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Transcription factor DUO1 generated by neo-functionalization is associated with evolution of sperm differentiation in plants

Author

Listed:
  • Asuka Higo

    (Kyoto University)

  • Tomokazu Kawashima

    (Vienna Biocenter (VBC)
    University of Kentucky)

  • Michael Borg

    (Vienna Biocenter (VBC))

  • Mingmin Zhao

    (University of Leicester)

  • Irene López-Vidriero

    (CNB-CSIC)

  • Hidetoshi Sakayama

    (Kobe University)

  • Sean A. Montgomery

    (Vienna Biocenter (VBC))

  • Hiroyuki Sekimoto

    (Japan Women’s University)

  • Dieter Hackenberg

    (University of Leicester)

  • Masaki Shimamura

    (Hiroshima University)

  • Tomoaki Nishiyama

    (Kanazawa University)

  • Keiko Sakakibara

    (Rikkyo University)

  • Yuki Tomita

    (Kyoto University)

  • Taisuke Togawa

    (Kindai University)

  • Kan Kunimoto

    (Kyoto University)

  • Akihisa Osakabe

    (Vienna Biocenter (VBC))

  • Yutaka Suzuki

    (The University of Tokyo)

  • Katsuyuki T. Yamato

    (Kindai University)

  • Kimitsune Ishizaki

    (Kobe University)

  • Ryuichi Nishihama

    (Kyoto University)

  • Takayuki Kohchi

    (Kyoto University)

  • José M. Franco-Zorrilla

    (CNB-CSIC)

  • David Twell

    (University of Leicester)

  • Frédéric Berger

    (Vienna Biocenter (VBC))

  • Takashi Araki

    (Kyoto University)

Abstract

Evolutionary mechanisms underlying innovation of cell types have remained largely unclear. In multicellular eukaryotes, the evolutionary molecular origin of sperm differentiation is unknown in most lineages. Here, we report that in algal ancestors of land plants, changes in the DNA-binding domain of the ancestor of the MYB transcription factor DUO1 enabled the recognition of a new cis-regulatory element. This event led to the differentiation of motile sperm. After neo-functionalization, DUO1 acquired sperm lineage-specific expression in the common ancestor of land plants. Subsequently the downstream network of DUO1 was rewired leading to sperm with distinct morphologies. Conjugating green algae, a sister group of land plants, accumulated mutations in the DNA-binding domain of DUO1 and lost sperm differentiation. Our findings suggest that the emergence of DUO1 was the defining event in the evolution of sperm differentiation and the varied modes of sexual reproduction in the land plant lineage.

Suggested Citation

  • Asuka Higo & Tomokazu Kawashima & Michael Borg & Mingmin Zhao & Irene López-Vidriero & Hidetoshi Sakayama & Sean A. Montgomery & Hiroyuki Sekimoto & Dieter Hackenberg & Masaki Shimamura & Tomoaki Nish, 2018. "Transcription factor DUO1 generated by neo-functionalization is associated with evolution of sperm differentiation in plants," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:9:y:2018:i:1:d:10.1038_s41467-018-07728-3
    DOI: 10.1038/s41467-018-07728-3
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    Cited by:

    1. Lei Li & Huaihao Yang & Yi Zhao & Qianqian Hu & Xiaotuo Zhang & Ting Jiang & Hua Jiang & Binglian Zheng, 2024. "ARID1 is required to regulate and reinforce H3K9me2 in sperm cells in Arabidopsis," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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