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Stepwise selection on homeologous PRR genes controlling flowering and maturity during soybean domestication

Abstract

Adaptive changes in plant phenology are often considered to be a feature of the so-called ‘domestication syndrome’ that distinguishes modern crops from their wild progenitors, but little detailed evidence supports this idea. In soybean, a major legume crop, flowering time variation is well characterized within domesticated germplasm and is critical for modern production, but its importance during domestication is unclear. Here, we identify sequential contributions of two homeologous pseudo-response-regulator genes, Tof12 and Tof11, to ancient flowering time adaptation, and demonstrate that they act via LHY homologs to promote expression of the legume-specific E1 gene and delay flowering under long photoperiods. We show that Tof12-dependent acceleration of maturity accompanied a reduction in dormancy and seed dispersal during soybean domestication, possibly predisposing the incipient crop to latitudinal expansion. Better understanding of this early phase of crop evolution will help to identify functional variation lost during domestication and exploit its potential for future crop improvement.

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Fig. 1: Characterization and GWAS for flowering time in soybean diversity panels.
Fig. 2: Genetic and regulatory interactions of Tof11, Tof12 and E1.
Fig. 3: Tof11 and Tof12 promote E1 transcription through direct downregulation of LHY genes.
Fig. 4: Model summarizing the mechanism of Tof11 and Tof12 action under LD conditions.
Fig. 5: Stepwise selection on Tof12 and Tof11 during soybean evolution.

Data availability

The sequencing data used in this study have been deposited into the Genome Sequence Archive (GSA) database in BIG Data Center (http://gsa.big.ac.cn/index.jsp) under accession number PRJCA001691 and into the NCBI database under accession number PRJNA608146. The previously reported sequence data were deposited into the NCBI database under accession number SRP045129 and into the GSA database in BIG Data Center under accession number PRJCA000205. Source data for Fig. 3 are provided with the paper.

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Acknowledgements

This work was supported by the National Key Research and Development Program (grant no. 2016YFD0100401 to F.K.), National Natural Science Foundation of China (grant nos 31725021, 31571686 and 31701445 to F.K., 31930083 to B.L. and 31801384 to S. Lu) and the National Key Research and Development Program (grant nos 2017YFE0111000 to F.K. and 2016YFD0101900 to X.Z.).

Author information

Authors and Affiliations

Authors

Contributions

F.K. coordinated the project, and designed and interpreted experiments with input from J.L.W., S. Lu, L.D., C.F., S. Liu, L.K., Q.C., L.C., T.S., H.N., D.Z., L.Z., Z.W. and Y.Y. performed the experiments. X. Liu., Q.Y., D.Y., Q.X., X. Lin., X. Yang, C.T., X. Li., Y.T., X.Z., X. Yuan, Z.T., B.L. and F.K. performed the data analysis. F.K. and J.L.W. wrote the manuscript.

Corresponding authors

Correspondence to Xiaohui Yuan, Zhixi Tian, Baohui Liu, James L. Weller or Fanjiang Kong.

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The authors declare no competing interests.

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Extended data

Extended Data Fig. 1 Flowering time and maturity variations in 424 accessions.

424 accessions (85 wild soybeans, 153 landraces and 186 improved cultivars) were recorded in 2018 in Zhengzhou and Hefei, in 2019 in Harbin, Zhengzhou, Wuhan and Guangzhou, China. Average flowering time of 85 wild soybeans, 153 landraces and 186 improved cultivars in Zhengzhou 2018 a, Hefei 2018 b and average maturity in Zhengzhou 2018 c, Hefei 2018 d. Average flowering time of 85 wild soybeans, 153 landraces and 186 improved cultivars in Guangzhou 2019 e, Wuhan 2019 f, Zhengzhou 2019 g and Harbin 2019 h. Some wild soybeans in Harbin were unable to flower at the end season and were treated as 130d (entire growth period). In a-h, the lower and upper box edges corresponded to the first and third quartiles (the twenty-fifth and seventy-fifth percentiles); the horizontal line indicated the median value; and the lower and upper whiskers corresponded to the smallest value at most 1.5× interquartile range and the largest value no further than 1.5× interquartile range; points, outliers. i, The black circles indicated the geographic locations in China. The map was drawn using software ArcGIS 10.3 for desktop (https://desktop.arcgis.com/en/).

Extended Data Fig. 2 Positional cloning of Tof11 and Tof12.

a, Characterization of key recombinants in the immediate vicinity of the Tof11 locus showed recombination break points (left panel), and mean flowering time of progeny (right panel). b, Gene structure of Tof11 showed the location of the loss-of-function tof11-1 mutation. c, Characterization of key recombinants in the immediate vicinity of the Tof12 locus showed recombination break points (left panel), and mean flowering time of progeny (right panel). d, Gene structure of Tof12 showed the location of the loss-of-function tof12-1 mutation. e, Transgenic complementation of the tof11-1 mutation showed phenotypes of two independent transformants TC#2 and TC#4 relative to the untransformed control DN50 tof11-1 plants under LD (14 h light/10 h dark) conditions. Scale bar, 10 cm. f, Flowering time, g, time to maturity and h, grain yield per plant of control and transgenic lines. i, Transgenic complementation of the tof12-1 mutation, showed phenotypes of two independent transformants TC#7 and TC#8 relative to the untransformed control DN50 tof12-1 plants under LD (14 h light/10 h dark) conditions. Scale bar, 10 cm. j, Flowering time, k, time to maturity and l, grain yield per plant of control and transgenic lines. All data were given as mean ± s.e.m. (n = 10 plants), the value of each plant was represented by a dot. A Student’s t-test was used to generate the P values.

Extended Data Fig. 3 Expressions of LHY homologues in DN50 and complementary transgenic lines of Tof11 and Tof12.

Expressions of LHY2b in Tof11 a and Tof12 b complementary transgenic lines. Expressions of LHY1b in Tof11 c and Tof12 d complementary transgenic lines. Expressions of LHY1a in Tof11 e and Tof12 f complementary transgenic lines. Expressions of LHY2a in Tof11 g and Tof12 h complementary transgenic lines. All data are given as mean ± s.e.m. (n = 5 plants). Plants were grown under LD (16 h light/8 h dark) and sampled at 20 DAE.

Extended Data Fig. 4 Tobacco transient assay of different alleles of Tof11/tof11-1 and Tof12/tof12-1.

a, Constructs used for the transient transfection assay. b, Luciferase activity under control of LHY1a promoter showing the results from three independent replications. The value of each replication was represented by a dot. The presence of the same lowercase letter above the histogram bars denotes nonsignificant differences across each panel (P > 0.05). A Student’s t-test was used to generate the P values.

Extended Data Fig. 5 Fst and Pi in the wild soybeans, landraces and improved cultivars spanning the 2 megabase genome regions of putative domesticated genes.

Domesticated genes of G a, Shat1-5 b and Hs1-1 c were analyzed using the 1295 panel of 146 wild soybeans, 575 landraces and 574 improved cultivars. Blue dash lines indicated the threshold of the whole genome level.

Extended Data Fig. 6 Haplotypes and their origins of Tof12.

a, Haplotypes of Tof12. b, loss-of-function alleles of tof12. c, haplotype origins of Tof12. Grey color represented the wild soybeans, green color represented the landraces, blue color represented the improved cultivars. Pink triangles represented the loss-of-function alleles. Haplotypes was extracted from the 1295 panel of 146 wild soybeans, 575 landraces and 574 improved cultivars.

Extended Data Fig. 7 Haplotypes and their origins of Tof11.

a, Haplotypes of Tof11. b, loss-of-function alleles of tof11. c, haplotype origins of Tof11. Grey color represented the wild soybeans, green color represented the landraces, blue color represented the improved cultivars. Pink triangles represented the loss-of-function alleles. Haplotypes was extracted from the 1295 panel of 146 wild soybeans, 575 landraces and 574 improved cultivars.

Extended Data Fig. 8 Flowering time variations of different alleles in the 424 accessions of Tof11 and Tof12.

a, flowering time (R1) and maturity (R8) variations in 424 accessions possess Tof11 and tof11-1 in Zhengzhou (ZZ) and Hefei (HF). b, flowering time (R1) and maturity (R8) variations in 424 accessions possess Tof12 and tof12-1 in Zhengzhou (ZZ) and Hefei (HF). Flowering time variations of four allelic combinations of Tof11 and Tof12 in Zhengzhou 2018 c, Hefei 2018 d, Harbin 2019 e, Zhengzhou 2019 f, Wuhan 2019 g and Guangzhou 2019 h. The horizontal dash lines from c-h indicated the growth period in each location. The lower and upper box edges corresponded to the first and third quartiles (the twenty-fifth and seventy-fifth percentiles); the horizontal line indicated the median value; and the lower and upper whiskers corresponded to the smallest value at most 1.5× interquartile range and the largest value no further than 1.5× interquartile range. The presence of the same lowercase letter above the histogram bars in c-h denoted nonsignificant differences across the two panels (P > 0.05). A Student’s t-test was used to generate the P values.

Extended Data Fig. 9 Loss of Tof11 and Tof12 function improves soybean adaptation to high latitudes.

ac, Geographic origins of soybean wild accessions (a), landraces (b), and improved cultivars (c) possessing different allelic combinations at Tof11 and Tof12. NE, North East region of China; NR, North region of China; HR, Huanghuai region of China; SR, South region of China. Data were for both diversity panels (424- and 809-accession panels) but only accessions from China were shown. The maps were drawn using software ArcGIS 10.3 for desktop (https://desktop.arcgis.com/en/). d, Latitudinal distribution of all the landraces from China from (b) possessing different allelic combinations at Tof11 and Tof12. The lower and upper box edges corresponded to the first and third quartiles (the twenty-fifth and seventy-fifth percentiles); the horizontal line indicated the median value; and the lower and upper whiskers corresponded to the smallest value at most 1.5× interquartile range and the largest value no further than 1.5× interquartile range. The presence of the same lowercase letter above the histogram bars in (d) denoted nonsignificant differences across the two panels (P > 0.05). Student’s t-test was used to generate P values.

Extended Data Fig. 10 Flowering time variation in two panels under latitudinal cline.

The 809 domesticated accessions diversity panel at different latitudes, according to Tof11 a or Tof12 b genotype. Flowering time variation in the 442 accessions diversity panel at different latitudes, according to Tof11 c or Tof12 d genotype. The lower and upper box edges corresponded to the first and third quartiles (the twenty-fifth and seventy-fifth percentiles); the horizontal line indicated the median value; and the lower and upper whiskers corresponded to the smallest value at most 1.5× interquartile range and the largest value no further than 1.5× interquartile range. Student’s t-test was used to generate P values.

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Lu, S., Dong, L., Fang, C. et al. Stepwise selection on homeologous PRR genes controlling flowering and maturity during soybean domestication. Nat Genet 52, 428–436 (2020). https://doi.org/10.1038/s41588-020-0604-7

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