A cis-acting bidirectional transcription switch controls sexual dimorphism in the liverwort

Tetsuya Hisanaga, Keitaro Okahashi, Shohei Yamaoka, Tomoaki Kajiwara, Ryuichi Nishihama, Masaki Shimamura, Katsuyuki T. Yamato, John L. Bowman, Takayuki Kohchi, Keiji Nakajima

Research output: Contribution to journalArticleResearchpeer-review

Abstract

Plant life cycles alternate between haploid gametophytes and diploid sporophytes. While regulatory factors determining male and female sexual morphologies have been identified for sporophytic reproductive organs, such as stamens and pistils of angiosperms, those regulating sex-specific traits in the haploid gametophytes that produce male and female gametes and hence are central to plant sexual reproduction are poorly understood. Here, we identified a MYB-type transcription factor, MpFGMYB, as a key regulator of female sexual differentiation in the haploid-dominant dioicous liverwort, Marchantia polymorpha. MpFGMYB is specifically expressed in females and its loss resulted in female-to-male sex conversion. Strikingly, MpFGMYB expression is suppressed in males by a cis-acting antisense gene SUF at the same locus, and loss-of-function suf mutations resulted in male-to-female sex conversion. Thus, the bidirectional transcription module at the MpFGMYB/SUF locus acts as a toggle between female and male sexual differentiation in M. polymorpha gametophytes. Arabidopsis thaliana MpFGMYB orthologs are known to be expressed in embryo sacs and promote their development. Thus, phylogenetically related MYB transcription factors regulate female gametophyte development across land plants.

Original languageEnglish
Article numbere100240
Number of pages12
JournalEMBO Journal
Volume38
Issue number6
DOIs
Publication statusPublished - 15 Mar 2019

Keywords

  • antisense transcription
  • lncRNA
  • Marchantia polymorpha
  • R2R3 MYB-type transcription factor
  • sexual differentiation

Cite this

Hisanaga, T., Okahashi, K., Yamaoka, S., Kajiwara, T., Nishihama, R., Shimamura, M., ... Nakajima, K. (2019). A cis-acting bidirectional transcription switch controls sexual dimorphism in the liverwort. EMBO Journal, 38(6), [e100240]. https://doi.org/10.15252/embj.2018100240
Hisanaga, Tetsuya ; Okahashi, Keitaro ; Yamaoka, Shohei ; Kajiwara, Tomoaki ; Nishihama, Ryuichi ; Shimamura, Masaki ; Yamato, Katsuyuki T. ; Bowman, John L. ; Kohchi, Takayuki ; Nakajima, Keiji. / A cis-acting bidirectional transcription switch controls sexual dimorphism in the liverwort. In: EMBO Journal. 2019 ; Vol. 38, No. 6.
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abstract = "Plant life cycles alternate between haploid gametophytes and diploid sporophytes. While regulatory factors determining male and female sexual morphologies have been identified for sporophytic reproductive organs, such as stamens and pistils of angiosperms, those regulating sex-specific traits in the haploid gametophytes that produce male and female gametes and hence are central to plant sexual reproduction are poorly understood. Here, we identified a MYB-type transcription factor, MpFGMYB, as a key regulator of female sexual differentiation in the haploid-dominant dioicous liverwort, Marchantia polymorpha. MpFGMYB is specifically expressed in females and its loss resulted in female-to-male sex conversion. Strikingly, MpFGMYB expression is suppressed in males by a cis-acting antisense gene SUF at the same locus, and loss-of-function suf mutations resulted in male-to-female sex conversion. Thus, the bidirectional transcription module at the MpFGMYB/SUF locus acts as a toggle between female and male sexual differentiation in M. polymorpha gametophytes. Arabidopsis thaliana MpFGMYB orthologs are known to be expressed in embryo sacs and promote their development. Thus, phylogenetically related MYB transcription factors regulate female gametophyte development across land plants.",
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Hisanaga, T, Okahashi, K, Yamaoka, S, Kajiwara, T, Nishihama, R, Shimamura, M, Yamato, KT, Bowman, JL, Kohchi, T & Nakajima, K 2019, 'A cis-acting bidirectional transcription switch controls sexual dimorphism in the liverwort' EMBO Journal, vol. 38, no. 6, e100240. https://doi.org/10.15252/embj.2018100240

A cis-acting bidirectional transcription switch controls sexual dimorphism in the liverwort. / Hisanaga, Tetsuya; Okahashi, Keitaro; Yamaoka, Shohei; Kajiwara, Tomoaki; Nishihama, Ryuichi; Shimamura, Masaki; Yamato, Katsuyuki T.; Bowman, John L.; Kohchi, Takayuki; Nakajima, Keiji.

In: EMBO Journal, Vol. 38, No. 6, e100240, 15.03.2019.

Research output: Contribution to journalArticleResearchpeer-review

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AU - Hisanaga, Tetsuya

AU - Okahashi, Keitaro

AU - Yamaoka, Shohei

AU - Kajiwara, Tomoaki

AU - Nishihama, Ryuichi

AU - Shimamura, Masaki

AU - Yamato, Katsuyuki T.

AU - Bowman, John L.

AU - Kohchi, Takayuki

AU - Nakajima, Keiji

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N2 - Plant life cycles alternate between haploid gametophytes and diploid sporophytes. While regulatory factors determining male and female sexual morphologies have been identified for sporophytic reproductive organs, such as stamens and pistils of angiosperms, those regulating sex-specific traits in the haploid gametophytes that produce male and female gametes and hence are central to plant sexual reproduction are poorly understood. Here, we identified a MYB-type transcription factor, MpFGMYB, as a key regulator of female sexual differentiation in the haploid-dominant dioicous liverwort, Marchantia polymorpha. MpFGMYB is specifically expressed in females and its loss resulted in female-to-male sex conversion. Strikingly, MpFGMYB expression is suppressed in males by a cis-acting antisense gene SUF at the same locus, and loss-of-function suf mutations resulted in male-to-female sex conversion. Thus, the bidirectional transcription module at the MpFGMYB/SUF locus acts as a toggle between female and male sexual differentiation in M. polymorpha gametophytes. Arabidopsis thaliana MpFGMYB orthologs are known to be expressed in embryo sacs and promote their development. Thus, phylogenetically related MYB transcription factors regulate female gametophyte development across land plants.

AB - Plant life cycles alternate between haploid gametophytes and diploid sporophytes. While regulatory factors determining male and female sexual morphologies have been identified for sporophytic reproductive organs, such as stamens and pistils of angiosperms, those regulating sex-specific traits in the haploid gametophytes that produce male and female gametes and hence are central to plant sexual reproduction are poorly understood. Here, we identified a MYB-type transcription factor, MpFGMYB, as a key regulator of female sexual differentiation in the haploid-dominant dioicous liverwort, Marchantia polymorpha. MpFGMYB is specifically expressed in females and its loss resulted in female-to-male sex conversion. Strikingly, MpFGMYB expression is suppressed in males by a cis-acting antisense gene SUF at the same locus, and loss-of-function suf mutations resulted in male-to-female sex conversion. Thus, the bidirectional transcription module at the MpFGMYB/SUF locus acts as a toggle between female and male sexual differentiation in M. polymorpha gametophytes. Arabidopsis thaliana MpFGMYB orthologs are known to be expressed in embryo sacs and promote their development. Thus, phylogenetically related MYB transcription factors regulate female gametophyte development across land plants.

KW - antisense transcription

KW - lncRNA

KW - Marchantia polymorpha

KW - R2R3 MYB-type transcription factor

KW - sexual differentiation

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SN - 0261-4189

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Hisanaga T, Okahashi K, Yamaoka S, Kajiwara T, Nishihama R, Shimamura M et al. A cis-acting bidirectional transcription switch controls sexual dimorphism in the liverwort. EMBO Journal. 2019 Mar 15;38(6). e100240. https://doi.org/10.15252/embj.2018100240