Repressive chromatin modification underpins the long-term expression trend of a perennial flowering gene in nature

• Published in: Nature communications Vol. 11; no. 1; pp. 2065 - 12
• Main Authors: Nishio, Haruki, Buzas, Diana M., Nagano, Atsushi J., Iwayama, Koji, Ushio, Masayuki, Kudoh, Hiroshi
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.05.2020; Nature Publishing Group; Nature Portfolio
• Subjects: 38/15; 38/39; 38/77; 38/90; 631/208/176; 631/449/1659; 631/449/2668; 631/449/2679/2681; Arabidopsis - genetics; Arabidopsis - physiology; Arabidopsis Proteins - genetics; Chromatin; Chromatin - chemistry; Epigenesis, Genetic; Flowering; Flowers - genetics; Flowers - physiology; Gene expression; Gene Expression Regulation, Plant; Histone Code; Histones; Histones - metabolism; Humanities and Social Sciences; Japan; Life cycles; MADS Domain Proteins - genetics; multidisciplinary; Natural environment; Science; Science (multidisciplinary); Seasonal variations; Seasons; Temperature; Trends; Japan
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-020-15896-4

Natural environments require organisms to possess robust mechanisms allowing responses to seasonal trends. In Arabidopsis halleri , the flowering regulator AhgFLC shows upregulation and downregulation phases along with long-term past temperature, but the underlying machinery remains elusive. Here, we investigate the seasonal dynamics of histone modifications, H3K27me3 and H3K4me3, at AhgFLC in a natural population. Our advanced modelling and transplant experiments reveal that H3K27me3-mediated chromatin regulation at AhgFLC provides two essential properties. One is the ability to respond to the long-term temperature trends via bidirectional interactions between H3K27me3 and H3K4me3; the other is the ratchet-like character of the AhgFLC system, i.e. reversible in the entire perennial life cycle but irreversible during the upregulation phase. Furthermore, we show that the long-term temperature trends are locally indexed at AhgFLC in the form of histone modifications. Our study provides a more comprehensive understanding of H3K27me3 function at AhgFLC in a complex natural environment. The flowering regulator FLC shows upregulation and downregulation phases along with long-term past temperature in Arabidopsis halleri . Here, the authors reveal that H3K27me3-mediated chromatin regulation at AhgFLC provides the ability to respond to both the seasonal temperature trends and the perennial life cycle.