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.
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This work was supported by FWF (I2163-B16 to F.B. and W1238-B20 to S.A.M.) and the Biotechnology and Biological Research Council (BB/N005090 to D.T.); ERA-CAPS EVOREPRO project to DT and FB; Spanish MINECO grant BIO2017-86651-P (AEI/FEDER) to J.F.-Z.; JSPS KAKENHI grant 15K07185 to H. Sa, MEXT grants (25113005, 23370022, and 24657031 to T.A.; 25113001 and 15K21758 to T.Ko. and T.A.; and 221S0002 to H. Sa., H. Se., and T.N.; and 26291081 to T.N., KS, and M.S.); a Grant-in-Aid for the Japan Society for the Promotion of Science Fellows (to A.H. and A.O.); the Kyoto University BRIDGE program (to A.H.); Lise-Meitner fellowship (M1818-B21 to M.B.); and GMI (T.Ka., M.B., O.A., and F.B.).
Novel data generated in this study have been deposited at GenBank under the accessions: MpDUO1 (LC172177), MpR2R3-MYB07 (KX683859), MpR2R3-MYB21 (KX683860) MpACT1 (LC172182) MpCEN1 (LC379265) MpTUA5 (LC172181) MpDAZ1 (LC172178) MpGCS1 (LC172179) MpGEX2 (LC172180) HmnDUO1 (LC379264) HmnACT1 (LC379378) CbrDUO1 (LC199499), CauDUO1 (LC221833), CleDUO1 (LC221832), CbrRSP11 (LC382020) CbrPACRG (LC382019) CbrRPL6 (LC382018) CauRPL6 (LC382017) CpeDUO1 (LC176570). Previously reported sequences used in this study are available at GenBank under the accession: MpPACRG (LC102460), MpPRM (LC102462) MpTUB4 (KM096548) MpLC7 (LC102461), MpMID/RWP2 (KU987912) CleRPL6 (AB035569), CpeRLK1 (AB920609) CpePI (AB012698). All other data are available from the authors on reasonable request.
Supplementary Information accompanies this paper at https://doi.org/10.1038/s41467-018-07728-3.
Higo, Asuka; Kawashima, Tomokazu; Borg, Michael; Zhao, Mingmin; López-Vidriero, Irene; Sakayama, Hidetoshi; Montgomery, Sean A.; Sekimoto, Hiroyuki; Hackenberg, Dieter; Shimamura, Masaki; Nishiyama, Tomoaki; Sakakibara, Keiko; Tomita, Yuki; Togawa, Taisuke; Kunimoto, Kan; Osakabe, Akihisa; Suzuki, Yutaka; Yamato, Katsuyuki T.; Ishizaki, Kimitsune; Nishihama, Ryuichi; Kohchi, Takayuki; Franco-Zorrilla, José M.; Twell, David; Berger, Frédéric; and Araki, Takashi, "Transcription Factor DUO1 Generated by Neo-Functionalization is Associated with Evolution of Sperm Differentiation in Plants" (2018). Plant and Soil Sciences Faculty Publications. 117.
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