Altered chromatin conformation and transcriptional regulation in watermelon following genome doubling

Abstract

Polyploidy has played a crucial role in plant evolution, development and function. Synthetic autopolyploid represents an ideal system to investigate the effects of polyploidization on transcriptional regulation. In this study, we deciphered the impact of genome duplication at phenotypic and molecular levels in watermelon. Overall, 88% of the genes in tetraploid watermelon followed a >1:1 dosage effect, and accordingly, differentially expressed genes were largely upregulated. In addition, a great number of hypomethylated regions (1688) were identified in an isogenic tetraploid watermelon. These differentially methylated regions were localized in promoters and intergenic regions and near transcriptional start sites of the identified upregulated genes, which enhances the importance of methylation in gene regulation. These changes were reflected in sophisticated higher-order chromatin structures. The genome doubling caused switching of 108 A and 626 B compartments that harbored genes associated with growth, development and stress responses.

Polyploidy as a Fundamental Phenomenon in Evolution, Development, Adaptation and Diseases

“…Detaching from the NL and moving inside the nucleus, LADs contribute to the opening of chromatin [ 123 ]. This is in agreement with the fact that the upregulation is stronger than the downregulation in the ploidy-associated changes in gene expression [ 126 ].…”

“…Accordingly, the association between polyploidy and chromatin decompactization under stress was well documented for cardiomyocytes and hepatocytes [ 76 , 128 ]. At the lower levels of genome organization, polyploidy can alter global patterns of DNA methylation, microRNA expression, and histone modification in mammal, insect, and plant cells [ 1 , 2 , 98 , 126 , 129 , 130 ]. Polyploid cells show higher expression of bivalent genes, which harbor both activating (H3K4me3) and repressive (H3K27me3) chromatin domains [ 78 , 112 ].…”

A Comparative Study of Morphology, Photosynthetic Physiology, and Proteome between Diploid and Tetraploid Watermelon (Citrullus lanatus L.)

“…In watermelon, in addition to a larger fruit size, the leaves, stem width, and staminate flowers of tetraploid watermelon (CLT1) were larger than those of diploid plants (CLD1) [ 31 ]. In another study, it was found that chromosome doubling enhanced seed size, cotyledon size, stem thickness, and trichome density and length [ 32 ]. Furthermore, there were differences in lycopene and hormone content between tetraploid and diploid watermelon during the fruit development stage; tetraploid watermelon contained more lycopene and IAA than the diploid genotype [ 33 ].…”

Polyploidy and Myc Proto-Oncogenes Promote Stress Adaptation via Epigenetic Plasticity and Gene Regulatory Network Rewiring

“…Chromatin regions transitioning from B to A are strongly enriched for heart developmental genes upregulated during human and mouse cardiogenesis and in cardiac differentiation of hPSCs [ 105 ]. Accordingly, data obtained from synthetic autotetraploid plants (watermelon, soybean, and Arabidopsis) also indicate that polyploidy shifts the A-to-B chromatin balance toward the actively transcribed A-chromatin [ 106 , 107 ]. Moreover, recent studies provide evidence that genome duplications reorganize topologically associated domains (TAD) packaged within A- and B-chromatin compartments via the increase in intra-TAD interaction and reorganization of chromatin loops [ 106 , 108 ].…”