Pan-genome inversion index reveals evolutionary insights into the subpopulation structure of Asian Rice (Oryza sativa)

Authors: ZHOU, YONG - King Abdullah University Of Science And Technology; YU, ZHICHAO - Huazhong Agricultural University; CHEBOTAROV, DMYTRO - International Rice Research Institute; CHOUGULE, KAPEEL - Cold Spring Harbor Laboratory; LY, ZHENYUAN - Cold Spring Harbor Laboratory; RIVERA, LUIS - King Abdullah University Of Science And Technology; KATHIRESAN, NAGARAJAN - King Abdullah University Of Science And Technology; AL-BADER, NOOR - King Abdullah University Of Science And Technology; MOHAMMED, NAHED - King Abdullah University Of Science And Technology; ALSANTELY, ASEEL - King Abdullah University Of Science And Technology; MUSSUROVA, SAULE - King Abdullah University Of Science And Technology; SANTOS, JOAO - King Abdullah University Of Science And Technology; THIMMA, MANJULA - King Abdullah University Of Science And Technology; TROUKHAN, MAXIM - Sensors & Software, Inc; FORNASIERO, ALICE - King Abdullah University Of Science And Technology; GREEN, CARL - University Of Arizona; COPETTI, DARIO - University Of Arizona; KUDRNA, DAVE - University Of Arizona; LLACA, VICTOR - Corteva Agriscience; LORIEUX, MATIAS - University Of Montpellier; ZUCCOLO, ANDREA - King Abdullah University Of Science And Technology; Ware, Doreen; MCNALLY, KENNETH - International Rice Research Institute; ZHANG, JIANWEI - Huazhong Agricultural University; WING, ROD - King Abdullah University Of Science And Technology; KUDRNA, DAVE - University Of Arizona

Submitted to: Nature Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/20/2022
Publication Date: 3/21/2023
Citation: Zhou, Y., Yu, Z., Chebotarov, D., Chougule, K., Ly, Z., Rivera, L.F., Kathiresan, N., Al-Bader, N., Mohammed, N., Alsantely, A., Mussurova, S., Santos, J., Thimma, M., Troukhan, M., Fornasiero, A., Green, C., Copetti, D., Kudrna, D., Llaca, V., Lorieux, M., Zuccolo, A., Ware, D., McNally, K., Zhang, J., Wing, R., Kudrna, D. 2023. Pan-genome inversion index reveals evolutionary insights into the subpopulation structure of Asian Rice (Oryza sativa). Nature Genetics. 14:1567. https://doi.org/10.1038/s41467-023-37004-y.
DOI: https://doi.org/10.1038/s41467-023-37004-y

Interpretive Summary: Genetic diversity is important for stable production of crops, including rice. The researchers used 16 rice genomes plus two genomes of close wild rice relatives (0. rufipogon and 0. punctata) in a search for sources of diversity to help create new varieties of rice that are sustainable, nutritious and climate resilient. One way to discover new sources of genetic diversity is to look at the other forms of a gene (alleles) at a given location (locus). These changes in the genetic code can include insertions, deletions, inversions, and transpositions. Inversions, the focus of this study, are complete reversals of a segment of DNA end to end. They are understudied in rice and the inversions that have been studied are small or mid-sized. The researchers built an index of 1,054 unique inversions that comprise about 14% of the Asian rice reference genome. Using this index they estimated that the rate of inversion in Asian rice is 1,100 inversions per million years, which is 37 to 73 times higher than previously estimated for plants. As the researchers further explored these inversions, they discovered that large inversions in particular had a connection with crop performance.

Technical Abstract: Understanding and exploiting genetic diversity is a key factor for the productive and stable production of rice. Utilizing 16 high-quality genomes that represent the subpopulation structure of Asian rice (O. sativa), plus the genomes of two close relatives (O. rufipogon and O. punctata), we built a pan-genome inversion index of 1,054 non-redundant inversions that span an average of ~ 14% of the O. sativa cv. Nipponbare reference genome sequence. Using this index we estimated an inversion rate of 1,100 inversions per million years in Asian rice, which is 37 to 73 times higher than previously estimated for plants. Detailed analyses of these inversions showed evidence of their effects on gene regulation, recombination rate, linkage disequilibrium and agronomic trait performance. Our study uncovers the prevalence and scale of large inversions (= 100 kb) across the pan-genome of Asian rice, and hints at their largely unexplored role in functional biology and crop performance.