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Building new insights in plant gametogenesis from an evolutionary perspective

Nature Plants volume 5, pages 663–669 (2019)Cite this article

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Abstract

Extant bryophytes are thought to preserve characteristics of ancestral land plants, with a life cycle dominated by the haploid gametophyte. The gametophyte produces gametes in specialized organs that differentiate after an extensive phase of vegetative development. During land plant evolution, these organs became extremely reduced. As a result, in flowers of angiosperms the haploid phase of the life cycle is reduced to few-celled gametophytes, namely the embryo sac (female) and pollen (male). Although many factors contributing to gametogenesis have been identified in flowering plants, the extreme reduction of the gametophytes has prevented a clear molecular dissection of key processes of gametogenesis. Recent studies in the model bryophyte Marchantia polymorpha have identified conserved transcription factors regulating the equivalent steps in the sexual reproduction of land plants. These include FEMALE GAMETOPHYTE MYB for female gametophyte development, BONOBO for gamete progenitor cell specification, DUO POLLEN1 for sperm differentiation and members of the RWP-RK domain family for female gamete formation. These studies demonstrate that M. polymorpha is a powerful model to untangle the core processes of gametogenesis in land plants. We anticipate that a deeper understanding of gametogenesis in bryophytes will circumscribe the origin of plant germ cells and define the differentiation programmes of sperm and eggs.

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Fig. 1: Sex determination of the gametophyte in M. polymorpha.
Fig. 2: Comparison between the controls of gametogenesis in A. thaliana and M. polymorpha.

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Acknowledgements

We thank Sean A. Montgomery and M. Watson for the critical reading of the manuscript. F.B. and T. Kawashima were supported by GMI and FWF (grant no. I2163-B16) linked to the ERA-CAPS consortium, EvoRepro. T. Kawashima was supported by the National Institute of Food and Agriculture, US Department of Agriculture, Hatch Program (grant no. 1014280). MEXT/JSPS KAKENHI grants were provided to T.H. (grant no. 17J08430), S.Y. (grant nos. 17H05841, 18K06285 and 19H04860), A.H. (grant no. 17J01153), K.N. (grant no. 25113007), T.A. (grant nos. 25113005, 23370022, 24657031 and 19H03244) and T. Kohchi (grant nos. 25113001, 25113009, 15K21758 and 17H07424).

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Author notes

  1. These authors contributed equally: T. Hisanaga, S. Yamaoka, T. Kawashima.

Authors and Affiliations

  1. Gregor Mendel Institute, Austrian Academy of Sciences, Vienna BioCenter, Vienna, Austria

    Tetsuya Hisanaga & Frédéric Berger

  2. Graduate School of Science and Technology, Nara Institute of Science and Technology, Ikoma, Japan

    Tetsuya Hisanaga & Keiji Nakajima

  3. Graduate School of Biostudies, Kyoto University, Kyoto, Japan

    Shohei Yamaoka, Asuka Higo, Takashi Araki & Takayuki Kohchi

  4. Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY, USA

    Tomokazu Kawashima

  5. Kihara Institute for Biological Research, Yokohama City University, Yokohama, Japan

    Asuka Higo

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Contributions

T.H., S.Y., T. Kawashima and F. B. led the writing of the manuscript. T.A., K.N. and A.H. contributed to the critical reading of the manuscript, provided suggestions and contributed to the writing of specific sections. T. Kohchi contributed to the critical reading of the manuscript and provided suggestions. S.Y. and T.A. composed the figures. F.B. initiated and coordinated the project.

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Correspondence to Frédéric Berger.

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Peer review information: Nature Plants thanks F. W. Li and other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Hisanaga, T., Yamaoka, S., Kawashima, T. et al. Building new insights in plant gametogenesis from an evolutionary perspective. Nat. Plants 5, 663–669 (2019). https://doi.org/10.1038/s41477-019-0466-0

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