Graduate School of Science and Technology, Nara Institute of Science and Technology, Nara, Japan; Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna Biocenter, Vienna, Austria
Shota Fujimoto
Graduate School of Science and Technology, Nara Institute of Science and Technology, Nara, Japan
Yihui Cui
Graduate School of Science and Technology, Nara Institute of Science and Technology, Nara, Japan
Katsutoshi Sato
Graduate School of Science and Technology, Nara Institute of Science and Technology, Nara, Japan
Ryosuke Sano
Graduate School of Science and Technology, Nara Institute of Science and Technology, Nara, Japan
KNOX and BELL transcription factors regulate distinct steps of diploid development in plants. In the green alga Chlamydomonas reinhardtii, KNOX and BELL proteins are inherited by gametes of the opposite mating types and heterodimerize in zygotes to activate diploid development. By contrast, in land plants such as Physcomitrium patens and Arabidopsis thaliana, KNOX and BELL proteins function in sporophyte and spore formation, meristem maintenance and organogenesis during the later stages of diploid development. However, whether the contrasting functions of KNOX and BELL were acquired independently in algae and land plants is currently unknown. Here, we show that in the basal land plant species Marchantia polymorpha, gamete-expressed KNOX and BELL are required to initiate zygotic development by promoting nuclear fusion in a manner strikingly similar to that in C. reinhardtii. Our results indicate that zygote activation is the ancestral role of KNOX/BELL transcription factors, which shifted toward meristem maintenance as land plants evolved.