A PARTHENOGENESIS allele from apomictic dandelion can induce egg cell division without fertilization in lettuce

Charles J. Underwood; Kitty Vijverberg; Diana Rigola; Shunsuke Okamoto; Carla Oplaat; Rik H.M. Op Den Camp; Tatyana Radoeva; Stephen E. Schauer; Joke Fierens; Kim Jansen; Sandra Mansveld; Marco Busscher; Wei Xiong; Erwin Datema; Koen Nijbroek; Evert-Jan Blom; Ross Bicknell; Andrew Catanach; Sylvia Erasmuson; Christopher Winefield; Arjen J. Van Tunen; Marcel Prins; Eric Schranz; Peter J. Van Dijk

doi:10.1038/s41588-021-00984-y

A PARTHENOGENESIS allele from apomictic dandelion can induce egg cell division without fertilization in lettuce

Charles J. Underwood, Kitty Vijverberg, Diana Rigola, Shunsuke Okamoto, Carla Oplaat, Rik H.M. Op Den Camp, Tatyana Radoeva, Stephen E. Schauer, Joke Fierens, Kim Jansen, Sandra Mansveld, Marco Busscher, Wei Xiong, Erwin Datema, Koen Nijbroek, Evert-Jan Blom, Ross Bicknell, Andrew Catanach, Sylvia Erasmuson, Christopher WinefieldArjen J. Van Tunen, Marcel Prins, Eric Schranz^*, Peter J. Van Dijk^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

75 Citations (Scopus)

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.

Original language	English
Pages (from-to)	84-93
Journal	Nature Genetics
Volume	54
Issue number	1
Early online date	6 Jan 2022
DOIs	https://doi.org/10.1038/s41588-021-00984-y
Publication status	Published - Jan 2022

Keywords

PRJEB40645
ERP124302

Access to Document

10.1038/s41588-021-00984-y

https://edepot.wur.nl/561757Licence: Taverne

Taraxacum officinale isolate A68: Raw sequence reads
Underwood, C. J. (Creator), Vijverberg, K. (Creator), Rigola, D. (Creator), Okamoto, S. (Creator), Oplaat, C. (Creator), Op Den Camp, R. H. M. (Creator), Radoeva, T. (Creator), Schauer, S. E. (Creator), Fierens, J. (Creator), Jansen, K. (Creator), Mansveld, S. (Creator), Busscher, M. (Creator), Xiong, W. (Creator), Datema, E. (Creator), Nijbroek, K. (Creator), Blom, E.-J. (Creator), Bicknell, R. (Creator), Catanach, A. (Creator), Erasmuson, S. (Creator), Winefield, C. (Creator), Van Tunen, A. J. (Creator), Prins, M. (Creator), Schranz, E. (Creator) & Van Dijk, P. J. (Creator), Keygene, 28 Oct 2021
https://www.ebi.ac.uk/ena/browser/view/PRJEB48186
Dataset
Investigation of the PAR gene conservation in Taraxacum germplasms
Underwood, C. J. (Creator), Vijverberg, K. (Creator), Rigola, D. (Creator), Okamoto, S. (Creator), Oplaat, C. (Creator), Op Den Camp, R. H. M. (Creator), Radoeva, T. (Creator), Schauer, S. E. (Creator), Fierens, J. (Creator), Jansen, K. (Creator), Mansveld, S. (Creator), Busscher, M. (Creator), Xiong, W. (Creator), Datema, E. (Creator), Nijbroek, K. (Creator), Blom, E.-J. (Creator), Bicknell, R. (Creator), Catanach, A. (Creator), Erasmuson, S. (Creator), Winefield, C. (Creator), Van Tunen, A. J. (Creator), Prins, M. (Creator), Schranz, E. (Creator) & Van Dijk, P. J. (Creator), Keygene, 13 Dec 2020
https://www.ebi.ac.uk/ena/browser/view/PRJEB40739
Dataset
Dandelion (Taraxacum officinale) female gametophyte cell transcriptomes
Underwood, C. J. (Creator), Vijverberg, K. (Creator), Rigola, D. (Creator), Okamoto, S. (Creator), Oplaat, C. (Creator), Op Den Camp, R. H. M. (Creator), Radoeva, T. (Creator), Schauer, S. E. (Creator), Fierens, J. (Creator), Jansen, K. (Creator), Mansveld, S. (Creator), Busscher, M. (Creator), Xiong, W. (Creator), Datema, E. (Creator), Nijbroek, K. (Creator), Blom, E.-J. (Creator), Bicknell, R. (Creator), Catanach, A. (Creator), Erasmuson, S. (Creator), Winefield, C. (Creator), Van Tunen, A. J. (Creator), Prins, M. (Creator), Schranz, E. (Creator) & Van Dijk, P. J. (Creator), Wageningen University & Research, 3 Dec 2020
https://www.ebi.ac.uk/ena/browser/view/PRJEB40645
Dataset

Gene found that produces unfertilized seeds
Schranz, E.
5/04/22 → 6/04/22
2 Media contributions
Press/Media: Research › Professional
Onderzoekers vinden gen in paardenbloem dat tot eiceldeling aanzet: ‘Dit kan grote gevolgen hebben voor de landbouw’
Schranz, E.
26/01/22
2 Media contributions
Press/Media: Research › Popular
Crucial gene discovered in dandelion
Busscher, M. & Xiong, W.
13/01/22 → 14/01/22
2 Media contributions
Press/Media: Research › Professional

Cite this

Underwood, C. J., Vijverberg, K., Rigola, D., Okamoto, S., Oplaat, C., Op Den Camp, R. H. M., Radoeva, T., Schauer, S. E., Fierens, J., Jansen, K., Mansveld, S., Busscher, M., Xiong, W., Datema, E., Nijbroek, K., Blom, E.-J., Bicknell, R., Catanach, A., Erasmuson, S., ... Van Dijk, P. J. (2022). A PARTHENOGENESIS allele from apomictic dandelion can induce egg cell division without fertilization in lettuce. Nature Genetics, 54(1), 84-93. https://doi.org/10.1038/s41588-021-00984-y

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title = "A PARTHENOGENESIS allele from apomictic dandelion can induce egg cell division without fertilization in lettuce",

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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author = "Underwood, {Charles J.} and Kitty Vijverberg and Diana Rigola and Shunsuke Okamoto and Carla Oplaat and {Op Den Camp}, {Rik H.M.} and Tatyana Radoeva and Schauer, {Stephen E.} and Joke Fierens and Kim Jansen and Sandra Mansveld and Marco Busscher and Wei Xiong and Erwin Datema and Koen Nijbroek and Evert-Jan Blom and Ross Bicknell and Andrew Catanach and Sylvia Erasmuson and Christopher Winefield and {Van Tunen}, {Arjen J.} and Marcel Prins and Eric Schranz and {Van Dijk}, {Peter J.}",

year = "2022",

month = jan,

doi = "10.1038/s41588-021-00984-y",

language = "English",

volume = "54",

pages = "84--93",

journal = "Nature Genetics",

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Underwood, CJ, Vijverberg, K, Rigola, D, Okamoto, S, Oplaat, C, Op Den Camp, RHM, Radoeva, T, Schauer, SE, Fierens, J, Jansen, K, Mansveld, S, Busscher, M, Xiong, W, Datema, E, Nijbroek, K, Blom, E-J, Bicknell, R, Catanach, A, Erasmuson, S, Winefield, C, Van Tunen, AJ, Prins, M, Schranz, E & Van Dijk, PJ 2022, 'A PARTHENOGENESIS allele from apomictic dandelion can induce egg cell division without fertilization in lettuce', Nature Genetics, vol. 54, no. 1, pp. 84-93. https://doi.org/10.1038/s41588-021-00984-y

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T1 - A PARTHENOGENESIS allele from apomictic dandelion can induce egg cell division without fertilization in lettuce

AU - Underwood, Charles J.

AU - Vijverberg, Kitty

AU - Rigola, Diana

AU - Okamoto, Shunsuke

AU - Oplaat, Carla

AU - Op Den Camp, Rik H.M.

AU - Radoeva, Tatyana

AU - Schauer, Stephen E.

AU - Fierens, Joke

AU - Jansen, Kim

AU - Mansveld, Sandra

AU - Busscher, Marco

AU - Xiong, Wei

AU - Datema, Erwin

AU - Nijbroek, Koen

AU - Blom, Evert-Jan

AU - Bicknell, Ross

AU - Catanach, Andrew

AU - Erasmuson, Sylvia

AU - Winefield, Christopher

AU - Van Tunen, Arjen J.

AU - Prins, Marcel

AU - Schranz, Eric

AU - Van Dijk, Peter J.

PY - 2022/1

Y1 - 2022/1

N2 - 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.

AB - 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.

KW - PRJEB40645

KW - ERP124302

U2 - 10.1038/s41588-021-00984-y

DO - 10.1038/s41588-021-00984-y

M3 - Article

SN - 1061-4036

VL - 54

SP - 84

EP - 93

JO - Nature Genetics

JF - Nature Genetics

IS - 1

ER -

A PARTHENOGENESIS allele from apomictic dandelion can induce egg cell division without fertilization in lettuce

Abstract

Keywords

Access to Document

Fingerprint

Datasets

Taraxacum officinale isolate A68: Raw sequence reads

Investigation of the PAR gene conservation in Taraxacum germplasms

Dandelion (Taraxacum officinale) female gametophyte cell transcriptomes

Press/Media

Gene found that produces unfertilized seeds

Onderzoekers vinden gen in paardenbloem dat tot eiceldeling aanzet: ‘Dit kan grote gevolgen hebben voor de landbouw’

Crucial gene discovered in dandelion

Cite this