Nuclear Organization Changes and the Epigenetic Silencing of FLC during Vernalization

Abstract

Changes in nuclear organization are considered an important complement to trans-acting factors, histone modifications and non-coding RNAs in robust and stable epigenetic silencing. However, how these multiple layers interconnect mechanistically to reinforce each other's activity is still unclear. A system providing long timescales facilitating analysis of these interconnections is vernalization. This involves the Polycomb-mediated epigenetic silencing of flowering locus C (FLC) that occurs as Arabidopsis plants are exposed to prolonged cold. Analysis of changes in nuclear organization during vernalization has revealed that disruption of a gene loop and physical clustering of FLC loci are part of the vernalization mechanism. These events occur at different times and thus contribute to distinct aspects of the silencing mechanism. The physical clustering of FLC loci is tightly correlated with the accumulation of specific Polycomb complexes/H3K27me3 at a localized intragenic site during the cold. Since the quantitative nature of vernalization is a reflection of a bistable cell autonomous switch in an increasing number of cells, this correlation suggests a tight connection between the switching mechanism and changes in nuclear organization. This integrated picture is likely to be informative for many epigenetic mechanisms.

Light signaling controls nuclear architecture reorganization during seedling establishment

“…Although we cannot exclude that expression of the LTR AtGP1 transgene could also be controlled by trans-acting factors superimposing RdDM-based repression, two-layered silencing has nonetheless been identified using mutant plants for the Morpheus' molecule1 (MOM1) putative helicase (70,71) and for the MORC ATPase (72), which are both believed to be involved in DNA or chromosomal remodeling processes. Based on these findings, it is possible that some heterochromatin loci might be sensitive to a position-dependent or condensation-dependent regulatory control during cotyledon development, a process that may relate to the observed relationship between chromatin-based repression and subnuclear positioning of multicopy transgenes (73) and of the FLC gene (66,74). Future studies aimed at dissecting nuclear architectural changes during photomorphogenesis should allow an assessment of the functional impact of heterochromatin organization and genome topology structuration on the reprogramming of gene expression.…”

DNA Topoisomerase Iα Affects the Floral Transition

“…Many studies have reported the involvement of histone modifications in regulating the expression of FLC and MAFs (Ausín et al, 2004;Kim et al, 2004;Sung and Amasino, 2004;Greb et al, 2007;Jiang et al, 2008Jiang et al, , 2009Buzas et al, 2011;He, 2012;Jégu et al, 2014;Shen et al, 2014;Zhu et al, 2015). Posttranslational modifications of RNA polymerase II components, whose recruitment is mediated by TOP1a, also contribute to histone modifications as transcription proceeds (Egloff and Murphy, 2008;Spain and Govind, 2011).…”

Epigenetic Regulation in Plants

“…SWI/SNF chromatin-remodelling complex BAF60 seems to be required for the formation of the FLC gene loop and the disruption of the loop seems to facilitate enhanced COOLAIR expression during cold. Zhu et al (2014) observed in addition a more long-range restructuring of chromatin in the FLC context. They visualised in vivo position of lacO-tagged FLC via YFP-LACI and could show a condensation of FLC during vernalisation indicating a physical clustering.…”