Abstract
Apomixis, the clonal formation of seeds, is a rare yet widely distributed trait in flowering plants. We have isolated the PARTHENOGENESIS (PAR) gene from apomictic dandelion that triggers embryo development in unfertilized egg cells. PAR encodes a K2-2 zinc finger, EAR-domain protein. Unlike the recessive sexual alleles, the dominant PAR allele is expressed in egg cells and has a miniature inverted-repeat transposable element (MITE) transposon insertion in the promoter. The MITE-containing promoter can invoke a homologous gene from sexual lettuce to complement dandelion LOSS OF PARTHENOGENESIS mutants. A similar MITE is also present in the promoter of the PAR gene in apomictic forms of hawkweed, suggesting a case of parallel evolution. Heterologous expression of dandelion PAR in lettuce egg cells induced haploid embryo-like structures in the absence of fertilization. Sexual PAR alleles are expressed in pollen, suggesting that the gene product releases a block on embryogenesis after fertilization in sexual species while in apomictic species PAR expression triggers embryogenesis in the absence of fertilization.
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Data availability
Transcriptome data of 27 laser-assisted microdissected female gametophyte tissue samples of T. officinale are deposited in the ENA SRA database under accession no. PRJEB40645. Illumina HiSeq2500 paired end sequencing datasets of T. richardsianum, T. albidum, T. brevicorniculatum, T. brachyglossum, T. gratum, T. cylleneum, and T. koksaghyz are deposited in the ENA SRA database under accession no. PRJEB40739. The T. officinale ONT PromethION sequence reads, and the Illumina NovaSeq6000 reads from the overlap library are deposited in the ENA SRA database under accession no. PRJEB48186.
Code availability
Automated Human Readable Descriptions: https://github.com/groupschoof/AHRD
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Acknowledgements
We thank the following: T. Gerats (KeyGene) for essential vision and support; S. van Liere, S. Lecoulant, D. Valkenburg, A. Bergsma, M. Frescatada, W. van Rengs and C. Schol (all of KeyGene) for technical assistance; H. Schneiders, H. van der Poel, R. Hulzink, A. Wittenberg and A. Janssen (all of KeyGene) for DNA-sequencing and bioinformatics; S. Keshtkar, M. V. Boekschoten, H. Hackert, I. van der Meer, L. Berke, T. Zhao, H. van der Geest and J. van Haarst (all of Wageningen University & Research (WUR)) and J. A. Mol (Utrecht University) for advice and access to facilities; R. van den Bulk (WUR) for supporting institutional cooperation; R. Mank and KeyGene greenhouse staff for plant culturing; P. Bundock and M. de Both for critical reading and discussion of the manuscript; and J. Kirschner and J. Štěpánek (Institute of Botany, Průhonice), R. Vašut (Palacký University Olomouc) and R. van der Hulst (Solynta) and K. Verhoeven (Netherland Institute of Ecology) for supplying plant materials and taxonomic information. The pUBI::Cas9 construct was a kind gift of H. Puchta. The Dutch Research Council Applied and Engineering Sciences grant (no. 13700 (ParTool) to K.V., C.O., M.B. and M.E.S.). The elucidation of the Pilosella LOP locus was supported by a basic science grant from the New Zealand Foundation for Science and Technology. The formation of the Pilosella BAC library was supported in part by the Arizona Genome institute.
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P.J.V.D., K.V., R.H.M.O.d.C., C.J.U., D.R., S.O., M.P., A.V.T., R.B. and M.E.S. conceived and designed the project. C.J.U., K.V., D.R., S.O., C.O., T.R., J.F., K.J., S.M., M.B., R.B., A.C., S.E., C.W. and P.J.V.D. generated the experimental data. K.V., D.R., C.J.U., R.H.M.O.d.C., T.R., S.E.S., S.M., R.B., P.J.V.D. and M.E.S. analyzed the experimental data. D.R., K.V., S.M., W.X., E.D., K.N., E-J. B., C.J.U., P.J.V.D., R.B., M.E.S. and C.W. conducted the bioinformatic analysis. P.J.V.D., M.E.S., S.E.S., R.B. and C.J.U. wrote the manuscript with contributions from K.V., T.R., R.H.M.O.d.C. and D.R. All authors critically read and edited the manuscript.
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D.R., P.J.V.D., R.H.M.O.d.C., M.P., A.J.V.T., T.R., J.F., K.J., S.M., E.D., K.N. and E-J.B. are employees of KeyGene N.V. C.J.U. is a former employee of KeyGene N.V. S.E.S. is an employee of KeyGene Inc. These authors declare that they are bound by confidentiality agreements that prevent them from disclosing their competing interests in this work. The remaining authors declare no competing interests.
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Supplementary information
Supplementary Information
Supplementary Figs. 1–21, Tables 1–2, 4, 6–10, and 14–22, Notes 1–18, URLs, References, and original gel scan of Supplementary Fig. 11.
Supplementary Data 1
The sequence of the PAR haplotype.
Supplementary Data 2
The sequence of the sex1 haplotype.
Supplementary Data 3
The sequence of the sex2 haplotype.
Supplementary Data 4
The sequences of the 20 genes of the Ks and Ka analyses.
Supplementary Data 5
The sequences of the Taraxacum and Pilosella PAR alleles.
Supplementary Data 6
The sequences of the Taraxacum and Pilosella MITEs.
Supplementary Tables
Supplementary Tables 3a, 3b, 3c, 5, 11, 12 and 13.
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Underwood, C.J., Vijverberg, K., Rigola, D. et al. A PARTHENOGENESIS allele from apomictic dandelion can induce egg cell division without fertilization in lettuce. Nat Genet 54, 84–93 (2022). https://doi.org/10.1038/s41588-021-00984-y
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DOI: https://doi.org/10.1038/s41588-021-00984-y
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