Altered H3K27 trimethylation contributes to flowering time variations in polyploid Arabidopsis thaliana ecotypes

Polyploidy is a widespread phenomenon in flowering plant species. Polyploid plants frequently exhibit considerable transcriptomic alterations after whole-genome duplication (WGD). It is known that the transcriptomic response to tetraploidization is ecotype-dependent in Arabidopsis. Nevertheless, the biological significance and the underlying mechanism are unknown. Here, we showed that 4x Col-0 and 4x Ler presented different flowering times, with a delayed flowering time in 4x Col-0 but not in 4x Ler. We found that the expression of FLOWERING LOCUS C (FLC), the major repressor of flowering, was significantly increased in 4x Col-0 but subtle change in 4x Ler. Moreover, the level of a repressive epigenetic mark, trimethylation of histone H3 at lysine 27 (H3K27me3), was significantly decreased in 4x Col-0 but not in 4x Ler, potentially leading to different transcription levels of FLC and flowering time in 4x Col-0 and 4x Ler. Apart from the FLC locus, hundreds of genes showed differentially H3K27me3 alterations in 4x Col-0 and 4x Ler. Comparably, LIKE HETEROCHROMATIN PROTEIN 1 (LHP1) and transcription factors required for H3K27me3 deposition presented differential transcriptional changes between 4x Col and Ler, potentially account for differential H3K27me3 alterations in 4x Col-0 and Ler. Last, we found that the natural 4x Arabidopsis ecotype Wa-1 presented early flowering time, associated with low expression and high H3K27me3 of FLC. Taken together, our results showed a role of H3K27me3 alterations in response to genome duplication in Arabidopsis autopolyploids and that flowering time variation potentially functions in autopolyploid speciation. We compared the transcriptomes and genome profiles of H3K27me3 for diploid and tetraploid Col-0 and Ler