The RopGEF KARAPPO Is Essential for the Initiation of Vegetative Reproduction in Marchantia polymorpha

• Published in: Current biology 2019-10, Vol.29 (20), p.3525-3531.e7
• Main Authors: Hiwatashi, Takuma, Goh, Honzhen, Yasui, Yukiko, Koh, Li Quan, Takami, Hideyuki, Kajikawa, Masataka, Kirita, Hiroyuki, Kanazawa, Takehiko, Minamino, Naoki, Togawa, Taisuke, Sato, Mayuko, Wakazaki, Mayumi, Yamaguchi, Katsushi, Shigenobu, Shuji, Fukaki, Hidehiro, Mimura, Tetsuro, Toyooka, Kiminori, Sawa, Shinichiro, Yamato, Katsuyuki T., Ueda, Takashi, Urano, Daisuke, Kohchi, Takayuki, Ishizaki, Kimitsune
• Format: Article
• Language: English
• Subjects: asexual reproduction; bryophytes; cell polarity; evolution; small GTPase
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2019.08.071

Many plants can reproduce vegetatively, producing clonal progeny from vegetative cells; however, little is known about the molecular mechanisms underlying this process. Liverwort (Marchantia polymorpha), a basal land plant, propagates asexually via gemmae, which are clonal plantlets formed in gemma cups on the dorsal side of the vegetative thallus [1]. The initial stage of gemma development involves elongation and asymmetric divisions of a specific type of epidermal cell, called a gemma initial, which forms on the floor of the gemma cup [2, 3]. To investigate the regulatory mechanism underlying gemma development, we focused on two allelic mutants in which no gemma initial formed; these mutants were named karappo, meaning “empty.” We used whole-genome sequencing of both mutants and molecular genetic analysis to identify the causal gene, KARAPPO (KAR), which encodes a ROP guanine nucleotide exchange factor (RopGEF) carrying a plant-specific ROP nucleotide exchanger (PRONE) catalytic domain. In vitro GEF assays showed that the full-length KAR protein and the PRONE domain have significant GEF activity toward MpROP, the only ROP GTPase in M. polymorpha. Moreover, genetic complementation experiments showed a significant role for the N- and C-terminal variable regions in gemma development. Our investigation demonstrates an essential role for KAR/RopGEF in the initiation of plantlet development from a differentiated cell, which may involve cell-polarity formation and subsequent asymmetric cell division via activation of ROP signaling, implying a similar developmental mechanism in vegetative reproduction of various land plants. [Display omitted] •Marchantia polymorpha propagates asexually by forming clonal plantlets, gemmae•karappo mutants are impaired in gemma initial formation•KARAPPO encodes a PRONE-type guanine nucleotide exchange factor for ROP GTPase•KARAPPO may play a critical role for asymmetrical cell division in gemma formation Many plants have the ability to reproduce asexually by producing clonal plantlets directly from vegetative organs. Hiwatashi et al. identify a PRONE-type activator of ROP GTPase as an essential regulator for initiation of plantlet development in the basal land plant Marchantia polymorpha.