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A telomere-to-telomere cotton genome assembly reveals centromere evolution and a Mutator transposon-linked module regulating embryo development

Nature Genetics volume 56, pages 1953–1963 (2024)Cite this article

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Abstract

Assembly of complete genomes can reveal functional genetic elements missing from draft sequences. Here we present the near-complete telomere-to-telomere and contiguous genome of the cotton species Gossypium raimondii. Our assembly identified gaps and misoriented or misassembled regions in previous assemblies and produced 13 centromeres, with 25 chromosomal ends having telomeres. In contrast to satellite-rich Arabidopsis and rice centromeres, cotton centromeres lack phased CENH3 nucleosome positioning patterns and probably evolved by invasion from long terminal repeat retrotransposons. In-depth expression profiling of transposable elements revealed a previously unannotated DNA transposon (MuTC01) that interacts with miR2947 to produce trans-acting small interfering RNAs (siRNAs), one of which targets the newly evolved LEC2 (LEC2b) to produce phased siRNAs. Systematic genome editing experiments revealed that this tripartite module, miR2947–MuTC01–LEC2b, controls the morphogenesis of complex folded embryos characteristic of Gossypium and its close relatives in the cotton tribe. Our study reveals a trans-acting siRNA-based tripartite regulatory pathway for embryo development in higher plants.

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Fig. 1: Assembly, comparative analysis of centromeric structures and epigenetic landscapes of the G. raimondii T2T genome.
Fig. 2: Identification of an ovule-specific, trans-acting, siRNA-generating DNA transposon MuTC01 in the G. raimondii genome.
Fig. 3: miR2947 is crucial for initiating siRNA production from MuTC01 during the formation of complex folded cotyledons.
Fig. 4: A tripartite regulatory pathway involving miR2947, MuTC01 and the LEC2b gene regulates cotton cotyledon folding.
Fig. 5: An evolutionary model for the formation of complex folded cotyledons in cotton seeds.

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Data availability

All raw sequencing data (ONT sequencing, PacBio HiFi and MGI reads) are available from the National Center for Biotechnology Information (NCBI) BioProject database (accession no. PRJNA812351) and the China National Center for Bioinformation (CNCB) (accession no. PRJCA008338). The genome sequence and gene annotation files for G. raimondii are available at the CNCB genome warehouse (https://ngdc.cncb.ac.cn/gwh) under accession no. GWHBISS00000000 or NCBI under accession nos. CP156731–CP156743 (BioProject PRJNA812351). The genome sequence, gene and transposable element annotation files for G. raimondii are also available at GitHub (https://github.com/huanggai/T2T-Cotton-DD5.git) and figshare (https://doi.org/10.6084/m9.figshare.25771302.v1)80. The RNA-seq, full-length NanoPore cDNA-seq, small RNA-seq and bisulfite sequencing for G. raimondii were deposited under NCBI project nos. PRJNA1128012, PRJNA1127988, PRJNA1127990, PRJNA1128006 or CNCB project nos. PRJCA016685, PRJCA016686, PRJCA016683 and PRJCA016687. The small RNA-seq data and degradome sequencing for G. hirsutum are available under the NCBI PRJNA1128045 or CNCB PRJCA016684 and PRJCA016814, respectively. The following databases were used: the Seed Information Database (https://ser-sid.org); the Seed Biology Place (http://seedbiology.eu/); and the Plant Genomes Database (https://www.plabipd.de). Source data are provided with this paper.

Code availability

All software used in the study is publicly available as described in the Methods and Reporting Summary. The custom code for the centromere analysis is available at Zenodo (https://zenodo.org/records/11115400)81 and GitHub (https://github.com/huanggai/T2T-Cotton-DD5.git).

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Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (grant nos. 32388101 to Y.Z. and 32201747 to G.H.).

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  1. Gai Huang

    Present address: Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China

Authors and Affiliations

  1. State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences, Peking University, Beijing, China

    Gai Huang & Yuxian Zhu

  2. Institute for Advanced Studies, Wuhan University, Wuhan, China

    Gai Huang & Yuxian Zhu

  3. Max Planck Institute for Biology Tübingen, Tübingen, Germany

    Zhigui Bao

  4. Department of Biology, School of Life Sciences, Southern University of Science and Technology, Shenzhen, China

    Li Feng & Jixian Zhai

  5. Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, IA, USA

    Jonathan F. Wendel

  6. Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China

    Xiaofeng Cao

  7. Hubei Hongshan Laboratory, Wuhan, China

    Yuxian Zhu

  8. Taikang Center for Life and Medical Sciences, Wuhan University, Wuhan, China

    Yuxian Zhu

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Contributions

Y.Z. and G.H. conceived and designed the project. G.H. and Z.B. conducted the T2T genome assembly. G.H. analyzed the data and performed the experiments. L.F. and J.Z. assisted in the small RNA analysis. X.C. and J.F.W. provided input for the discussions. Y.Z. and G.H. wrote and revised the paper, with assistance from J.F.W.

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Huang, G., Bao, Z., Feng, L. et al. A telomere-to-telomere cotton genome assembly reveals centromere evolution and a Mutator transposon-linked module regulating embryo development. Nat Genet 56, 1953–1963 (2024). https://doi.org/10.1038/s41588-024-01877-6

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