A Genome Doubling Event Reshapes Rice Morphology and Products by Modulating Chromatin Signatures and Gene Expression Profiling

Abstract

Evolutionarily, polyploidy represents a smart method for adjusting agronomically important in crops through impacts on genomic abundance and chromatin condensation. Autopolyploids have a relatively concise genetic background with great diversity and provide an ideal system to understand genetic and epigenetic mechanisms attributed to the genome-dosage effect. However, whether and how genome duplication events during autopolyploidization impact chromatin signatures are less understood in crops. To address it, we generated an autotetraploid rice line from a diploid progenitor, Oryza sativa ssp. indica 93-11. Using transposase-accessible chromatin sequencing, we found that autopolyploids lead to a higher number of accessible chromatin regions (ACRs) in euchromatin, most of which encode protein-coding genes. As expected, the profiling of ACR densities supported that the effect of ACRs on transcriptional gene activities relies on their positions in the rice genome, regardless of genome doubling. However, we noticed that genome duplication favors genic ACRs as the main drivers of transcriptional changes. In addition, we probed intricate crosstalk among various kinds of epigenetic marks and expression patterns of ACR-associated gene expression in both diploid and autotetraploid rice plants by integrating multiple-omics analyses, including chromatin immunoprecipitation sequencing and RNA-seq. Our data suggested that the combination of H3K36me2 and H3K36me3 may be associated with dynamic perturbation of ACRs introduced by autopolyploidization. As a consequence, we found that numerous metabolites were stimulated by genome doubling. Collectively, our findings suggest that autotetraploids reshape rice morphology and products by modulating chromatin signatures and transcriptional profiling, resulting in a pragmatic means of crop genetic improvement.

Allele‐specific expression and chromatin accessibility contribute to heterosis in tea plants (Camellia sinensis)

“…The number of ACRs and the total sequence length of the hybrids were significantly larger than those of the parents, indicating more robust chromatin accessibility of the hybrid genomes. By comparing the ATAC-seq data of multiple plant genomes reported previously (Lu et al, 2019;Schwope et al, 2021;Zhou et al, 2021), the genome proportion of ACRs in tea plants was much lower than that of plants with smaller genomes such as Spirodela polyrhiza, Arabidopsis thaliana, Eutrema salsugineum and Vitis vinifera, but higher than that of Hordeum vulgare (Figure 4b). We further examined the distribution of ACRs in the tea plant genome and classified them as gACRs (genic ACRs in exons, introns and UTRs), pACRs (proximal ACRs within 2 kb upstream of the TSS and 2 kb downstream of the TTS) and dACRs (distal ACRs in the intergenic).…”

Genome-wide chromatin accessibility analysis unveils open chromatin convergent evolution during polyploidization in cotton

“…This hypothesis is supported by several studies in plants. For example, a study in rice showed that induced chromatin accessibility leads to preferential recruitment of H3K36me2 and H3K36me3 ( 89 ). In Arabidopsis , genome duplication can contribute to the switching of some loose and compact structural domains and altered H3K4me3 and H3K27me3 modification ( 90 ).…”

Autotetraploidy of rice does not potentiate the tolerance to drought stress in the seedling stage

“…Wang et al ( 2021 ) found that polyploidy induces DNA hypomethylation and salt stress-induced hypermethylation to repress proximal TEs and/or TE-associated stress-responsive genes in 4X of two japonica varieties (Wang et al 2021 ). Autopolyploids lead to a higher number of accessible chromatin regions (ACRs) in euchromatin, and modulate chromatin signatures and transcriptional profiling (Zhou et al 2021 ). The results suggested that chromosome doubling magnified genomic instability, epigenetic variability and chromatin accessibility.…”