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One of the most attractive challenges in current biology is to understand organismal functions in natural environments. It is important because any functions should operate and have evolved in the natural context of environments. I will present the results of our long-term study on molecular phenology of Arabidopsis halleri subsp. gemmifera in its natural populations with special emphasis on flowering-time controls. We conducted ‘molecular phenology’ studies on A. halleri Flowering Locus C (AhgFLC), a homolog of the key flowering repressor in the vernalization pathway. By analysing the relationship between the gene expression and past temperature, we revealed that this key gene for flowering-time control is regulated in response to temperature over the past six weeks. Furthermore, we conducted seasonal transcriptome analyses using in the
natural population for two years, by visiting the field site at weekly intervals. Approximately 15%-20% of analysed genes showed seasonal patterns. In particular, flowering time, circadian clock, and defence related-genes had specific seasonal patterns. In our field analyses on histone modifications, delayed seasonal changes of H3K27me3 from those of H3K4me3 were observed at many genes, and amongst these genes, H3K27me3 behaved as a mechanism to track past transcriptional activities. Among them, AhgFLC, was characterized by the largest delay of H3K27me3 from H3K4me3. Two-year high-frequency ChIP-qPCR analyses identified unidirectional changes of H3K27me3 between the transcription start site and gene body regions of AhgFLC. This unidirectional change of H3K27me3 serve as a mechanism for unidirectional transitions of plant life stages in a seasonal environment. In conclusion, one of the
major roles of H3K27me3 is the robust control of seasonal gene expression under the fluctuating natural conditions.
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