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Genomic history and ecology of the geographic spread of rice

Abstract

Rice (Oryza sativa) is one of the world’s most important food crops, and is comprised largely of japonica and indica subspecies. Here, we reconstruct the history of rice dispersal in Asia using whole-genome sequences of more than 1,400 landraces, coupled with geographic, environmental, archaeobotanical and paleoclimate data. Originating around 9,000 yr ago in the Yangtze Valley, rice diversified into temperate and tropical japonica rice during a global cooling event about 4,200 yr ago. Soon after, tropical japonica rice reached Southeast Asia, where it rapidly diversified, starting about 2,500 yr bp. The history of indica rice dispersal appears more complicated, moving into China around 2,000 yr bp. We also identify extrinsic factors that influence genome diversity, with temperature being a leading abiotic factor. Reconstructing the dispersal history of rice and its climatic correlates may help identify genetic adaptations associated with the spread of a key domesticated species.

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Fig. 1: Factors underlying geographic distribution of genomic diversity in japonica and indica.
Fig. 2: Subpopulations of japonica and indica rice.
Fig. 3: Demographic, paleoenvironmental and archaeological context of temperate japonica rice emergence.
Fig. 4: Proposed dispersal map of japonica rice in Asia.
Fig. 5: Proposed dispersal map of indica rice in Asia.

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Data availability

Raw FASTQ reads for 178 accessions whose genomes were resequenced for this study have been deposited in the SRA under Bioproject accession numbers PRJNA422249 and PRJNA557122. Sources for all downloaded data are referred to in the Supplementary Information.

Code availability

Code repositories are available at: https://github.com/bocinsky/gutaker2020, https://github.com/grafau/discretize, https://github.com/grafau/NextGatkSNPs and https://github.com/em-bellis/riceTravelTime.

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Acknowledgements

We thank our colleagues for helpful discussions on this project. This work was supported in part by Zegar Family Foundation grant A16-0051-004 and US National Science Foundation Plant Genome Research Program grant IOS-1546218 to M.D.P., Portugal Fundação para a Ciência e a Tecnologia grant EXPL/BIA-BIC/0947/2012 to S.N., SFRH/BD/68835/2010 to I.S.P. and UID/Multi/04551/2013 to M.M.O., Gordon and Betty Moore Foundation and Life Sciences Research Foundation grant GBMF2550.06 to S.C.G., US National Science Foundation grant PRFB 1711950 to E.S.B., Natural Environment Research Council UK grant NE/N010957/1 to C.C.C. and D.Q.F., US National Science Foundation grant BCS-1632207 to J.A.d.G. and United States Department of Agriculture and National Institute of Food and Agriculture grant 2019-67009-29006 to J.R.L.

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Authors and Affiliations

Authors

Contributions

R.M.G. and M.D.P. conceived and designed the study with input from J.R.L. and S.C.G. J.Y.C., I.S.P. and O.W. generated sequencing data. M.D.P., S.N. and M.M.O. supervised laboratory work. R.M.G. assembled and processed the sequencing data. S.C.G. and E.S.B. assembled and processed the environmental data with input from J.R.L. J.R.L. led the spatial analyses with input from R.M.G. E.S.B. and E.R.S. carried out travel-time analyses with input from J.R.L. J.R.L. carried out R.D.A. analyses. R.M.G. carried out population-structure, admixture-graph and coalescence analyses. R.K.B. and J.A.d.G. conducted thermal-niche modelling. D.Q.F., C.C.C. and J.A.d.G. provided archaeological context. M.D.P., R.M.G. and J.R.L. wrote the manuscript with input from all authors.

Corresponding authors

Correspondence to Jesse R. Lasky or Michael D. Purugganan.

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The authors declare no competing interests.

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Peer review information Nature Plants thanks Laura Botigué and Angé́lica Cibrián-Jaramillo and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–24.

Reporting Summary

Supplementary Video 1

Spatio-temporal distribution of rice thermal niche. Video illustrating the probability of rice being in niche based on the minimum and maximum growing degree days requirement for tropical japonica landraces. Map of Asia with plotted thermal niche probabilities, colour-coded as indicated below the map. White lines denote the border under which niche probability drops below 75%. Below the map is a plot of probabilities averaged across spatial scale. The thick black line represents mean, thin lines show interquartile range, and grey shaded area represents 25% to 75% probability of being in the thermal niche (n = 477,708 cells). The thin black lines are the mean probabilities of being in the thermal niche across the study area when modelled using the 1σ uncertainty intervals as provided by the Northern Hemisphere temperature reconstruction (n = 73 datasets)40. Moving vertical red line indicates time before present.

Supplementary Table 1

Supplementary Tables 1–3.

Source data

Source Data Fig. 1

Geographic coordinates, migration data, statistical data and Canonical coordinates.

Source Data Fig. 2

Dimension (MDS) coordinates, country codes and graph dot format.

Source Data Fig. 3

Statistical data points, geographic coordinates, graph trajectories, statistical data and raster data.

Source Data Fig. 4

Geographic coordinates and statistical data.

Source Data Fig. 5

Geographic coordinates and statistical data.

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Gutaker, R.M., Groen, S.C., Bellis, E.S. et al. Genomic history and ecology of the geographic spread of rice. Nat. Plants 6, 492–502 (2020). https://doi.org/10.1038/s41477-020-0659-6

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