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Comparative evolutionary genetics of deleterious load in sorghum and maize

Abstract

Sorghum and maize share a close evolutionary history that can be explored through comparative genomics1,2. To perform a large-scale comparison of the genomic variation between these two species, we analysed ~13 million variants identified from whole-genome resequencing of 499 sorghum lines together with 25 million variants previously identified in 1,218 maize lines. Deleterious mutations in both species were prevalent in pericentromeric regions, enriched in non-syntenic genes and present at low allele frequencies. A comparison of deleterious burden between sorghum and maize revealed that sorghum, in contrast to maize, departed from the domestication-cost hypothesis that predicts a higher deleterious burden among domesticates compared with wild lines. Additionally, sorghum and maize population genetic summary statistics were used to predict a gene deleterious index with an accuracy greater than 0.5. This research represents a key step towards understanding the evolutionary dynamics of deleterious variants in sorghum and provides a comparative genomics framework to start prioritizing these variants for removal through genome editing and breeding.

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Fig. 1: Population structure and LD patterns in sorghum.
Fig. 2: Comparative analysis of deleterious alleles in sorghum and maize.
Fig. 3: Genomic landscape of sorghum.
Fig. 4: CNN architecture.

Data availability

The raw sequencing data for the TERRA-MEPP lines are available through the NCBI BioProject PRJNA513297. The raw data for Mace et al.5 are available through the BioProject PRJNA182489. The TERRA-REF raw data are available through the data commons database at CyVerse: http://datacommons.cyverse.org/browse/iplant/home/shared/terraref. The gene expression raw data are available through the BioProject PRJNA503076. The SIFT raw results and VCF files, among others, are available through the CyVerse repository: (http://datacommons.cyverse.org/browse/iplant/home/shared/GoreLab/dataFromPubs/Lozano_MaizeSorghum_2019).

Code availability

The code used throughout the article is available at the GitHub repository: https://github.com/GoreLab/Sorghum-HapMap

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Acknowledgements

We thank J. Schnable for the maize, sorghum and setaria orthologue lists. We also thank the Ross-Ibarra lab at UC Davis for helpful comments and sound advice on an earlier draft of this manuscript. We thank J. Grimwood and J. Schmutz at the HudsonAlpha Institute for the sequencing of the included TERRA-REF lines. The information, data or work presented herein was funded in part by the Advanced Research Projects Agency-Energy (ARPA-E), US Department of Energy, under Award Numbers DE-AR0000598, DE-AR0000661 and DE-AR0000594. This work was also supported by the United States Department of Agriculture–Agricultural Research Service (USDA–ARS). The views and opinions of the authors expressed herein do not necessarily state or reflect those of the United States government or any agency thereof. This work was also supported by the Next-Generation BioGreen 21 Program (Project No. PJ01321305), Rural Development Administration, Republic of Korea. For J.P.R.d.S., this work was partially supported by FAPESP grant nos 2017/03625-2 and 2017/25674-5 / CAPES (São Paulo Research Foundation) Finance Code 001 / Conselho Nacional de Desenvolvimento Cientıfico e Tecnológico (CNPq).

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Authors

Contributions

R.L., E.G., E.S.B., J.R.-I. and M.A.G. designed the project and all the experiments. R.L. and J.P.R.d.S. performed the CNN analysis. R.L. and E.G. performed the bioinformatic analysis. M.G.S. performed the burden simulation analysis. R.V. and N.B. performed the transcriptome analysis. S.B.F., N.S., T.C.M., E.A.C. and P.J.B. contributed the plant material. M.T.P. constructed the genomic libraries for sequencing the 14 S. bicolor subsp. verticilliflorum accessions. P.J.B., N.S., T.C.M., E.S.B., J.R.-I. and M.A.G. contributed the whole-genome sequence data. R.L., E.G., M.G.S., J.P.R.d.S., R.V., S.B.F., J.R.-I. and M.A.G. analysed the data. R.L. prepared the figures and together with M.A.G. and J.R.-I. wrote the manuscript. All authors provided critical insights and read and approved the manuscript.

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Correspondence to Jeffrey Ross-Ibarra or Michael A. Gore.

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The authors declare no competing interests.

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Peer review information Nature Plants thanks Xuehui Huang and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Lozano, R., Gazave, E., dos Santos, J.P.R. et al. Comparative evolutionary genetics of deleterious load in sorghum and maize. Nat. Plants 7, 17–24 (2021). https://doi.org/10.1038/s41477-020-00834-5

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