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Chromosome-level genomes of three key Allium crops and their trait evolution

Nature Genetics volume 55, pages 1976–1986 (2023)Cite this article

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An Author Correction to this article was published on 14 December 2023

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Abstract

Allium crop breeding remains severely hindered due to the lack of high-quality reference genomes. Here we report high-quality chromosome-level genome assemblies for three key Allium crops (Welsh onion, garlic and onion), which are 11.17 Gb, 15.52 Gb and 15.78 Gb in size with the highest recorded contig N50 of 507.27 Mb, 109.82 Mb and 81.66 Mb, respectively. Beyond revealing the genome evolutionary process of Allium species, our pathogen infection experiments and comparative metabolomic and genomic analyses showed that genes encoding enzymes involved in the metabolic pathway of Allium-specific flavor compounds may have evolved from an ancient uncharacterized plant defense system widely existing in many plant lineages but extensively boosted in alliums. Using in situ hybridization and spatial RNA sequencing, we obtained an overview of cell-type categorization and gene expression changes associated with spongy mesophyll cell expansion during onion bulb formation, thus indicating the functional roles of bulb formation genes.

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Fig. 1: Evolution of Allium and African lily genomes.
Fig. 2: Comparative genomic analyses.
Fig. 3: Insights into allicin/isoallicin biosynthesis.
Fig. 4: Spatial RNA-seq reveals spatial distribution of gene expression in metabolic process and onion bulb formation.
Fig. 5: Evolution of genes involved in bulb formation in Allium plants and expression pattern divergence.

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Data availability

The raw sequencing data of onion, garlic, Welsh onion and Africa lily were deposited in the National Center for Biotechnology Information Sequence Read Archive under the accession PRJNA948806 and in the National Genomics Data Center (https://ngdc.cncb.ac.cn/?lang=en) under the accession PRJCA016760. The assemblies of the four genomes reported in this paper have been deposited in the National Center for Biotechnology Information under accessions JASDDO000000000, JASFAV000000000, JASFAW000000000, JASFAX000000000 and in the Genome Warehouse in National Genomics Data Center128,129, Beijing Institute of Genomics, Chinese Academy of Sciences/China National Center for Bioinformation, under accession GWHCBHY00000000, GWHCBHZ00000000, GWHCBIA00000000 and GWHCBIB00000000 that are publicly accessible at https://ngdc.cncb.ac.cn/gwh.

Code availability

All software used in the study are publicly available on the Internet as described in the Methods and Reporting Summary.

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Acknowledgements

We thank M. J. Havey from the Department of Horticulture, University of Wisconsin (Madison, WI, USA) for providing the onion seeds of the doubled haploid line and L. Cui from the Liaoning Academy of Agricultural Sciences (Shenyang, Liaoning, China) for providing the inbred lines of Welsh onion. We thank Y. Gu, L. Chen, Q. Lin, L. Chen, B. Mu, H. Sun, X. Wei, J. Li, S. Li, H. Lu and S. Zhang for general technical assistance or discussion. We thank G. Zhang from Zhejiang University and K. Wang from Northwestern Polytechnical University (NWPU) for their comments and suggestions when preparing our manuscript. We thank Y. Zeng from BGI-Shenzhen for sharing his idea on Allium genome study. This work was supported by the Thousand Talents Plan (5113190037), the Talents Team Construction Fund of NWPU and the Fundamental Research Funds for the Central Universities (3102019JC007) to J.C.; the Talents Team Construction Fund of NWPU and the Projects of Interdisciplinary of NWPU (0202022GH0306) to W.W.; National Natural Science Foundation of China (21801206), the Joint Research Funds of Department of Science & Technology of Shaanxi Province and NWPU (2020GXLH-Z-015) to Z.R.; Guangdong Provincial Key Laboratory of Genome Read and Write (2017B030301011) to X.X.

Author information

Author notes

  1. These authors contributed equally: Fei Hao, Xue Liu, Botong Zhou, Zunzhe Tian, Lina Zhou, Hang Zong, Jiyan Qi, Juan He.

  2. These authors jointly supervised this work: Jing Cai, Wen Wang, Richard C. Macknight, Hui Yang, Xun Xu.

Authors and Affiliations

  1. School of Ecology and Environment, Northwestern Polytechnical University, Xi’an, China

    Fei Hao, Xue Liu, Botong Zhou, Zunzhe Tian, Lina Zhou, Hang Zong, Jiyan Qi, Juan He, Yongting Zhang, Peng Zeng, Qiong Li, Kai Wang, Yingmei Peng, Wenbo Zhu, Wen Wang & Jing Cai

  2. Center of Special Environmental Biomechanics & Biomedical Engineering, School of Life Sciences, Northwestern Polytechnical University, Xi’an, China

    Fei Hao & Hui Yang

  3. State Key Laboratory of Agricultural Genomics, BGI, Shenzhen, China

    Keke Xia, Xing Guo, Li Li, Wenwen Shao, Shengkang Li & Xun Xu

  4. BGI Research, Wuhan, China

    Xing Guo

  5. BGI Research, Beijing, China

    Bohan Zhang

  6. Lianyungang Academy of Agricultural Sciences, Lianyungang, China

    Haifeng Yang, Linchong Hui & Wei Chen

  7. National Engineering Research Center for Non-Food Biorefinery, Guangxi Academy of Sciences, Nanning, China

    Lixin Peng

  8. Frontiers Science Center for Flexible Electronics (FSCFE), Shaanxi Institute of Flexible Electronics (SIFE) & Shaanxi Institute of Biomedical Materials and Engineering (SIBME), Northwestern Polytechnical University, Xi’an, China

    Feipeng Liu & Zi-Qiang Rong

  9. The New Zealand Institute for Plant and Food Research, Christchurch, New Zealand

    John A. McCallum

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

    Zhen Li

  11. Guangdong Provincial Key Laboratory of Genome Read and Write, Shenzhen, China

    Xun Xu

  12. Department of Biochemistry, University of Otago, Dunedin, New Zealand

    Richard C. Macknight

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  1. Fei Hao
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  2. Xue Liu
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  3. Botong Zhou
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Contributions

F.H. and J.C. managed the project. J.C., W.W., R.M., H.Y. and X.X. conceived the study. F.H. and J.C. wrote the manuscript with contributions from all other authors. B.Z. and H.Z. were responsible for genome assembly into contigs and Hi-C scaffolding. X.L. handled genome annotation and analysis of phylogeny, transcriptome, gene family evolution, allicin/isoallicin pathway and immune system. B.Z., Z.T., X.L. and Z.L. were responsible for the analysis of whole-genome synteny and whole-genome duplication (WGD). Z.T. and P.Z. handled repeat annotation and conducted analysis of LTR retrotransposons. L.Z., J.H., J.Q., Q.L., Y.Z. and K.W. were responsible for in situ hybridization experiments. L.Z. focused on studying the evolution and formation of tunicated bulbs. H.Z. was responsible for genome evaluation and conducted ultra-high-performance liquid chromatography/tandem mass spectrometry (UHPLC-MS/MS) analysis. H.Z., K.X., X.G., L.L., W.S., B.Z., S.L. and L.P. conducted spatial RNA sequencing and analyzed spatial transcriptome data. Y.P., W.Z., F.L., Z.R. and J.M. were in charge of plant material collection and DNA/RNA preparation. H.Y., L.H. and W.C. supervised genome sequencing and library construction and also collected plant material for bulb development.

Corresponding authors

Correspondence to Xun Xu, Hui Yang, Richard C. Macknight, Wen Wang or Jing Cai.

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Nature Genetics thanks Zhangjun Fei and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Genome overview and phylogenetic analyses of Allium species and African lily, related to Fig. 1.

a, Overview of genomes of Allium species and African lily: track a corresponds to chromosome length. From b to d, three rings represent density distribution of different genomic features, including coding gene, GC, and repeat sequences, respectively. Track e corresponds to syntenic blocks. b, Species tree by summarizing each gene tree with Astral. c, Phylogenies from three supergene matrice, each of which was constructed by concatenating ortholog gene sets defined by reciprocal best hit (RBH) by BLAST, single-copy genes (SCG) identified using OrthoFinder and single-copy genes (SCG) identified using OrthoMCL, respectively. d, Single-copy genes identified using OrthoMCL. e, Single-copy genes identified using OrthoFinder. f, Relative evolutionary rate comparison among three Allium species and African lily.

Extended Data Fig. 2 Analysis of repetitive sequences in three Allium species and African lily.

a, Overall composition of repetitive elements in different genomes. DNA, DNA element; LINE, long interspersed nuclear element; LTR, long terminal repeat transposable element; SINE, short interspersed nuclear element. Divergence distribution of Copia (b) and Gypsy (c) retrotransposons in four assembled genomes. X-axis represents divergence measured in percentage of sequence differences with consensus in TE library. d, Phylogenetic relationships of Gypsy and Copia retrotransposon domains across genomes of asparagus, rice, and four species sequenced in this study (Supplementary Data 3 for alignments of sequences and a version with support values on branches).

Extended Data Fig. 3 Evolution of gene families, related to Fig. 3.

a, Pie diagram on each branch of tree represents the proportion of gene families undergoing gain (green) or loss (red) events. Numbers below pie diagram denote total number of expanded and contracted gene families. b, Distribution of single-copy, multiple-copy, unique, and other orthologs in 10 plant species, and three columns on right show number of genes in families, family number, and average genes per family in 10 plant species. c, Point-line and Venn diagrams represent shared and unique gene families among 10 species or four closely related Amaryllidaceae species (Welsh onion, garlic, onion, and African lily). Each number represents number of gene families. d, Significant GO terms of molecular function, biological process, and cellular component enriched in expanded gene families in ancestral branch of three Allium plants. e, Significant KEGG pathways enriched in expanded gene families in ancestral branch of three Allium plants. f, Network diagram of significant KEGG pathways enriched in expanded gene families in ancestral branch of three Allium plants. GO terms or KEGG pathways probably related to alliinase, plant immune system, and bulb development discussed in this study are labeled with red arrows. The p values (unadjusted, one side) presented in d and e were calculated using the hypergeometric test.

Extended Data Fig. 4 Clustering of alliinase gene family in Allium and outgroup species, related to Fig. 3.

Phylogenetic analysis of alliinase gene family, with alliinase genes forming 15 distinct groups (A–O). Bootstrap values are shown on each branch. For the alliinase gene family, we constructed a gene tree using standard maximum-likelihood phylogenetic analysis implemented in IQ-TREE with default parameters and 1,000 bootstraps.

Extended Data Fig. 5 Clustering of lachrymatory factor synthase gene family (LFS) in Allium, related to Fig. 3.

Phylogenetic analysis of LFS gene family, with LFS genes forming eight distinct groups (A–H). Bootstrap values are shown on each branch. For LFS gene family, we constructed a gene tree using standard maximum-likelihood phylogenetic analysis implemented in IQ-TREE with default parameters and 1,000 bootstraps.

Extended Data Fig. 6 Location of genes associated with allicin/isoallicin biosynthesis on chromosomes.

Localization of genes related to allicin/isoallicin biosynthetic pathways on chromosomes of a, Welsh onion, b, garlic, and c, onion.

Extended Data Fig. 7 Gene expression changes upon pathogen infection in onion.

a, Relative expression levels of alliin biosynthesis genes in transcriptome of fungal-infected blades. b, Significant KEGG pathways enriched in up-regulated genes in response to fungal infection. Comparing gene expression profiles between leaf blades of fungal-infected and healthy plants, we identified 1,035 up-regulated genes during infection. c, Relative expression levels of alliin biosynthesis genes after artificial injury and exposure to bacterial culture by qRT-PCR. d and e, Relative expression levels of homologous genes of alliin biosynthesis genes in Arabidopsis thaliana. TPM: transcripts per kilobase of exon model per million mapped reads. Transcriptome data were downloaded from https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE142747. Four-week-old Arabidopsis thaliana plant leaves were infiltrated with sterile water (Mock) or different Pst strains, then harvested at 3 or 6 h after infiltration. Two bacterial strains, P. s. pv. tomato (Pst) DC3000 (avrRpt2), which activates RPS2 (resistance to P. syringae 2)-dependent effector-triggered immunity (ETI) and pattern-triggered immunity (PTI), and Pst DC3000 without ‘avirulent’ effector to activate PTI only in wild-type plants. Data presented in a, c–e are mean ± standard error of three or four independent experiments, and bars with p values were significantly different based on t test (two-sided). The p values (unadjusted, one side) presented in b were calculated using the hypergeometric test.

Extended Data Fig. 8 Cell marker genes in different clusters, related to Fig. 4.

a, Dot plot showing expression profiles of marker genes in all 14 cell clusters. ID of cell marker genes in onion are below x-axis. Expression level for each bin was calculated by scaled number of molecular identifiers (MIDs) for each marker gene. Average expression (AE) level of all bins in each cell cluster is denoted by dot color. Percentage of bins expressing marker gene (PE) in each cell cluster is denoted by dot size. b, Spatial expression patterns of cell marker genes from in situ hybridization (left) and spatial RNA-seq (right), showing that in situ hybridization and stereo-seq data were highly consistent and supported cell categorization. Scale bars equal to 1 mm for in situ hybridization, 800 um for spatial RNA-seq. Number in parenthesis represents number of samples with same signal pattern over total number of samples.

Extended Data Fig. 9 Spatial expression patterns of genes related to synthesis of flavonoid compounds and cuticular wax, related to Fig. 4e,f.

a, Spatial expression patterns of genes (CHS, CHIL, CHI, F3H, F3'H, LTP2 and LTP3) in different onion bulb development stages based on stereo-seq data. Co-expression of genes in epidermal cells was observed in all samples, showing that flavonoid and cuticular wax biosynthesis is mainly active in epidermal cells. b, Expression pattern of LTP in leaf base of onion by RNA in situ hybridization. Lower panels are images with reverse colors produced by ImageJ based on images in upper panels. Expression patterns based on in situ hybridization confirmed LTP results in Fig. 4f from large-scale Stereo-seq analysis. Scale bars equal to 800 μm for a, 1 mm for b. Number in parenthesis represents number of samples with same signal pattern over total number of samples.

Extended Data Fig. 10 Spongy mesophyll cell lineages and onion bulb formation, related to Figs. 4g,5.

a, Visualization of spongy mesophyll cell lineages, including six sections at three development stages. Sections from different stages and individuals show similar patterns of spongy mesophyll cell development: spongy mesophyll cells from inner to outer layer, and for each layer from base to top and from outer to inner, represent early to late points along the expansion process. Progression of numbers from small to large indicates pseudotime sequence, reflecting progression of spongy mesophyll cell expansion. Same color pattern is also used in panel b. b and c, UMAP dimensionality reduction projection of spongy mesophyll cells grouped by pseudotime scores and sections, respectively. General pattern of pseudotime increasing from left to right can be seen in panel b, but no clear pattern can be seen in c, suggesting that expansion of spongy mesophyll cell development is a fundamentally short process, starting asynchronously at different development stages as indicated in panel a. d and e, Spatial visualization of expression of indicated genes related to onion bulb formation. Scale bars equal to 800 μm for a, d and e.

Supplementary information

Supplementary Information

Supplementary Results 1–6, Supplementary Methods and Supplementary Figs. 1–20.

Reporting Summary

Supplementary Tables

Supplementary Tables 1–54.

Supplementary Data 1

Sequence alignment for the analysis of positive selection of genes in the three Allium species.

Supplementary Data 2

Sequence alignment of alliinase gene family and LFS gene family.

Supplementary Data 3

Sequence alignment of phylogenetic relationships of Gypsy and Copia retrotransposon domains across genomes of asparagus, rice and four species sequenced in this study, and a version with support values on branches.

Supplementary Data 4

Sequence alignment of positively selected or rapidly evolving genes involved in bulb formation in onion or garlic.

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Hao, F., Liu, X., Zhou, B. et al. Chromosome-level genomes of three key Allium crops and their trait evolution. Nat Genet 55, 1976–1986 (2023). https://doi.org/10.1038/s41588-023-01546-0

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