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Recurrent neo-sex chromosome evolution in kiwifruit

Nature Plants volume 9, pages 393–402 (2023)Cite this article

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Abstract

Sex chromosome evolution is thought to be tightly associated with the acquisition and maintenance of sexual dimorphisms. Plant sex chromosomes have evolved independently in many lineages1,2 and can provide a powerful comparative framework to study this. We assembled and annotated genome sequences of three kiwifruit species (genus Actinidia) and uncovered recurrent sex chromosome turnovers in multiple lineages. Specifically, we observed structural evolution of the neo-Y chromosomes, which was driven via rapid bursts of transposable element insertions. Surprisingly, sexual dimorphisms were conserved in the different species studied, despite the fact that the partially sex-linked genes differ between them. Using gene editing in kiwifruit, we demonstrated that one of the two Y-chromosome-encoded sex-determining genes, Shy Girl, shows pleiotropic effects that can explain the conserved sexual dimorphisms. These plant sex chromosomes therefore maintain sexual dimorphisms through the conservation of a single gene, without a process involving interactions between separate sex-determining genes and genes for sexually dimorphic traits.

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Fig. 1: Movement of both sex-determining factors, SyGl and FrBy, and the formation of neo-MSYs around them.
Fig. 2: Rapid evolution of neo-MSYs via independent TE insertions.
Fig. 3: Pleiotropic functions of SyGl explain the conserved sexual dimorphisms.
Fig. 4: Model for recurrent neo-sex chromosome evolution in the genus Actinidia.

Data availability

All sequencing data from Illumina and three Actinidia genomes have been deposited in the DDBJ database: Sequence Read Archives database (BioProject ID PRJDB13958, Run ID DRR396285–DRR396297 for the Illumina sequencing reads; BRYE01000001–BRYE01000030 for the A. arguta genome; BRYF01000001–BRYF01000030 for the A. polygama genome; BRYG01000001–BRYG01000029 for the A. rufa genome).

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Acknowledgements

We thank L. Comai (Department of Plant Biology and Genome Center, University of California, Davis, USA) for discussion and comments on this study and K. Miyata (Board of Education of Miyoshi city, Tokushima, Japan) for sampling of native Actinidia germplasm collections. This work was supported by PRESTO from Japan Science and Technology Agency (grant no. JPMJPR20Q1) and Grant-in-Aid for Transformative Research Areas (A) from JSPS (grant nos 22H05172 and 22H05173) to T.A.

Author information

Author notes

  1. These authors contributed equally: Takashi Akagi, Erika Varkonyi-Gasic.

Authors and Affiliations

  1. Graduate School of Environmental and Life Science, Okayama University, Okayama, Japan

    Takashi Akagi, Kanae Masuda, Naoko Fujita, Eriko Kuwada & Koichiro Ushijima

  2. Japan Science and Technology Agency (JST), PRESTO, Kawaguchi-shi, Japan

    Takashi Akagi

  3. The New Zealand Institute for Plant and Food Research Limited (PFR), Auckland, New Zealand

    Erika Varkonyi-Gasic, Daniel Mertten, Paul Datson & Andrew C. Allan

  4. Kazusa DNA Research Institute, Kazusa-Kamatari, Kisarazu, Japan

    Kenta Shirasawa

  5. The New Zealand Institute for Plant and Food Research Limited (PFR), Christchurch, New Zealand

    Andrew Catanach

  6. Department of Plant Biology and Genome Center, University of California Davis, Davis, CA, USA

    Isabelle M. Henry

  7. The Kiwifruit Breeding Centre, Auckland, New Zealand

    Paul Datson

  8. Faculty of Agriculture, Kagawa University, Miki, Kagawa, Japan

    Kenji Beppu & Ikuo Kataoka

  9. School of Biological Sciences, University of Auckland, Auckland, New Zealand

    Andrew C. Allan

  10. Institute of Ecology and Evolution, University of Edinburgh, Edinburgh, UK

    Deborah Charlesworth

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Contributions

T.A., D.C. and I.K. conceived the study. T.A., E.V.-G., A.C., I.M.H. and D.C. designed the experiments. T.A., E.V.-G., A.C., K.S., K.M., N.F. and E.K. conducted the experiments. T.A., E.V.-G., A.C., K.S., P.D., D.M., K.M. and N.F. analysed the data. T.A., E.V.-G., K.S., I.M.H., P.D., K.U., K.B., A.C.A. and I.K. contributed to the plant resources and facilities. T.A., E.V.-G., A.C., I.M.H., D.C. and I.K. drafted the manuscript. All authors approved the manuscript.

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Correspondence to Takashi Akagi.

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Extended data

Extended Data Fig. 1 Conserved sexual dimorphisms in a wide variety of Actinidia species.

a, Representative female and male flowers in Actinidia species (from a segregated F1 population of A. chinensis x A. rufa, named KE-population in Akagi et al. 2018). Male flowers frequently form big clusters. B Floral shoots of four Actinidia species: A. chinensis, A. rufa, A. polygama, and A. arguta var. hypoleuca. Males produced more flower buds (fb) than female. This tendency is thought to be linked to two factors, increased number of flowers per inflorescence in male than in female (c), and increased number of floral nodes per shoot in male than in female (d). *p < 0.05, **p < 0.01, ***p < 0.001 Student’s t-test (biological replicates N = 10 for c, N = 5 for d).

Extended Data Fig. 2 Genome-wide syntenic relationships among A. chinensis, A. rufa, A. polygama, and A. arguta.

Syntenic blocks were defined based on conserved physical order of homologous gene pairs (<1e-50), using MCSanX (Wang et al. 2012) with default parameters. Basic collinearity was conserved amongst the four species for most chromosomes, although some chromosomes exhibited large scale inversions or translocations (for example, Chr19 and 23).

Extended Data Fig. 3 Genetic evidence for transition of the sex determining regions in the genus Actinidia.

Circos plots showing the genomic locations and significance (–log10 P values) of SNPs segregating with sex. These SNPs were identified after mapping reads of interspecific hybrid populations to different genome assemblies. a-d, Reads from populations CR (A. chinensis X A. rufa) (a), CM (A. chinensis X A. arguta var. melanandra) (b), CP (A. chinensis X A. arguta var. purpurea) (c) and CV (A. chinensis X A. valvata) (d) were aligned to the cv. Russell male A. chinensis genome assembly (Tahir et al., 2022). In this assembly, the sex determining region is located on the edge of chr. 25. e, Reads from population CR was aligned to the de novo assembled A. rufa genome. f-g, Reads from populations CM (f) and CP (g) were aligned to the de novo assembled A. arguta genome. h, Reads from population CV was aligned to the de novo assembled A. polygama genome. i-k, Linkage maps of populations CR (i), CM (j), and CP (k), are consistent with the results that the sex determining genes are located on Chr. 4 and Chr. 3 in A. rufa and A. arguta, respectively. l, Summary of the location of the sex determining regions (or sex chromosomes), based on these genomic and genetic analyses.

Extended Data Fig. 4 Sequence contexts of the sex determining regions in Chr25 of A. chinensis and A. polygama.

a-b, close-up of the Y-haplotype region of Chr25 in A. chinensis. a, An approximately 1.3 Mb region (putative MSY) exhibited mostly male-specific coverage of genomic reads. b, Synteny between Y- and X-haplotypes. Green bands indicate predicted genes. c, close-up view of the Chr25 Y-haplotype region in A. polygama. The MSY corresponds to a ~1.1 Mb region.

Extended Data Fig. 5 No synteny is conserved amongst the MSYs of four Actinidia species.

a, Syntenic dotplots between sex determining regions of A. chinensis and A. polygama, in Chr25. Although PAR regions exhibited significant collinearity, no long syntenic blocks were observed within the MSYs. b-c, Syntenic dotplot of the neo-sex determining regions, Chr3 in A. arguta (b) and Chr4 in A. rufa (c), against A. chinensis Chr25. d-e, Synteny analyses between the two neo-sex determining regions in A. arguta and A. rufa. No collinearity was detected, except for the presence of three conserved genes in the MSYs, Shy Girl, Friendly Boy, and YFT. Green bands indicate predicted genes (not including TE-like genes) for panel e.

Extended Data Fig. 6 Dynamic inversions of the three conserved genes in the MSYs of four Actinidia species.

Physical location of the three conserved genes, Shy Girl (SyGI, magenta), Friendly Boy (FrBy, light green), and Y-encoded FT-like (YFT, orange) genes in the MSYs of 4 Actinidia species. Their physical orders were different in all 4 species, implying frequent lineage-specific inversions.

Extended Data Fig. 7 TE enrichments in neo-MSY were not observed in the counterpart region in X chromosome.

a, Distribution of four TE classes (LTR-unknown, CACTA, hAT, and Helitron) in the A. rufa Y- and X-chromosomes (Chr 4), surrounding the neo-MSY. b, Distribution of Gypsy TE in the A. arguta Y- and X-chromosomes (Chr 3), surrounding the neo-MSY. Hyper enrichment of these TEs was specific to the neo-MSY in both species.

Extended Data Fig. 8 Shy Girl is solely explainable for most of the representative sexual dimorphisms in the genus Actinidia.

a, Disruptive mutations in the sygl lines. Red arrows indicated the gRNA sequences used for gene-editing. b-h, Sexual dimorphism traits are comparable between sygl gene-edited A. chinensis cv. Bruce and female A. chinensis cv. Hort16A grown in glasshouse conditions. (b, c) Solitary flowers with aborted bracts and lateral flower initials (arrows) in sygl and female lines. (d) Terminal and lateral flowers and multiple bracts (orange arrows) in male lines. (e) Comparison of floral node numbers in glasshouse-grown female, sygl and male A. chinensis. (f, g) Typical sygl and female shoots bearing fruit after pollination. (h) Schematic representation of the number of lateral shoots (horizontal axis) and position of vegetative (green) and floral nodes (yellow) on lateral shoots (vertical axis) in representative male, hermaphrodite sygl (gene-edited) and female lines.

Extended Data Fig. 9 Transcriptomic characterization of flower buds in comparison of the original male and the sygl (edited) lines.

a, Principal component analysis (PCA) of gene expression profiles in inflorescences of male and sygl hermaphrodite lines. Day 0 and day 4 represented embryonic inflorescence from dormant and breaking buds, respectively. Day 10 and day 14 represented inflorescences developing in leaf axils of expanding shoots. b, Representative images demonstrating early inflorescence development. Comparable development was observed in male and sygl lines with dome shaped meristems (dsm) and early inflorescence (inf) and bract (br) development at day 0, initiation of lateral flowers (lf) and sepals (s) at day 4, and presence of lateral and terminal flowers (tf) at day 10, but only terminal and aborted lateral flowers (alf) were present in sygl lines at day 14. c, Heatmap and hierarchical clustering of the DEGs between the male and the sygl-edited hermaphrodite inflorescences. Clust 2 (d) and Clust 5 (f) include genes upregulated in the sygl-edited hermaphrodite during the time period of day 4 to 10, and constantly downregulated in the sygl-edited hermaphrodite for the time period from day 0 to 14, respectively (Supplementary Data S5). GO analysis of Clust2 (e), and Clust5 (g).

Extended Data Fig. 10 Evolutionary topology of HB21/40/53-MeGI-Vrs1-like genes and their functional conservation.

Maximum-likelihood (ML)-based phylogenetic analysis of HB21/40/53-MeGI-Vrs1 orthologs including Acc06091 from the kiwifruit genome, which is a DEG nested into Clust 5 (see Extended Data Fig. 9). Three clades of angiosperms (Asterid, Rosid, and Monocot) are shown in different colors. MeGI silencing by the Y-encoded OGI gene is responsible for development of trifurcated cyme-like male, instead of solitary female flowers in persimmon (Asterid, blue shade), absence of HB21, HB40 and HB53 is associated with a highly branched phenotype in Arabidopsis (Rosid, green shade), and absence of Vrs1 gives rise to six-rowed instead of wild-type two-rowed spike in barley (Monocot, yellow shade). Consistently, differential expression of Acc06091 is correlated with variation in branching in male vs sygl inflorescences.

Supplementary information

Reporting Summary

Supplementary Data

Supplementary Data 1: Genome assembly qualities. Supplementary Data 2: Genome-wide repeats statistics. Supplementary Data 3: MSY gene lists in four Actinidia species. Supplementary Data 4: TE counts in MSYs of four Actinidia species. Supplementary Data 5: List of the DEGs in Clusters 2 and 5.

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Akagi, T., Varkonyi-Gasic, E., Shirasawa, K. et al. Recurrent neo-sex chromosome evolution in kiwifruit. Nat. Plants 9, 393–402 (2023). https://doi.org/10.1038/s41477-023-01361-9

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