Comparison of Oryza sativa and Oryza brachyantha genomes reveals selection-driven gene escape from the centromeric regions

Authors: LIAO, YI - Beijing Academy Of Agricultural Sciences; ZHANG, XUEMEI - Beijing Academy Of Agricultural Sciences; LI, BO - Beijing Academy Of Agricultural Sciences; LIU, TIEYAN - Beijing Academy Of Agricultural Sciences; CHEN, JINFENG - Beijing Academy Of Agricultural Sciences; BAI, ZETAO - Beijing Academy Of Agricultural Sciences; WANG, MEIJIAO - Beijing Academy Of Agricultural Sciences; SHI, JINFENG - Beijing Academy Of Agricultural Sciences; Walling, Jason; WING, ROD - Arizona Genomics Institute; JIANG, JIMING - University Of Wisconsin; CHEN, MINGSHENG - Beijing Academy Of Agricultural Sciences

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/28/2018
Publication Date: 7/1/2018
Citation: Liao, Y., Zhang, X., Li, B., Liu, T., Chen, J., Bai, Z., Wang, M., Shi, J., Walling, J.G., Wing, R., Jiang, J., Chen, M. 2018. Comparison of Oryza sativa and Oryza brachyantha genomes reveals selection-driven gene escape from the centromeric regions. The Plant Cell. https://doi.org/10.1105/tpc.18.00163.
DOI: https://doi.org/10.1105/tpc.18.00163

Interpretive Summary: Understanding how genes evolve through speciation and how, in turn, these genes might be gained, lost, turned on, or turned off is critical to our understanding of functional genetics. Why is it that in some species genes exist that allow a plant or animal to exhibit a particular trait, good or bad, while in other species they are lost? To understand these very basic questions is truly fundamental to our ability to leverage this knowledge toward improvement of human health and ecology. The study presented here provides great insight into such a phenomenon by exploring the evolution of genes and tracking their presence and activity within a unique region of the genome: the centromere of a chromosome; a genetic element that is of critical importance toward ensuring proper and mistake-free cell division. Both plants and animals have centromeres, including humans where centromere integrity is paramount for human health and development. Compromised centromeres can lead to “mistakes” during cell division and is especially devastating when the misdivision occurs early in human development which can typically result in congenital disorders, e.g. trisomy. Therefore, increasing our understanding of centromere structure and function, even in plants, will provide clues as to how these structures provide faithful governance over correct cell division in humans. Using state-of-the-art genetic tools, we were able to provide an incredibly robust analysis of gene movement within and around the centromeres of rice chromosomes. We choose to use the cereal grain rice (Oryza) as the subject of interrogation. It’s well known that rice is a major source of carbohydrate nutrition world-wide and efforts to increase the utility of this plant are in great demand. Through characterizing the genetic composition of rice and then comparing it to the genetic composition of rice’s wild relatives, we were able to impact the current state of genomic and chromosomal science by: 1) providing a precise account of how genes might move around the genome and how the function of these genes depends on such movement, 2) hunting for unique/favorable alleles or genes found in wild species that are missing from the rice we grow and eat and 3) elucidating the structure and dynamics of the centromere region and how, together with the genes they harbor, they can evolve and respond to speciation.

Technical Abstract: In genomes of higher eukaryotes, centromeres are commonly located in or near regions of repetitive DNA. These regions are vastly underrepresented in whole genome assemblies, thus preventing the pursuit of in-depth evolutionary and genomic analyses within such regions. Here, we report a 12.3 Mb high-quality BAC-based sequence within the pericentromeric regions of a wild rice species, O. brachyantha, which diverged from rice (O. sativa) ~15 Mya (million years ago). Using genome assemblies within the genus Oryza together with closely related grass species, we conducted comprehensive syntenic and phylogenomic analyses of the centromeric regions from all rice chromosomes. Six and twelve pericentric inversions were identified in O. sativa and O. brachyantha, respectively. Centromere movements between rice and O. brachyantha were mainly caused by inversions, which were easily detected on chromosomes 1, 7 and 9. A clear centromere repositioning event was identified in which the ancestral centromere of chromosome 12 in O. brachyantha “jumped” ~ 400kb away, possibly mediated by a duplicated transposition (>28kb). More strikingly, we observed an excess of genes moving out of centromeric regions (P < 2.2×10-16). Such movement could be explained by selective loss of the parental copy within or near centromeric regions after gene duplication, which strongly supports the view that centromeres are bad neighborhoods for genes. Overall, our results highlight the power of high quality assembly and phylogenomic approach to understand the centromere evolution. The improved assembly will further facilitate centromere studies in the genus Oryza.