Skip to main content
Log in

Telomere-to-telomere genome of the allotetraploid legume Sesbania cannabina reveals transposon-driven subgenome divergence and mechanisms of alkaline stress tolerance

  • Research Paper
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

Alkaline soils pose an increasing problem for agriculture worldwide, but using stress-tolerant plants as green manure can improve marginal land. Here, we show that the legume Sesbania cannabina is very tolerant to alkaline conditions and, when used as a green manure, substantially improves alkaline soil. To understand genome evolution and the mechanisms of stress tolerance in this allotetraploid legume, we generated the first telomere-to-telomere genome assembly of S. cannabina spanning ∼2,087 Mb. The assembly included all centromeric regions, which contain centromeric satellite repeats, and complete chromosome ends with telomeric characteristics. Further genome analysis distinguished A and B subgenomes, which diverged approximately 7.9 million years ago. Comparative genomic analysis revealed that the chromosome homoeologs underwent large-scale inversion events (>10 Mb) and a significant, transposon-driven size expansion of the chromosome 5A homoeolog. We further identified four specific alkali-induced phosphate transporter genes in S. cannabina; these may function in alkali tolerance by relieving the deficiency in available phosphorus in alkaline soil. Our work highlights the significance of S. cannabina as a green tool to improve marginal lands and sheds light on subgenome evolution and adaptation to alkaline soils.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Akdemir, K.C., and Chin, L. (2015). HiCPlotter integrates genomic data with interaction matrices. Genome Biol 16, 198.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bertioli, D.J., Jenkins, J., Clevenger, J., Dudchenko, O., Gao, D., Seijo, G., Leal-Bertioli, S.C.M., Ren, L., Farmer, A.D., Pandey, M.K., et al. (2019). The genome sequence of segmental allotetraploid peanut Arachis hypogaea. Nat Genet 51, 877–884.

    Article  CAS  PubMed  Google Scholar 

  • Bunma, S., and Balslev, H. (2019). A review of the economic botany of Sesbania (Leguminosae). Bot Rev 85, 185–251.

    Article  Google Scholar 

  • Cao, X., Sun, B., Chen, H., Zhou, J., Song, X., Liu, X., Deng, X., Li, X., Zhao, Y., Zhang, J., et al. (2021). Approaches and research progresses of marginal land productivity expansion and ecological benefit improvement in China. Bull Chin Acad Sci 36, 336–348.

    Google Scholar 

  • Carr, P.M., Cavigelli, M.A., Darby, H., Delate, K., Eberly, J.O., Fryer, H.K., Gramig, G. G., Heckman, J.R., Mallory, E.B., Reeve, J.R., et al. (2020). Green and animal manure use in organic field crop systems. Agronomy J 112, 648–674.

    Article  Google Scholar 

  • Chen, J., Wang, Z., Tan, K., Huang, W., Shi, J., Li, T., Hu, J., Wang, K., Wang, C., Xin, B., et al. (2023). A complete telomere-to-telomere assembly of the maize genome. Nat Genet 55, 1221–1231.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng, H., Concepcion, G.T., Feng, X., Zhang, H., and Li, H. (2021). Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm. Nat Methods 18, 170–175.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Emms, D.M., and Kelly, S. (2019). OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol 20, 238.

    Article  PubMed  PubMed Central  Google Scholar 

  • Estruch, F. (2000). Stress-controlled transcription factors, stress-induced genes and stress tolerance in budding yeast. FEMS Microbiol Rev 24, 469–486.

    Article  CAS  PubMed  Google Scholar 

  • FAO, and ITPS. (2015). Status of the World’s Soil Resources (SWSR)—Main Report. In: Nachtergaele, F., ed. Rome: FAO and ITPS.

  • Gladman, N., Goodwin, S., Chougule, K., Richard McCombie, W., and Ware, D. (2023). Era of gapless plant genomes: innovations in sequencing and mapping technologies revolutionize genomics and breeding. Curr Opin Biotechnol 79, 102886.

    Article  CAS  PubMed  Google Scholar 

  • Griesmann, M., Chang, Y., Liu, X., Song, Y., Haberer, G., Crook, M.B., Billault-Penneteau, B., Lauressergues, D., Keller, J., Imanishi, L., et al. (2018). Phylogenomics reveals multiple losses of nitrogen-fixing root nodule symbiosis. Science 361, eaat1743.

    Article  PubMed  Google Scholar 

  • Holt, C., and Yandell, M. (2011). MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects. BMC Bioinf 12, 491.

    Article  Google Scholar 

  • Huang, G., Wu, Z., Percy, R.G., Bai, M., Li, Y., Frelichowski, J.E., Hu, J., Wang, K., Yu, J.Z., and Zhu, Y. (2020). Genome sequence of Gossypium herbaceum and genome updates of Gossypium arboreum and Gossypium hirsutum provide insights into cotton A-genome evolution. Nat Genet 52, 516–524.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang, G., and Zhu, Y. (2022). Insights of section-wide pan-genome into hybrid potato breeding. Sci China Life Sci 65, 2125–2127.

    Article  PubMed  Google Scholar 

  • Jayakodi, M., Golicz, A.A., Kreplak, J., Fechete, L.I., Angra, D., Bednář, P., Bornhofen, E., Zhang, H., Boussageon, R., Kaur, S., et al. (2023). The giant diploid faba genome unlocks variation in a global protein crop. Nature 615, 652–659.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jayakodi, M., Padmarasu, S., Haberer, G., Bonthala, V.S., Gundlach, H., Monat, C., Lux, T., Kamal, N., Lang, D., Himmelbach, A., et al. (2020). The barley pangenome reveals the hidden legacy of mutation breeding. Nature 588, 284–289.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jia, K., Wang, Z., Wang, L., Li, G., Zhang, W., Wang, X., Xu, F., Jiao, S., Zhou, S., Liu, H., et al. (2022). SUBPHASER: a robust allopolyploid subgenome phasing method based on subgenome-specific k-mers. New Phytol 235, 801–809.

    Article  CAS  PubMed  Google Scholar 

  • Kreplak, J., Madoui, M.A., Cápal, P., Novák, P., Labadie, K., Aubert, G., Bayer, P.E., Gali, K.K., Syme, R.A., Main, D., et al. (2019). A reference genome for pea provides insight into legume genome evolution. Nat Genet 51, 1411–1422.

    Article  CAS  PubMed  Google Scholar 

  • Kumar, S., Stecher, G., Li, M., Knyaz, C., and Tamura, K. (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35, 1547–1549.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lescot, M., Dehais, P., Thijs, G., Marchal, K., Moreau, Y., Van de Peer, Y., Rouze, P., and Rombauts, S. (2002). PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30, 325–327.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levi, M., Gratton, E., Forster, I.C., Hernando, N., Wagner, C.A., Biber, J., Sorribas, V., and Murer, H. (2019). Mechanisms of phosphate transport. Nat Rev Nephrol 15, 482–500.

    Article  CAS  PubMed  Google Scholar 

  • Li, H. (2018). Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, H., Jiang, F., Wu, P., Wang, K., and Cao, Y. (2020). A high-quality genome sequence of model legume Lotus japonicus (MG-20) provides insights into the evolution of root nodule symbiosis. Genes 11, 483.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, Y., Li, X., Liu, Y., Wang, E.T., Ren, C., Liu, W., Xu, H., Wu, H., Jiang, N., Li, Y., et al. (2016). Genetic diversity and community structure of rhizobia nodulating Sesbania cannabina in saline-alkaline soils. Syst Appl Microbiol 39, 195–202.

    Article  CAS  PubMed  Google Scholar 

  • Li, Y.H., Qin, C., Wang, L., Jiao, C., Hong, H., Tian, Y., Li, Y., Xing, G., Wang, J., Gu, Y., et al. (2023). Genome-wide signatures of the geographic expansion and breeding of soybean. Sci China Life Sci 66, 350–365.

    Article  CAS  PubMed  Google Scholar 

  • Liu, Y., Du, H., Li, P., Shen, Y., Peng, H., Liu, S., Zhou, G.A., Zhang, H., Liu, Z., Shi, M., et al. (2020). Pan-genome of wild and cultivated soybeans. Cell 182, 162–176.e13.

    Article  CAS  PubMed  Google Scholar 

  • Lomsadze, A., Ter-Hovhannisyan, V., Chernoff, Y.O., and Borodovsky, M. (2005). Gene identification in novel eukaryotic genomes by self-training algorithm. Nucleic Acids Res 33, 6494–6506.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maitra, S., Zaman, A., Mandal, T.K., and Palai, J.B. (2018). Green manures in agriculture: a review. J Pharmacogn Phytochem 7, 1319–1327.

    CAS  Google Scholar 

  • Marçais, G., and Kingsford, C. (2011). A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics 27, 764–770.

    Article  PubMed  PubMed Central  Google Scholar 

  • Naher, U.A., Choudhury, A.T.M.A., Biswas, J.C., Panhwar, Q.A., and Kennedy, I.R. (2020). Prospects of using leguminous green manuring crop Sesbania rostrata for supplementing fertilizer nitrogen in rice production and control of environmental pollution. J Plant Nutr 43, 285–296.

    Article  CAS  Google Scholar 

  • Naish, M., Alonge, M., Wlodzimierz, P., Tock, A.J., Abramson, B.W., Schmücker, A., Mandáková, T., Jamge, B., Lambing, C., Kuo, P., et al. (2021). The genetic and epigenetic landscape of the Arabidopsis centromeres. Science 374, eabi7489.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ou, S., Su, W., Liao, Y., Chougule, K., Agda, J.R.A., Hellinga, A.J., Lugo, C.S.B., Elliott, T.A., Ware, D., Peterson, T., et al. (2019). Benchmarking transposable element annotation methods for creation of a streamlined, comprehensive pipeline. Genome Biol 20, 275.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Padmanabhan, P., and Sahi, S.V. (2009). Genetic transformation and regeneration of Sesbania drummondii using cotyledonary nodes. Plant Cell Rep 28, 31–40.

    Article  CAS  PubMed  Google Scholar 

  • Pertea, M., Kim, D., Pertea, G.M., Leek, J.T., and Salzberg, S.L. (2016). Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat Protoc 11, 1650–1667.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peterbauer, C., Litscher, D., and Kubicek, C. (2002). The Trichoderma atroviride seb1 (stress response element binding) gene encodes an AGGGG-binding protein which is involved in the response to high osmolarity stress. Mol Gen Genomics 268, 223–231.

    Article  CAS  Google Scholar 

  • Puttick, M.N. (2019). MCMCtreeR: functions to prepare MCMCtree analyses and visualize posterior ages on trees. Bioinformatics 35, 5321–5322.

    Article  CAS  PubMed  Google Scholar 

  • Quan, W., Liu, X., Wang, H., and Chan, Z. (2016). Physiological and transcriptional responses of contrasting alfalfa (Medicago sativa L.) varieties to salt stress. Plant Cell Tiss Organ Cult 126, 105–115.

    Article  CAS  Google Scholar 

  • Quilbé, J., Lamy, L., Brottier, L., Leleux, P., Fardoux, J., Rivallan, R., Benichou, T., Guyonnet, R., Becana, M., Villar, I., et al. (2021). Genetics of nodulation in Aeschynomene evenia uncovers mechanisms of the rhizobium-legume symbiosis. Nat Commun 12, 829.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ranallo-Benavidez, T.R., Jaron, K.S., and Schatz, M.C. (2020). GenomeScope 2.0 and Smudgeplot for reference-free profiling of polyploid genomes. Nat Commun 11, 1432.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rhie, A., Walenz, B.P., Koren, S., and Phillippy, A.M. (2020). Merqury: reference-free quality, completeness, and phasing assessment for genome assemblies. Genome Biol 21, 245.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmutz, J., Cannon, S.B., Schlueter, J., Ma, J., Mitros, T., Nelson, W., Hyten, D.L., Song, Q., Thelen, J.J., Cheng, J., et al. (2010). Genome sequence of the palaeopolyploid soybean. Nature 463, 178–183.

    Article  CAS  PubMed  Google Scholar 

  • Shen, Y., Liu, J., Geng, H., Zhang, J., Liu, Y., Zhang, H., Xing, S., Du, J., Ma, S., and Tian, Z. (2018). De novo assembly of a Chinese soybean genome. Sci China Life Sci 61, 871–884.

    Article  CAS  PubMed  Google Scholar 

  • Shi, X., Cao, S., Wang, X., Huang, S., Wang, Y., Liu, Z., Liu, W., Leng, X., Peng, Y., Wang, N., et al. (2023). The complete reference genome for grapevine (Vitis vinifera L.) genetics and breeding. Hort Res 10, uhad061.

    Article  Google Scholar 

  • Song, J., and Wang, B. (2015). Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model. Ann Bot 115, 541–553.

    Article  CAS  PubMed  Google Scholar 

  • Song, J.M., Guan, Z., Hu, J., Guo, C., Yang, Z., Wang, S., Liu, D., Wang, B., Lu, S., Zhou, R., et al. (2020). Eight high-quality genomes reveal pan-genome architecture and ecotype differentiation of Brassica napus. Nat Plants 6, 34–45.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stanke, M., Diekhans, M., Baertsch, R., and Haussler, D. (2008). Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 24, 637–644.

    Article  CAS  PubMed  Google Scholar 

  • Sun, X., Sun, M., Jia, B., Qin, Z., Yang, K., Chen, C., Yu, Q., and Zhu, Y. (2016). A Glycine soja methionine sulfoxide reductase B5a interacts with the Ca2+/CAM-binding kinase GsCBRLK and activates ROS signaling under carbonate alkaline stress. Plant J 86, 514–529.

    Article  CAS  PubMed  Google Scholar 

  • Tang, H., Bowers, J.E., Wang, X., Ming, R., Alam, M., and Paterson, A.H. (2008). Synteny and collinearity in plant genomes. Science 320, 486–488.

    Article  CAS  PubMed  Google Scholar 

  • Trifinopoulos, J., Nguyen, L.T., von Haeseler, A., and Minh, B.Q. (2016). W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res 44, W232–W235.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van de Velde, W., Mergeay, J., Holsters, M., and Goormachtig, S. (2003). Agrobacterium rhizogenes-mediated transformation of Sesbania rostrata. Plant Sci 165, 1281–1288.

    Article  CAS  Google Scholar 

  • Vasimuddin, M., Misra, S., Li, H., and Aluru, S. (2019). Efficient architecture-aware acceleration of BWA-MEM for multicore systems. Int Parall Distrib P, 314–324.

  • Wang, H., Wu, Z., Chen, Y., Yang, C., and Shi, D. (2011). Effects of salt and alkali stresses on growth and ion balance in rice (Oryza sativa L.). Plant Soil Environ 57, 286–294.

    Article  Google Scholar 

  • Wang, Y., Chen, Y., and Wu, W. (2021). Potassium and phosphorus transport and signaling in plants. J Integr Plant Biol 63, 34–52.

    Article  CAS  PubMed  Google Scholar 

  • Wen, X., Chen, Z., Yang, Z., Wang, M., Jin, S., Wang, G., Zhang, L., Wang, L., Li, J., Saeed, S., et al. (2023). A comprehensive overview of cotton genomics, biotechnology and molecular biological studies. Sci China Life Sci doi: https://doi.org/10.1007/s11427-022-2278-0.

  • Wlodzimierz, P., Hong, M., and Henderson, I.R. (2023). TRASH: tandem repeat annotation and structural hierarchy. Bioinformatics 39, btad308.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu, Y., Li, D., Hu, Y., Li, H., Ramstein, G.P., Zhou, S., Zhang, X., Bao, Z., Zhang, Y., Song, B., et al. (2023). Phylogenomic discovery of deleterious mutations facilitates hybrid potato breeding. Cell 186, 2313–2328.e15.

    Article  CAS  PubMed  Google Scholar 

  • Xiao, J., Liu, B., Yao, Y., Guo, Z., Jia, H., Kong, L., Zhang, A., Ma, W., Ni, Z., Xu, S., et al. (2022). Wheat genomic study for genetic improvement of traits in China. Sci China Life Sci 65, 1718–1775.

    Article  PubMed  Google Scholar 

  • Xu, L., Zhao, H., Wan, R., Liu, Y., Xu, Z., Tian, W., Ruan, W., Wang, F., Deng, M., Wang, J., et al. (2019). Identification of vacuolar phosphate efflux transporters in land plants. Nat Plants 5, 84–94.

    Article  CAS  PubMed  Google Scholar 

  • Yang, C., Chong, J., Li, C., Kim, C., Shi, D., and Wang, D. (2007). Osmotic adjustment and ion balance traits of an alkali resistant halophyte Kochia sieversiana during adaptation to salt and alkali conditions. Plant Soil 294, 263–276.

    Article  CAS  Google Scholar 

  • Yang, H., Zhang, P., Zhu, T., Li, Q., and Cao, J. (2019). The characteristics of soil C, N, and P stoichiometric ratios as affected by geological background in a karst graben area, Southwest China. Forests 10, 601.

    Article  Google Scholar 

  • Yang, R., Song, S., Chen, S., Du, Z., and Kong, J. (2023). Adaptive evaluation of green manure rotation for a low fertility farmland system: Impacts on crop yield, soil nutrients, and soil microbial community. Catena 222, 106873.

    Article  CAS  Google Scholar 

  • Yang, T., Liu, R., Luo, Y., Hu, S., Wang, D., Wang, C., Pandey, M.K., Ge, S., Xu, Q., Li, N., et al. (2022). Improved pea reference genome and pan-genome highlight genomic features and evolutionary characteristics. Nat Genet 54, 1553–1563.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu, H., Lin, T., Meng, X., Du, H., Zhang, J., Liu, G., Chen, M., Jing, Y., Kou, L., Li, X., et al. (2021). A route to de novo domestication of wild allotetraploid rice. Cell 184, 1156–1170.e14.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, H., Liu, X.L., Zhang, R.X., Yuan, H.Y., Wang, M.M., Yang, H.Y., Ma, H.Y., Liu, D., Jiang, C.J., and Liang, Z.W. (2017). Root damage under alkaline stress is associated with reactive oxygen species accumulation in rice (Oryza sativa L.). Front Plant Sci 8, 1580.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang, H., Yu, F., Xie, P., Sun, S., Qiao, X., Tang, S., Chen, C., Yang, S., Mei, C., Yang, D., et al. (2023). A Gγ protein regulates alkaline sensitivity in crops. Science 379, eade8416.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, H., Zhu, J., Gong, Z., and Zhu, J.K. (2022a). Abiotic stress responses in plants. Nat Rev Genet 23, 104–119.

    Article  PubMed  Google Scholar 

  • Zhang, Q., Qi, Y., Pan, H., Tang, H., Wang, G., Hua, X., Wang, Y., Lin, L., Li, Z., Li, Y., et al. (2022b). Genomic insights into the recent chromosome reduction of autopolyploid sugarcane Saccharum spontaneum. Nat Genet 54, 885–896.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, W., Liu, J., Zhang, Y., Qiu, J., Li, Y., Zheng, B., Hu, F., Dai, S., and Huang, X. (2020). A high-quality genome sequence of alkaligrass provides insights into halophyte stress tolerance. Sci China Life Sci 63, 1269–1282.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, Z., Xiao, J., Wu, J., Zhang, H., Liu, G., Wang, X., and Dai, L. (2012). ParaAT: a parallel tool for constructing multiple protein-coding DNA alignments. Biochem Biophys Res Commun 419, 779–781.

    Article  CAS  PubMed  Google Scholar 

  • Zhuang, W., Chen, H., Yang, M., Wang, J., Pandey, M.K., Zhang, C., Chang, W.C., Zhang, L., Zhang, X., Tang, R., et al. (2019). The genome of cultivated peanut provides insight into legume karyotypes, polyploid evolution and crop domestication. Nat Genet 51, 865–876.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgement

This work was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA28030000), the National Key Research and Development Program of China (2022YFD1500503, 2022YFF1003401), Science & Technology Specific Projects in Agricultural High-tech Industrial Demonstration Area of the Yellow River Delta (2022SZX14), the earmarked fund for CARS-Green Manure (CARS-22), the Youth Innovation Promotion Association of CAS (Y2022039). We thank Prof.s Keke Yi and Lei Xu from Chinese Academy of Agricultural Sciences for their assistance in the Pi transport activity of PHT in yeast experiment.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Xiaofeng Cao, Xianwei Song or Gai Huang.

Ethics declarations

The author(s) declare that they have no conflict of interest.

Supporting information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Luo, H., Wang, X., You, C. et al. Telomere-to-telomere genome of the allotetraploid legume Sesbania cannabina reveals transposon-driven subgenome divergence and mechanisms of alkaline stress tolerance. Sci. China Life Sci. 67, 149–160 (2024). https://doi.org/10.1007/s11427-023-2463-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-023-2463-y

Keywords

Navigation