The Flowering Season-Meter at FLOWERING LOCUS C Across Life Histories in Crucifers

Abstract

Many plant species overwinter before they flower. Transition to flowering is aligned to the seasonal transition as a response to the prolonged cold in winter by a process called vernalization. Multiple well-documented vernalization properties in crucifer species with diverse life histories are derived from environmental regulation of a central inhibitor of the flowering gene, Flowering Locus C (FLC). Episode(s) of flowering are prevented during high FLC expression and enabled during low FLC expression. FLC repression outlasts the winter to coincide with spring; this heterochronic aspect is termed “winter memory.” In the annual Arabidopsis thaliana, winter memory has long been associated with the highly conserved histone modifiers Polycomb and Trithorax, which have antagonistic roles in transcription. However, there are experimental limitations in determining how dynamic, heterogenous histone modifications within the FLC locus generate the final transcriptional output. Recent theoretical considerations on cell-to-cell variability in gene expression and histone modifications generating bistable states brought support to the hypothesis of chromatin-encoded memory, as with other experimental systems in eukaryotes. Furthermore, these advances unify multiple properties of vernalization, not only the winter memory. Similarly, in the perennial Arabidopsis halleri ssp. gemmifera, recent integration of molecular with mathematical and ecological approaches unifies FLC chromatin features with the all-year-round memory of seasonal temperature. We develop the concept of FLC season-meter to combine existing information from the contrasting annual/perennial and experimental/theoretical sectors into a transitional framework. We highlight simplicity, high conservation, and discrete differences across extreme life histories in crucifers.

Plant environmental memory: implications, mechanisms and opportunities for plant scientists and beyond

“…Probably the most studied within-generation memory mechanism in plants is the one involving the regulation of flowering by overwintering, a process called vernalization. The A. thaliana MADS box transcription factor FLOWERING LOCUS C ( AtFLC ) is a central inhibitor of flowering and serves as a key developmental checkpoint where multiple signalling pathways converge ( Shindo et al 2005 ; Deng et al 2011 ; Méndez-Vigo et al 2015 ; Whittaker and Dean 2017 ; Buzas et al 2021 ). AtFLC regulation is a multilayered process, ranging from transcriptional regulation to epigenetic silencing ( Choi et al 2011 ; Yang et al 2017 ; Antoniou-Kourounioti et al 2018 ; Qüesta et al 2020 ), allowing the fine-tuning of AtFLC expression by environmental cues.…”