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

Asuka Higo, Tomokazu Kawashima, Michael Borg, Mingmin Zhao, Irene López-Vidriero, Hidetoshi Sakayama, Sean A. Montgomery, Hiroyuki Sekimoto, Dieter Hackenberg, Masaki Shimamura, Tomoaki Nishiyama, Keiko Sakakibara, Yuki Tomita, Taisuke Togawa, Kan Kunimoto, Akihisa Osakabe, Yutaka Suzuki, Katsuyuki T. Yamato, Kimitsune Ishizaki, Ryuichi Nishihama, Takayuki Kohchi, José M. Franco-Zorrilla, David Twell, Frédéric Berger () and Takashi Araki ()
Additional contact information
Asuka Higo: Kyoto University
Tomokazu Kawashima: Vienna Biocenter (VBC)
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

Nature Communications, 2018, vol. 9, issue 1, 1-13

Abstract: 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.

Date: 2018
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DOI: 10.1038/s41467-018-07728-3

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