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Genomic insights into the recent chromosome reduction of autopolyploid sugarcane Saccharum spontaneum

Nature Genetics volume 54, pages 885–896 (2022)Cite this article

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Abstract

Saccharum spontaneum is a founding Saccharum species and exhibits wide variation in ploidy levels. We have assembled a high-quality autopolyploid genome of S. spontaneum Np-X (2n = 4x = 40) into 40 pseudochromosomes across 10 homologous groups, that better elucidates recent chromosome reduction and polyploidization that occurred circa 1.5 million years ago (Mya). One paleo-duplicated chromosomal pair in Saccharum, NpChr5 and NpChr8, underwent fission followed by fusion accompanied by centromeric split around 0.80 Mya. We inferred that Np-X, with x = 10, most likely represents the ancestral karyotype, from which x = 9 and x = 8 evolved. Resequencing of 102 S. spontaneum accessions revealed that S. spontaneum originated in northern India from an x = 10 ancestor, which then radiated into four major groups across the Indian subcontinent, China, and Southeast Asia. Our study suggests new directions for accelerating sugarcane improvement and expands our knowledge of the evolution of autopolyploids.

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Fig. 1: The phenotypes, karyotypes and genomic features of S. spontaneum AP85-441 and Np-X.
Fig. 2: The evolution of PdCPs.
Fig. 3: The higher chromatin structure, synonymous base substitution rates and allelic expression of the S. spontaneum Np-X genome.
Fig. 4: The evolution of Saccharum.
Fig. 5: Gene families associated with crucial biological traits in sugarcane.
Fig. 6: Genetic relationships among S. spontaneum populations.
Fig. 7: Population evolution in S. spontaneum.

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Data availability

All raw sequencing data and assembled genome sequences for the S. spontaneum were deposited into the Sequence Read Archive (under BioProject accession PRJNA721787). Genome assemblies and annotation files of S. officinarum (LA-Purple) are available from NCBI with the same accession number and under Bioproject accession PRJNA744175.

Code availability

All public software used in this study is provided in the accompanying Nature Research Reporting Summary.

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Acknowledgements

This work was supported by funding from the National Key Research and Development Program (2021YFF1000100), the Science and Technology Planting Project of Guangdong Province (2019B020238001), the National High-tech R&D Program (2013AA100604) and the Fujian Provincial Department of Education (JA12082) to J.Z.; the National Key Research and Development Program (2021YFF1000104) to H.T.; the Science and Technology Major Project of Guangxi (AA17202025) to M.Z.; and the China Scholarship Council (201707877011), the Scientific Research Foundation of the Graduate School of Fujian Agriculture and Forestry University Grant (324-1122yb050) and the fellowship of China Postdoctoral Science Foundation (2021M703555) to Q.Z.

Author information

Author notes

  1. These authors contributed equally: Qing Zhang, Yiying Qi, Haoran Pan, Haibao Tang.

Authors and Affiliations

  1. Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Sugarcane Biology and Genetic Breeding, National Engineering Research Center for Sugarcane, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, China

    Qing Zhang, Yiying Qi, Haoran Pan, Haibao Tang, Gang Wang, Yongjun Wang, Lianyu Lin, Zhen Li, Yihan Li, Tianyou Wang, Panpan Ma, Meijie Dou, Yibin Wang, Hengbo Wang, Xingtan Zhang, Zuhu Deng, Jingsheng Xu & Jisen Zhang

  2. Guangxi Key Lab for Sugarcane Biology, Guangxi University, Nanning, China

    Xiuting Hua, Fan Yu, Zehuai Yu, Wei Yao, Baoshan Chen & Muqing Zhang

  3. Institute of Oceanography, Marine Biotechnology Center, Minjiang University, Fuzhou, China

    Yongji Huang

  4. GrandOmics Biosciences, Beijing, China

    Zongyi Sun

  5. Biomarker Technologies Corporation, Beijing, China

    Yuntong Wang

  6. Yunnan Key Laboratory of Sugarcane Genetic Improvement, Sugarcane Research Institute, Yunnan Academy of Agricultural Sciences, Kaiyuan, China

    Xinlong Liu

  7. National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, China

    Maojun Wang

  8. Department of Agronomy, University of Florida, Gainesville, FL, USA

    Jianping Wang

  9. Sugarcane Research Institute, Yunnan Agricultural University, Kunming, China

    Qinghui Yang

  10. Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization at College of Landscape Architecture, Fujian Agriculture and Forestry University, Fuzhou, China

    ZhongJian Liu

  11. Department of Plant Biology, University of Illinois Urbana-Champaign, Urbana, IL, USA

    Ray Ming

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  1. Qing Zhang
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Contributions

J.Z. conceived this genome project and coordinated research activities; J.Z. and Q.Z. designed the experiments; Q.Z., J.Z., Q.Y., Yongjun Wang., Z.D., B.C., M.Z., J.W., R.M. and X.L. collected and generated sugarcane materials; F.Y., Z.Y., Y.H. and Z.D. performed the Oligo-FISH experiments; Q.Z., J.Z., G.W., Y.Q., L.L., X.Z., Z.S. and H.T. assembled and annotated the genome; Q.Z., H.P., Yibin Wang, M.W., J.Z. and H.T. analyzed the 3D genome; J.Z., X.H., Yongjun Wang, Z. Li, Y.L., T.W., P.M., J.X., Z. Liu and M.D. studied the genes relevant to the key characteristics in sugarcane; Q.Z., J.Z. and H.T. studied genome evolution; Q.Z., J.Z., Q.Y., H.W., H.T. and Yuntong Wang contributed to the population genetic analysis; and J.Z. and Q.Z. wrote the manuscript.

Corresponding author

Correspondence to Jisen Zhang.

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Extended data

Extended Data Fig. 1 Chromosome specific oligo probes to S. spontaneum accessions with x = 8.

(a) Probes to S. spontaneum SES208 (2n = 8x = 64, x = 8). In I, II, III, IV, and V, S. spontaneum Np-X chromosome-specific oligo probes NpC1, NpC3, NpC5, NpC7, and NpC9 are visualized in red, respectively. S. spontaneum Np-X chromosome-specific oligo probes NpC2, NpC4, NpC6, NpC8, and NpC10 are visualized in gree. S. spontaneum Np-X chromosome-specific oligo probes NpC7 and NpC8 are visualized in cyan in I, III, and V. Karyotypes of SES208 by Sschr 01 to Sschr 08 in VI. These results confirm the major chromosomal rearrangement events between Np-X and AP85-441 genomes. Bars = 10 μm. (b)Probes to S. spontaneum 82-114 (2n = 10x = 80, x = 8). In I, II, III, IV, V, VI, and VII, S. spontaneum Np-X chromosome-specific oligo probes NpC1, NpC3, NpC5, NpC7, NpC9, NpC5 and NpC8 are visualized in red, respectively. S. spontaneum Np-X chromosome-specific oligo probes NpC2, NpC4, NpC6, NpC8 and NpC10 are visualized in green. S. spontaneum Np-X chromosome-specific oligo probes NpC7 and NpC9 are visualized in cyan in VI and VII. Karyotypes of S. spontaneum 82-114 by Sschr01 to Sschr08 in VIII. The experiments were repeated independently at least three times with similar results. These results confirm the major chromosomal rearrangement events between Np-X and AP85-441 genomes, Bars = 10 μm.

Extended Data Fig. 2 Genome-wide chromatin interactions at 500-kb resolution in the S. spontaneum Np-X genome.

The intensity of pixels represents the count of Hi-C links between 500-kb windows on all chromosomes on a logarithmic scale. Darker red color indicates higher contact probability.

Extended Data Fig. 3 Assessment of S. spontaneum Np-X genome assembly using ultra-long reads.

(a) Counts of total ultra-long reads lengths. The centerline in each box represents the median; the lower and upper hinges represent the 25th and 75th percentiles, respectively. the whiskers represent 1.5× the interquartile range and the dots beyond the whiskers are outliers. The number of ultra-long reads: n = 288,773. (b) Distribution of whole ultra-long read alignments by identity on the S. spontaneum Np-X genome. The centerline in each box represents the median; the lower and upper hinges represent the 25th and 75th percentiles, respectively. the whiskers represent 1.5× the interquartile range and the dots beyond the whiskers are outliers. The number of ultra-long reads: n = 288,773. (c) The genome sequence of Np-X (shown on the x-axis) was aligned and plotted against ONT reads (shown on the y-axis) by Minimap2 (https://github.com/lh3/minimap2). The line in the dot plot indicates that both the sequences are very similar to each other. The red dots indicate the best match of the reads among the four homologous chromosomes.

Extended Data Fig. 4 Schematic diagram of switch errors evaluation.

The longest 10000 ultra-long ONT reads with N50 of 193 kb were aligned against each 10 kb window to all haplotypes (A, B, C, and D) of S. spontaneum Np-X genome. The switch error was detected according to the best matches to more than one chromosome or non-consecutive contigs.

Extended Data Fig. 5 Alignment of the S. spontaneum Np-X and Miscanthus sinensis genomes shown as a dot plot.

The labels (0, 10000, 20000,…) at x/y-axis mean the gene rank along the chromosomes (i.e. the span of x/y-axis represent the total number of genes in the respective genome in comparison).

Extended Data Fig. 6 Restructured chromosomes validation.

(a)FISH signals of centromere satellite repeat probes were detected as a single centromere of each chromosome in Np-X, while in AP85-441 FISH signals of dicentric chromosomes were detected in some chromosomes (arrowhead). The experiments were repeated independently at least three times with similar results. Scale bars = 5 μm. (b). The Hi-C read of S. spontaneum AP85-441 (upper) and S. spontaneum Np-X (bottom) were mapped to S. spontaneum AP85-441 genome respectively. The chromosomal rearrangement breakpoints are indicated by blue arrows that show matching discontinuities in the contrasting Hi-C contact maps. (c). The Hi-C reads of S. spontaneum Np-X (upper) and S. spontaneum AP85-441 (bottom), respectively, were mapped to the S. spontaneum Np-X genome. The chromosomal rearrangement breakpoints are indicated by blue arrows. AP: S. spontaneum AP85-441; Np: S. spontaneum Np-X.

Extended Data Fig. 7 Recombination of higher chromatin structure in the S. spontaneum Np-X and S. spontaneum AP85-441 genomes and related species.

(a) The four tracks represent first principal component values showing A/B compartment status for O. sativa, S. bicolor, S. spontaneum Np-X, and S. spontaneum AP85-441, respectively. In the analysis of each set of species, the grey line indicates syntenic regions of the chromosome between species. (b) The red, green, and blue bars indicate A-to-B compartment switching, B-to-A compartment switching, and conserved compartments during species evolution, respectively.

Extended Data Fig. 8 Transcript expression of genes within B to A compartment switching in S. spontaneum Np-X and corresponding genes in S. spontaneum AP85-441.

Note: The genes expression in leaf and stem are indicated in (a), and the transcript expression of genes located in the A to B switching, B to A switching, or in the conserved compartment in leaf and stem are shown in (b) and (c), respectively. n indicates the number of genes expression. The centerline in each box represents the median; the lower and upper hinges represent the 25th and 75th percentiles, respectively. The whiskers represent 1.5× the interquartile range. The dots beyond the whiskers are outliers. P-values were calculated using the two-sided Wilcoxon rank-sum test.

Extended Data Fig. 9 Phylogenetic and cis-elements analysis of Narrow Leaf (NAL)-related genes in S. spontaneum Np-X (Npp) and its related species.

(a) Phylogenetic analysis of Narrow Leaf (NAL)-related genes in S. spontaneum Np-X (Npp), S. spontaneum AP85-441 (Ss), S. officinarum (So), Z. mays (GRM), rice (Os), Sorghum (Sobic), and Arabidopsis (AT). The genes from S. spontaneum Np-X, S. officinarum and S. spontaneum AP85-441 are marked with purple, orange or blue circle, respectively. (b) Variation in cis-elements presents in the 2-kb upstream sequences of the NAL1 gene in S. spontaneum and S. officinarum. The cis-elements present in NAL1 in S. spontaneum and S. officinarum predicted using PlantCARE (http://bioinformatics.psb.ugent.be/webtools/plantcare/html/). Typical cis-elements are illustrated by boxes of different colors as shown, and unique cis-elements and the transcript abundances of these genes in different plant tissues based on RNA-seq data are presented in the table. AP: S. spontaneum AP85-441; Np: S. spontaneum Np-X; SO: S. officinarum.

Extended Data Fig. 10 Population genomics analysis for 102S. spontaneum accessions.

(a) Plot of ADMIXTURE cross-validation errors for K = 1 through K = 10. (b) STRUCTURE analysis of re-sequenced populations with K values from 2 to 6. (c) Linkage disequilibrium decay in different subpopulations of S. spontaneum. (d) Nucleotide diversity (π) and population divergence (FST) between different subpopulation of S. spontaneum. The value inside each circle represents a measure of π for that group, and the value on each line indicates FST between two groups.

Supplementary information

Supplementary Information

Supplementary Note, Supplementary Figures 1-30, and Supplementary Tables 1-24.

Reporting Summary

Supplementary Data 1

Gene function annotation for the S. spontaneum Np-X genome. The functional information of the S. spontaneum Np-X genes are predicted by searching against Nr, SWISS-PROT, KOG, GO, InterPro, KEGG and TrEMBL databases with defaults parameters. The transverse line indicates the unannotated items.

Supplementary Data 2

The gene allele information for S. spontaneum Np-X genome. The dataset contains the allele identification (ID) of each gene and the representative monoploidy gene ID. The transverse line indicates the unidentified alleles.

Supplementary Data 3

The core photosynthesis-related gene families in S. spontaneum Np-X, S. spontaneum AP85-441, Miscanthus and sorghum. The photosynthesis-related genes and alleles in S. spontaneum Np-X are presented in Sheet1, and the orthologous genes in S. spontaneum AP85-441, Miscanthus and sorghum and the homology of the amino acid sequence are indicated in Sheet2.

Supplementary Data 4

The orthologous genes in S. spontaneum Np-X, S. spontaneum AP85-441 and sorghum. The ortholog genes of S. pontaneum Np-X in S. spontaneum AP85-441 and sorghum, as well as the functional description, are shown in the table.

Supplementary Data 5

The function information of candidate genes in the selective sweep region. The genes located in the selective sweep region of S. spontaneum population and their corresponding ortholog genes in Arabidopsis, rice, sorghum and maize and their functions information annotated according to the GO database are indicated in the table. Lines marked with red represent the genes mentioned in the text.

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Zhang, Q., Qi, Y., Pan, H. et al. Genomic insights into the recent chromosome reduction of autopolyploid sugarcane Saccharum spontaneum. Nat Genet 54, 885–896 (2022). https://doi.org/10.1038/s41588-022-01084-1

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