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Origin and evolution of the triploid cultivated banana genome

Nature Genetics volume 56, pages 136–142 (2024)Cite this article

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Abstract

Most fresh bananas belong to the Cavendish and Gros Michel subgroups. Here, we report chromosome-scale genome assemblies of Cavendish (1.48 Gb) and Gros Michel (1.33 Gb), defining three subgenomes, Ban, Dh and Ze, with Musa acuminata ssp. banksii, malaccensis and zebrina as their major ancestral contributors, respectively. The insertion of repeat sequences in the Fusarium oxysporum f. sp. cubense (Foc) tropical race 4 RGA2 (resistance gene analog 2) promoter was identified in most diploid and triploid bananas. We found that the receptor-like protein (RLP) locus, including Foc race 1-resistant genes, is absent in the Gros Michel Ze subgenome. We identified two NAP (NAC-like, activated by apetala3/pistillata) transcription factor homologs specifically and highly expressed in fruit that directly bind to the promoters of many fruit ripening genes and may be key regulators of fruit ripening. Our genome data should facilitate the breeding and super-domestication of bananas.

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Fig. 1: Genome evolution of AAA bananas.
Fig. 2: The resistance genes/QTLs among Cavendish, Gros Michel and their wild ancestors.
Fig. 3: Identification of genes controlling ripening in banana.

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Data availability

Genome assemblies of Cavendish, Gros Michel and Zebrina v2.0 have been deposited into NCBI under GenBank numbers JAVVNX000000000, JAVVNW000000000 and JAVVNV000000000 and in the National Genomics Data Center BioProject database (https://ngdc.cncb.ac.cn/bioproject/) under the accession number PRJCA019650. Genome assemblies with annotations and results of ChIP–seq and DNase-seq can be accessed at FigShare (https://figshare.com/projects/Origin_and_evolution_of_the_triploid_cultivated_banana_genome/178041). Raw data used for the assemblies, including PacBio, Illumina and Hi-C data, are available through the Sequence Read Archive of the National Centre for Biotechnology Information (NCBI) under the BioProject PRJNA1017453 with SRA accessions from SRR23425440 to SRR23425472 and from SRR23885547 to SRR23885549. Fifty-eight RNA-seq datasets were downloaded from NCBI BioProject accessions PRJNA381300, PRJNA394594 and PRJNA598018. DNA methylation data were downloaded from NCBI BioProject PRJNA381300.

Code availability

Custom code and scripts for mapping the origins of chromosomal segments are available at FigShare (https://doi.org/10.6084/m9.figshare.21229205.v1)70. All public software used in this study is provided in the accompanying Nature Portfolio Reporting Summary.

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Acknowledgements

We thank G. Riddihough (Life Science Editors) for text editing. X.L. acknowledges funding from the National Natural Science Foundation of China (32370687). P.L. acknowledges funding from the National Natural Science Foundation of China (32372666) and Construction of Plateau Discipline of Fujian Province (102/71201801104). L.Z. acknowledges funding from the National Natural Science Foundation of China (32272750). Y.V.d.P. acknowledges funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (no. 833522) and from Ghent University (Methusalem funding, BOF.MET.2021.0005.01).

Author information

Author notes

  1. These authors contributed equally: Xiuxiu Li, Sheng Yu, Zhihao Cheng, Xiaojun Chang, Yingzi Yun, Mengwei Jiang.

Authors and Affiliations

  1. State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Haixia Institute of Science and Technology, College of Horticulture, Fujian Agriculture and Forestry University, Fuzhou, China

    Xiuxiu Li, Yingzi Yun, Mengwei Jiang, Xuequn Chen, Hua Li, Wenjun Zhu, Shiyao Xu, Yanbing Xu, Xianjun Wang, Chen Zhang, Zonghua Wang & Peitao Lü

  2. Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China

    Sheng Yu

  3. Haikou Experimental Station, National Key Laboratory for Tropical Crop Breeding, Chinese Academy of Tropical Agricultural Sciences, Haikou, China

    Zhihao Cheng & Qiong Wu

  4. Laboratory of Medicinal Plant Biotechnology, School of Pharmaceutical Sciences, Zhejiang Chinese Medical University, Hangzhou, China

    Xiaojun Chang

  5. Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, China

    Xiaohui Wen, Jin Hu & Liangsheng Zhang

  6. Hainan Institute of Zhejiang University, Sanya, China

    Xiaohui Wen, Jin Hu & Liangsheng Zhang

  7. Fuzhou Institute of Oceanography, Minjiang University, Fuzhou, China

    Chen Zhang & Zonghua Wang

  8. Department of Biology, Saint Louis University, St. Louis, MO, USA

    Zhenguo Lin

  9. Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, Evry, France

    Jean-Marc Aury

  10. Department of Plant Biotechnology and Bioinformatics, Ghent University and VIB Center for Plant Systems Biology, Ghent, Belgium

    Yves Van de Peer

  11. Centre for Microbial Ecology and Genomics, Department of Biochemistry, Genetics and Microbiology, University of Pretoria, Pretoria, South Africa

    Yves Van de Peer

  12. College of Horticulture, Academy for Advanced Interdisciplinary Studies, Nanjing Agricultural University, Nanjing, China

    Yves Van de Peer

  13. State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Laboratory for Lingnan Modern Agriculture, Guangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Center, South China Agricultural University, Guangzhou, China

    Xiaofan Zhou

  14. Yunnan Seed Laboratory, Kunming, China

    Jihua Wang

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  1. Xiuxiu Li
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Contributions

L.Z. conceived and designed the project. P.L., Z.C., Y.Y., W.Z., S.X., Y.X., J.W. and H.L. collected the samples and extracted DNA and RNA. L.Z., P.L., J.W. and S.Y. coordinated the Illumina and PacBio sequencing. X.Z., M.J. and X. Chang assembled genomes and Hi-C data analyses. X.Z., C.Z. and X. Wang conducted protein-coding gene and repetitive sequence annotations. L.Z. and X.L. performed phylogenetic analyses. X.L., X. Chen and L.Z. performed comparative genomic analysis. X.L., X.Z., Q.W. and X. Wen performed the RNA-seq analysis. P.L. and S.Y. performed ChIP–seq experiments, DNase-seq experiments and bioinformatic analysis of ChIP–seq, DNase-seq and WGBS data. X.L., P.L., S.Y. and X.Z. wrote the manuscript draft. L.Z., P.L., S.Y., X.L., X.Z., Y.V.d.P., Z.L., Z.W., J.H. and J.-M.A. reviewed and revised the manuscript. All authors read and approved the manuscript.

Corresponding authors

Correspondence to Yves Van de Peer, Zonghua Wang, Xiaofan Zhou, Jihua Wang, Peitao Lü or Liangsheng Zhang.

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Extended data

Extended Data Fig. 1 Genome assemblies of Cavendish and Gros Michel.

a, BUSCO completeness assessments of the genome assemblies of Cavendish, Gros Michel, and four diploid wild banana species (Banksii, DH-Pahang, Zebrina, and Calcutta 4). Cavendish* was assembled by Busche et al.18. Zebrina v1.0 was assembled by Rouard et al.1, and Zebrina v2.0 was our assembly based on nanopore long-reads. The abbreviations of banana species refer to Fig. 1a. b, Macrosyntenic comparison of the entire Cavendish, Gros Michel and three diploid wild banana genomes (Banksii, DH-Pahang, and Zerbina), with each chromosome colored according to sub-genomes (Ban in blue, Dh in orange, and Ze in green).

Extended Data Fig. 2 Macrosyntenic comparison of the entire Cavendish and three diploid wild banana genomes: Banksii (a), DH-Pahang (b), and Zebrina (c).

Each chromosome set colored according to sub-genomes (Ban in blue, Dh in orange, and Ze in green). The abbreviations of banana species refer to Fig. 1a.

Extended Data Fig. 3 Macrosyntenic comparison of the entire Gros Michel and three diploid wild banana genomes: Banksii (a), DH-Pahang (b), and Zebrina (c).

Each chromosome set colored according to sub-genomes (Ban in blue, Dh in orange, and Ze in green). The abbreviations of banana species refer to Fig. 1a.

Extended Data Fig. 4 Examples of high-quality Cavendish and Zebrina genome assemblies.

a-d, NBS-LRR cluster, RLK cluster, RLP cluster, and RLP/LRR cluster on Ze03, Ze01, Dh10, and Ze10 of Cavendish, while not assembled in the previously published Cavendish assembly. Cavendish* was assembled by Busche et al.18. e and f, NBS-LRR cluster on chromosome 3 and RLP/LRR cluster on chromosome 10 of our assembled Zebrina v2.0 with length of 280 kb and 370 kb, while being two big gaps in the published Zebrina v1.0 (ref. 1). Each resistance gene was colored on micro-synteny plot (NBS-LRR in blue, RLK in pink, RLP in red, LRR in green, and other gene in yellow). The abbreviations of banana species refer to Fig. 1a.

Extended Data Fig. 5 Phylogenetic tree of banana RLPs involved in Foc race1-associated QTL (named as RLP locus)25.

The purple stars denote RLPs located in the Ze sub-genome, while the two red stars denote RLPs found only in the Ze sub-genome of Cavendish. The abbreviations of banana species refer to Fig. 1a.

Extended Data Fig. 6 A model of MaNAP4/5′ regulation of banana fruit ripening.

In the model, these genes directly regulated by MaNAP4/5 are key genes in the fruit ripening process.

Extended Data Fig. 7 Sub-genome dominance in the triploid banana genome.

a, Statistical comparison of categories of syntenic triad homoeolog expression bias. P-values were determined by one-way ANOVA with Tukey’s HSD test (n = 26 tissues of each category) within the suppression and dominance categories, and P-values less than 0.05 was highlighted in red. For boxplot in this study, the middle line represents the median, the lower and upper edges of the box represent the first and third quartiles, the end of the lower whisker represents the smallest value at most 1.5× inter-quartile range from the lower edge of the box, the end of the upper whisker represents the largest value at most 1.5× inter-quartile range from the upper edge of the box. b and c, Total number (b) and length (c) of DNase-hypersensitive sites (DHSs) detected in mature green and ripe fruits. d-f, Sub-genome distribution of MaNAP4/5 binding motifs (d), sites (e) and genes (f). g, Distribution of NBS-LRR resistance genes in the sub-genomes.

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Li, X., Yu, S., Cheng, Z. et al. Origin and evolution of the triploid cultivated banana genome. Nat Genet 56, 136–142 (2024). https://doi.org/10.1038/s41588-023-01589-3

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  • DOI: https://doi.org/10.1038/s41588-023-01589-3

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