Environmental perception and epigenetic memory: mechanistic insight through FLC

Abstract

Chromatin plays a central role in orchestrating gene regulation at the transcriptional level. However, our understanding of how chromatin states are altered in response to environmental and developmental cues, and then maintained epigenetically over many cell divisions, remains poor. The floral repressor gene FLOWERING LOCUS C (FLC) in Arabidopsis thaliana is a useful system to address these questions. FLC is transcriptionally repressed during exposure to cold temperatures, allowing studies of how environmental conditions alter expression states at the chromatin level. FLC repression is also epigenetically maintained during subsequent development in warm conditions, so that exposure to cold may be remembered. This memory depends on molecular complexes that are highly conserved among eukaryotes, making FLC not only interesting as a paradigm for understanding biological decision-making in plants, but also an important system for elucidating chromatin-based gene regulation more generally. In this review, we summarize our understanding of how cold temperature induces a switch in the FLC chromatin state, and how this state is epigenetically remembered. We also discuss how the epigenetic state of FLC is reprogrammed in the seed to ensure a requirement for cold exposure in the next generation.Significance StatementFLOWERING LOCUS C (FLC) regulation provides a paradigm for understanding how chromatin can be modulated to determine gene expression in a developmental context. This review describes our current mechanistic understanding of how FLC expression is genetically specified and epigenetically regulated throughout the plant life cycle, and how this determines plant life-history strategy.

Chloroplast retrograde signal regulates flowering

“…3E and Fig. S8B), suggesting that the FLC promoter also contributes to its epigenetic regulation in addition to the first intron and noncoding RNA (14,45). Thus, our study supports the idea that specific nucleotide sequence signatures in different parts of FLC may be recognized by distinct genetic mechanisms to facilitate a flexible evolutionary response to diverse environmental factors (52,53).…”

“…In winterannual Arabidopsis, FLC expression is stably silenced by prolonged cold exposure during winter and then maintained until embryogenesis in an epigenetic-dependent manner. This process involves the polycomb-mediated multiple chromatin regulation and different long noncoding RNA (lncRNA) transcription to quantitatively repress the FLC gene expression, thereby enabling other floral promotion signals to induce flowering in the spring (13,14).…”

The RNA-induced transcriptional silencing complex targets chromatin exclusively via interacting with nascent transcripts

“…However, this seemingly "analog" silencing response is the net result of digital silencing events that occur in individual cells of that particular tissue over time. Thereby, a population of cells as a whole can respond quantitatively to an environmental change by simply switching individual cells from an on state to an off state (Berry and Dean 2015).…”

Physical coupling of activation and derepression activities to maintain an active transcriptional state at FLC

“…We used Arabidopsis FLOWERING LOCUS C (FLC) as a model gene to explore histone-based transcriptional regulation and epigenetic memory. Local chromatin states are critical for quantitatively controlling FLC expression (9). Active FLC expression requires functional FRIGIDA (FRI) and a set of histone modifying Trithorax homologs, Complex Proteins Associated with Set1 (COMPASS), RNA polymerase II Associated Factor 1 complex (PAF1C), and SET DOMAIN GROUP 8 (SDG8), the major H3K36 methyltransferase (10)(11)(12)(13)(14)(15)(16)(17).…”