that will give rise to the vegetative parts of the plant (e.g., leaves) to produce the reproductive structures (flowers). Thus flowering is an excellent system for studying how undifferentiated cells choose between alternative fates. Because proper timing of this transition is critical to reproductive success, it is highly regulated by both environmenta and endogenous factors. These cues allow plants to flower at a favorable time of year and at an appropriate stage of development. One key regulator of flowering time in Arabidopsis is FLOWERING LOCUS C (FLC), a MADS-domain-containing transcription factor that acts to delay flowering. The transcriptional regulation of FLC is highly complex. Late- flowering winter-annual strains contain active alleles of FRIGIDA (FRI) that cause FLC to be highly expressed. Through a process known as vernalization, however, FLC expression can be epigenetically silenced by a long period of cold exposure (e.g., winter). This system prevents winter-annual Arabidopsis from flowering prior to winter and promotes spring flowering. Rapid-cycling strains, in contrast, are naturally occurring null mutants for fri and flower early without vernalization. I these stains, FLC expression is repressed by a group of genes known collectively as the autonomous floral-promotion pathway. The autonomous pathway is required for the Polycomb Repressor Complex 2 (PRC2) to deposit repressive histone H3 lysine 27 trimethylation (H3K27me3) at FLC chromatin. The details of how the autonomous pathway facilitates PRC2 action remain unknown. The putative functions of the autonomous-pathway proteins (chromatin remodeling and RNA-binding/processing), however, suggest a link between RNA metabolism and chromatin remodeling. We propose a comprehensive set of genetic, genomic, and biochemical approaches to determine the molecular mechanism of the autonomous pathway. The fact that homologs of PRC2 and many of the autonomous pathway proteins exist in both plants and animals suggests that this mechanism is evolutionarily conserved and that our findings are likely to have broad impacts for understanding gene regulation in both plants and animals.

Public Health Relevance

Proper gene regulation is essential for development and the specification of tissue types;consequently, missexpression is associated with birth defects and many diseases (including cancer). DNA-packaging proteins, called histones, undergo extensive post- translational modification and these modifications comprise one of the primary mechanisms controlling gene expression in all eukaryotes. A complete understanding of how individual genes are targeted by histone modifying enzymes and how these modifications stimulate or repress gene expression is essential to our understanding of development and disease.

Agency
National Institute of Health (NIH)
Institute
National Institute of General Medical Sciences (NIGMS)
Type
Research Project (R01)
Project #
5R01GM075060-07
Application #
8633465
Study Section
Development - 1 Study Section (DEV1)
Program Officer
Haynes, Susan R
Project Start
2007-02-01
Project End
2017-01-31
Budget Start
2014-02-01
Budget End
2015-01-31
Support Year
7
Fiscal Year
2014
Total Cost
Indirect Cost
Name
Indiana University Bloomington
Department
Biology
Type
Schools of Arts and Sciences
DUNS #
City
Bloomington
State
IN
Country
United States
Zip Code
47401
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Ding, Lei; Kim, Sang Yeol; Michaels, Scott D (2013) FLOWERING LOCUS C EXPRESSOR family proteins regulate FLOWERING LOCUS C expression in both winter-annual and rapid-cycling Arabidopsis. Plant Physiol 163:243-52
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Stroud, Hume; Hale, Christopher J; Feng, Suhua et al. (2012) DNA methyltransferases are required to induce heterochromatic re-replication in Arabidopsis. PLoS Genet 8:e1002808

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