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Near-gapless and haplotype-resolved apple genomes provide insights into the genetic basis of rootstock-induced dwarfing

Nature Genetics volume 56, pages 505–516 (2024)Cite this article

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Abstract

Dwarfing rootstocks have transformed the production of cultivated apples; however, the genetic basis of rootstock-induced dwarfing remains largely unclear. We have assembled chromosome-level, near-gapless and haplotype-resolved genomes for the popular dwarfing rootstock ‘M9’, the semi-vigorous rootstock ‘MM106’ and ‘Fuji’, one of the most commonly grown apple cultivars. The apple orthologue of auxin response factor 3 (MdARF3) is in the Dw1 region of ‘M9’, the major locus for rootstock-induced dwarfing. Comparing ‘M9’ and ‘MM106’ genomes revealed a 9,723-bp allele-specific long terminal repeat retrotransposon/gypsy insertion, DwTE, located upstream of MdARF3. DwTE is cosegregated with the dwarfing trait in two segregating populations, suggesting its prospective utility in future dwarfing rootstock breeding. In addition, our pipeline discovered mobile mRNAs that may contribute to the development of dwarfed scion architecture. Our research provides valuable genomic resources and applicable methodology, which have the potential to accelerate breeding dwarfing rootstocks for apple and other perennial woody fruit trees.

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Fig. 1: Rootstock genetic divergence and population structure.
Fig. 2: Genome phasing and ASE analysis.
Fig. 3: Genome comparison between ‘M9’ and ‘MM106’.
Fig. 4: A LTR-RT insertion with MdARF3 gene associated with dwarfing traits.
Fig. 5: Identification of mobile mRNAs.

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Data availability

All raw sequencing reads of PacBio HiFi, Hi-C, Illumina, Iso-Seq and RNA-seq have been deposited in the NCBI database with the BioProject PRJNA814760 (Supplementary Table 32). Genome assemblies have been deposited in the NCBI under accession JAXBLQ000000000 (Fuji haploid consensus genome), JAXBLN000000000 (M9 haploid consensus genome) and JAXBLK000000000 (MM106 haploid consensus genome) for the haploid consensus genome and JAXBLO000000000 (Fuji haplome A genome), JAXBLP000000000 (Fuji haplome B genome), JAXBLL000000000 (M9 haplome A genome), JAXBLM000000000 (M9 haplome B genome), JAXBLI000000000 (MM106 haplome A genome) and JAXBLJ000000000 (MM106 haplome B genome) for the haplotype-resolved genome. The assembly and annotation files have also been submitted to the National Genomics Data Center (https://ngdc.cncb.ac.cn/) with the BioProject number PRJCA010465. The genome assembly and annotation files are also available at Figshare (https://figshare.com/projects/Near-gapless_and_haplotype-resolved_apple_genomes_provide_insights_into_the_genetic_basis_of_rootstock-induced_dwarfing/190926). Source data are provided with this paper.

Code availability

Computational pipelines related to identification of mobile mRNAs can be accessed through GitHub (https://github.com/simoncchu/RNAGlass) and Zenodo (https://zenodo.org/records/10146626)98.

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Acknowledgements

This work was supported by the earmarked fund for the China Agricultural Research System (CARS-27 to Z.H.), 2115 Talent Development Program of China Agricultural University, the National Key Research and Development Program (2018YFD1000100 to W.L.), the National Natural Science Foundation of China (32172522 to Z.H. and 31801823 to W.L.) 111 Project (B17043) and the Growing Futures Fund from the New Zealand Institute for Plant and Food Research Limited.

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Author notes

  1. These authors contributed equally: Wei Li, Chong Chu, Hui Li, Hengtao Zhang.

Authors and Affiliations

  1. Institute for Horticultural Plants, China Agricultural University, Beijing, China

    Wei Li, Hui Li, Haochen Sun, Shiyao Wang, Zijun Wang, Yuqi Li, Bowen Zhou, Xingqiang Fan, Yao Xiong, Yi Wang, Xuefeng Xu & Zhenhai Han

  2. Department of Biomedical Informatics, Harvard Medical School, Boston, MA, USA

    Chong Chu

  3. Zhengzhou Fruit Research Institute, Chinese Academy of Agricultural Sciences, Zhengzhou, China

    Hengtao Zhang

  4. The New Zealand Institute for Plant and Food Research Limited (Plant & Food Research), Motueka, New Zealand

    Toshi M. Foster

  5. The New Zealand Institute for Plant and Food Research Limited (Plant & Food Research), Palmerston North, New Zealand

    Elena López-Girona

  6. Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Chinese Academy of Agricultural Sciences, Shenzhen, China

    Jiaxin Yu

  7. Department of Plant Science and Landscape Architecture, University of Connecticut, Storrs, CT, USA

    Yi Li

  8. College of Horticulture, Shenyang Agricultural University, Shenyang, China

    Yue Ma

  9. State Key Laboratory of North China Crop Improvement and Regulation; Key Laboratory of Crop Growth Regulation of Hebei Province, College of Agronomy, Hebei Agricultural University, Baoding, China

    Ke Zhang

  10. College of Information Science and Technology, Beijing University of Chemical Technology, Beijing, China

    Yongming Han

  11. The New Zealand Institute for Plant and Food Research Limited (Plant & Food Research), Auckland, New Zealand

    Cecilia H. Deng

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  1. Wei Li
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Contributions

Z.H., W.L. and C.C. conceived and designed the project. W.L., Z.H., H.Z., H.L., Y.W. and H.S. collected and provided plant materials. W.L., C.C., H.L., H.S., C.H.D., S.W., Z.W., J.Y. and Y.X. assembled the genome and performed ASE analysis. C.C., W.L., H.L., C.H.D., H.S., Z.W. and Y.H. developed and validated the new pipeline for mobile mRNA identification. W.L., Yuqi Li and S.W. analyzed and interpreted population resequencing data. W.L., H.L., H.Z., Y.M., K.Z., B.Z., X.F., T.M.F. and E.L.-G. performed the validation and transformation experiments. Z.H., W.L., C.C., C.H.D., T.M.F., E.L.-G, H.L., H.Z., Y.W., H.S., S.W., Z.W. and Yuqi Li contributed to writing the paper. Yi Li and X.X. provided suggestions on data analysis and editing the paper. All authors read and approved the paper.

Corresponding authors

Correspondence to Chong Chu, Cecilia H. Deng, Yi Wang or Zhenhai Han.

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Nature Genetics thanks Patrick Edger, Zhongchi Liu and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Notes 1–5, Methods, Figs. 1–24 and supporting data for Supplementary Fig. 21 (unprocessed gels).

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Supplementary Tables 1–32.

Source data

Source Data Fig. 4

Unprocessed gels for Fig. 4c.

Source Data Fig. 4

Statistical source data for Fig. 4g,i.

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Li, W., Chu, C., Li, H. et al. Near-gapless and haplotype-resolved apple genomes provide insights into the genetic basis of rootstock-induced dwarfing. Nat Genet 56, 505–516 (2024). https://doi.org/10.1038/s41588-024-01657-2

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