Altered chromatin confirmation and transcriptional regulation in watermelon following genome doubling

Authors: GARCIA-LOZANO, MARLENY - West Virginia State University; NATARAJAN, PURUSHOTHAMAN - West Virginia State University; Levi, Amnon; KATAM, RAMESH - West Virginia State University; NIMMAKAYALA, PADMA - West Virginia State University; REDDY, UMESH - West Virginia State University

Submitted to: Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/26/2021
Publication Date: 3/31/2021
Citation: Garcia-Lozano, M., Natarajan, P., Levi, A., Katam, R., Nimmakayala, P., Reddy, U. 2021. Altered chromatin confirmation and transcriptional regulation in watermelon following genome doubling. Plant Journal. https://doi.org/10.1111/tpj.15256.
DOI: https://doi.org/10.1111/tpj.15256

Interpretive Summary: In the last two decades there has been an increased demand for high quality seedless watermelon varieties. However, the process of developing seedless watermelons is highly involved and demands special efforts from seed company breeders. The seedless watermelon is a triploid hybrid plant (having three sets of chromosomes per cell). It is created by crossing a diploid (having the standard two sets of chromosomes per cell) with a tetraploid watermelon plant (having four sets of chromosomes per cell). The resulting triploid is the plant that produces the seedless watermelon seeds. To date, there is little knowledge on the events that take place in the genome of diploid versus triploid or tetraploid watermelon plants. Here, an ARS scientist at the U.S. Vegetable Laboratory (Charleston SC) have collaborated with a team of scientists at West Virginia State University on elucidating the events that take place in the genome of diploid versus triploid and tetraploid watermelons. They found significant differences in gene expression, whereas many genes that typically have low level of expression in the diploid plants have higher expression levels in tetraploid plants. On the other hand, some other genes that are highly expressed in the diploid plants showed relatively lower levels of expression in the tetraploid plants. The results of this study indicate that gene expression and interaction greatly vary between diploid triploid and tetraploid plants that contain the same genome. These results should be useful for researchers and plant breeders interested in developing and improving triploid seedless watermelon varieties.

Technical Abstract: Polyploidy has played a crucial role in plant evolution, development, and function. Autopolyploids represent ideal systems to investigate the effect of polyploidization on transcriptional regulation, although this research is limited. In this study, we deciphered the impact of genome duplication at phenotypic and molecular levels in watermelon. 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 (1,688) were identified in 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.