An Early Arising Role of the MicroRNA156/529-SPL Module in Reproductive Development Revealed by the Liverwort Marchantia polymorpha

• Published in: Current biology 2019-10, Vol.29 (19), p.3307-3314.e5
• Main Authors: Tsuzuki, Masayuki, Futagami, Kazutaka, Shimamura, Masaki, Inoue, Chikako, Kunimoto, Kan, Oogami, Takashi, Tomita, Yuki, Inoue, Keisuke, Kohchi, Takayuki, Yamaoka, Shohei, Araki, Takashi, Hamada, Takahiro, Watanabe, Yuichiro
• Format: Article
• Language: English
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2019.07.084

In angiosperms, the phase transition from vegetative to reproductive growth involves the de-repression of the squamosa promoter-binding-protein-like (SPL) class of transcription factors, which is negatively regulated by the specific microRNAs (miRNAs/miRs) miR156/529 [1]. Non-vascular land plants also undergo growth-phase transition to the reproductive state, but knowledge regarding the controlling mechanisms is limited. Here, we investigate the reproductive transition in the liverwort Marchantia polymorpha, focusing on the roles of miR529c [2–4] and MpSPL2. First, we established mir529c-null mutants using CRISPR/Cas9. Even in the absence of far-red light-supplemented long-day condition, which is usually needed to induce reproductive development [5, 6], the mutant thalli developed sexual reproductive organs (gametangia) and produced gametes. Transgenic plants expressing a miR529-resistant MpSPL2 transgene also showed a similar phenotype of reproductive transition in the absence of inductive far-red light signals. In these mutants and transgenic plants, the MpSPL2 mRNA abundance was elevated. Mpspl2ko mutant plants showed successful gamete development and fertilization, which suggests that MpSPL2 is involved in, but not essential for, sexual reproduction in M. polymorpha. Furthermore, analysis of Mpspl2ko mutant and its complemented lines suggests that MpSPL2 may have a role in promotion of reproductive transition. These findings support the notion that the transition to reproductive development in liverworts is controlled by a system similar to that in angiosperms, and the miR156/529-SPL module has common significance in the control of the vegetative-to-reproductive transition during development in many land plants, including liverworts. [Display omitted] •Loss of miR529c causes gamete production in the absence of environmental signals•Repression of MpSPL2 expression by miR529c prevents the reproductive transition•MpSPL2 is involved in, but not essential for, reproductive development•The miR156/529-SPL module controls the reproductive transition in land plants Tsuzuki et al. report that the loss of miR529c in the liverwort Marchantia polymorpha causes gametangium formation and gamete production without the far-red light signaling needed for the reproductive transition, because of de-repressed expression of MpSPL2. The miR156/529-SPL module generally controls the reproductive transition in land plants.