Abstract
Polyploidy and life-strategy transitions between annuality and perenniality often occur in flowering plants. However, the evolutionary propensities of polyploids and the genetic bases of such transitions remain elusive. We assembled chromosome-level genomes of representative perennial species across the genus Glycine including five diploids and a young allopolyploid, and constructed a Glycine super-pangenome framework by integrating 26 annual soybean genomes. These perennial diploids exhibit greater genome stability and possess fewer centromere repeats than the annuals. Biased subgenomic fractionation occurred in the allopolyploid, primarily by accumulation of small deletions in gene clusters through illegitimate recombination, which was associated with pre-existing local subgenomic differentiation. Two genes annotated to modulate vegetative–reproductive phase transition and lateral shoot outgrowth were postulated as candidates underlying the perenniality–annuality transition. Our study provides insights into polyploid genome evolution and lays a foundation for unleashing genetic potential from the perennial gene pool for soybean improvement.
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Data availability
Raw sequences generated during this study are deposited in the public repository of the National Center for Biotechnology Information under accession number PRJNA44023. The annotated assemblies are deposited in the European Nucleotide Archive under accession number PRJEB44023. Additionally, the assembled genome data and gene annotation have been deposited in SoyBase (http://soybase.org/data/v2/Glycine/) for future visualization of interspecific genome content comparison that is under development.
Code availability
The main custom scripts have been deposited in GitHub (https://github.com/Yongbinzhuang/Perennial_Soybean_Genome).
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Acknowledgements
We thank J. Campbell for preparing BES data generated from the SoyMapII project and A. Farmer for integrating the genome sequence data generated in this study into SoyBase. The work was mainly supported by the National Key Research and Development Program (grant no. 2021YFF1001203), the Taishan Scholars Program of Shandong Province (tsqn201812036), the Agricultural Variety Improvement Project of Shandong Province (2019LZGC004) and the Program for Scientific Research Innovation Team of Young Scholar in Colleges and Universities of Shandong Province, China (2020KJF008) to D.Z., Y.Z. and X.S.Z. Partial support was provided by the US National Science Foundation Plant Genome Research Program to S.A.J., J.J.D., S.B.C., J.G., J.S. and J.M. (IOS-0822258) and the US Department of Agriculture (USDA) National Institute of Food and Agriculture MultiState Project to J.J.D. and J.B.L. (NC7 1014310). This research was also supported in part by the USDA Agricultural Research Service, project 5030-21000-069-00D to S.B.C. for integration of this source of genome data into SoyBase. The findings and conclusions in this publication are those of the authors and should not be construed to represent any official USDA or US government determination or policy. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA.
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Y.Z., D.Z. and J.M. conceived and designed the research. J.G. and J.S. generated BES data. Y.Z., X.W., X.L., J.H., L.F, J.B.L. and D.Z. performed analysis. Y.Z., X.W., S.B.C., S.A.J, J.J.D., X.S.Z., D.Z and J.M. interpreted the data. Y.Z., D.Z. J.J.D. and J.M. wrote the manuscript.
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Extended data
Extended Data Fig. 1 Genomic collinearity and rearrangements among the annual and perennial Glycine species.
a, Syntenic plots of perennial Glycine species. b, Illustration of an segmental inversion occurred in the annual Glycine lineage. c, Illustration of chromosomal rearrangements involving chromosomes 8 and 10 of the A, D, and F genomes. Red vertical bar indicates gaps in assemblies. d, Portion of chromosomes show conserved synteny through the whole chromosome in each perennial Glycine species. e, Portion of identified genome variations supported by species-specific BAC end sequences.
Extended Data Fig. 2 Comparison of LTR-retrotransposons in the annual and perennial Glycine species.
a, Ratios of solo LTRs to intact LTR-retrotransposons identified in each genome. b, c, Relative abundances and insertion times of LTR-RTs belonging to the five largest families in G. cyrtoloba (b) and G. falcata (c). A mutation rate of 1.3×10-8 per nucleotide per year was used for estimation of insertion times of individual LTR-RTs. d, e, Relative abundances of LTR-RTs belonging to the five most abundant copia-LTR-RT families (d) and the five most abundant gypsy-LTR-RT families (e) in the G. max and each perennial genome.
Extended Data Fig. 3 Comparison of centromeric satellite repeat families, Gm-Cent1, Gm-Cent2, and Gf-Cent.
a, Consensus sequence of Gf-Cent constructed based on 500 Gf-Cent repeats randomly selected from the F genome, the orange bars indicate highly variable nucleotide positions (<0.7). b, Alignment of representative Gm-Cent1, Gm-Cent2 and Gf-Cent repeats.
Extended Data Fig. 4 Analysis of centromeric satellite repeats and their associated centromeric retrotransposon families in the G. max and perennial Glycine species.
a, Estimation of the divergent times of Gm-Cent1, Gm-Cent2, and Gf-Cent repeats. A mutation rate of 1.3×10-8 per nucleotide per year was used for estimation of divergence times. b, c, d, Relative abundance of putative centromere retrotransposon families with detected internal sequences, which were predicted to encode five key enzymes (GAP, AP, INT, RT and RNase H).
Extended Data Fig. 5 Relative abundances of singletons and duplicated genes in G. max and the perennial Glycine genomes.
a, The numbers of core genes identified in 26 annual Glycine datasets. b, Boxplot showing the number of Non-core, core genes and Non-redundant genes for five random selected annual soybeans from 26 annual Glycine datasets. d, Bar plot showing the number of shared singletons c and duplicated genes d between G. max and individual perennial genomes. e, Proportions of singletons and duplicates identified in individual genomes. Undefined categories of genes such as tandem duplicates were not shown in the plots.
Extended Data Fig. 6
GO enrichment analysis of Glycine orthologs underwent adaptive evolution between the two subgenera.
Extended Data Fig. 7 Neighbour-joining tree of young (<0.35 MY) copia-LTR-RTs in the two subgenomes of the recent allopolyploid.
Highlighted elements represent nearly identical elements amplified from one of the two subgenomes and inserted into the other subgenome. after the recent allopolyploidy event.
Extended Data Fig. 8 Neighbour-joining tree of young (<0.35 MY) gypsy-LTR-RTs in the two subgenomes of the recent allopolyploid.
Highlighted elements represent nearly identical elements amplified from one of the two subgenomes and inserted into the other subgenome after the recent allopolyploidy event.
Extended Data Fig. 9 Neighbour-joining tree of young (<0.35 MY) copia-LTR-RTs from in the A and D genomes.
No nearly identical elements in A and D were found.
Extended Data Fig. 10 Neighbour-joining tree of young (<0.35 MY) gypsy-LTR-RTs from in the A and D genomes.
No nearly identical elements in A and D were found.
Supplementary information
Supplementary Information
Supplementary Figs. 1–8 and additional Fig. 1.
Supplementary Tables
Supplementary Tables 1–18: 1, Evaluation and correction of the raw assembled genomes using bacterial artificial chromosome sequences (BESs); 2, k-mer analysis of perennial Glycine genomes; 3, Statistics of the six assembled perennial Glycine genomes; 4, Genome assembly and annotation completeness evaluated by BUSCO; 5, Genome assembly and annotation completeness evaluated by CEGMA; 6, Numbers of annotated genes and TE content in the assembled perennial genomes; 7, Genomic rearrangements identified in the sequenced Glycine species using common bean as a reference; 8, PCR primers used in the validation of ten selected genome conversions; 9, Summary of copia-LTR-retrotransposons identified in the perennial Glycine genomes; 10, Summary of gypsy-LTR-retrotransposons identified in perennial Glycine species; 11, The top five most abundant tandem repeats in perennial Glycine species; 12, Synteny table among 26 annual and 5 perennial soybeans; 13, Duplicates and singletons in the annual and perennial Glycine genomes; 14, Classification of gene status; 15, List of genes showing adaptive evolution between annual and perennial soybeans; 16, McDonald–Kreitman tests for a single flowering controlling gene showing adaptive evolution as candidates underlying the life-strategy transition in Glycine; 17, List of genes used for analysis of subgenome fractionation in G. dolichocarpa; 18, Losses of genes in At and Dt that are orthologues to the core or non-core Glycine genes in A and D.
Supplementary Data
Genome coordinations of transposons identified in each perennial Glycine species.
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Zhuang, Y., Wang, X., Li, X. et al. Phylogenomics of the genus Glycine sheds light on polyploid evolution and life-strategy transition. Nat. Plants 8, 233–244 (2022). https://doi.org/10.1038/s41477-022-01102-4
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DOI: https://doi.org/10.1038/s41477-022-01102-4
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