Beate Asper

Multicellular organisms produced by sexual reproduction develop from single cells, and the asymmetry of these cells can define the orientation of the earliest developmental axes. The haploid multicellular stage of the plant, Marchantia polymorpha, develops from a single cell—the spore—that divides asymmetrically, producing an apical germ cell that generates the plant body and a smaller basal cell that differentiates as an anchoring germ rhizoid cell. We show that the orientation of this asymmetric cell division is controlled by an external environmental cue—blue light—that is perceived by the photoreceptor phototropin. This process requires the NCH1 (NRL PROTEIN FOR CHLOROPLAST MOVEMENT 1) protein for downstream signaling. Together, these findings define core elements of the mechanism by which a directional environmental signal orients cell division, which, in turn, orients the first axis of symmetry.

Multicellular organisms produced by sexual reproduction develop from single cells and the asymmetry of these cells can define the orientation of the earliest developmental axes. The haploid multicellular stage of the plant, Marchantia polymorpha, develops from a single cell – the spore – that divides asymmetrically, producing an apical germ cell that generates the plant body and a smaller basal cell that differentiates as an anchoring germ rhizoid cell. We show that the orientation of this asymmetric cell division is controlled by an external, environmental cue – blue light – that is perceived by the photoreceptor PHOTOTROPIN and signals in an NCH1-dependent manner. This defines core elements of the mechanism by which a directional environmental signal orients cell division, which in turn orients the first axis of symmetry.

The growth orientation of the Marchantia polymorpha thallus – a system of dorsiventralized, indeterminate axes – is modulated by light. We show that red and blue light act antagonistically to control thallus growth tropisms, with red light signalling promoting epinasty and blue light signalling promoting hyponasty. We found that loss-of-function mutations in the blue light receptor Mp PHOT led to epinasty, while loss-of-function mutations in the red light receptor Mp PHY resulted in hyponasty. We hypothesize that these antagonistic activities of blue and red light signalling are balanced in white light, resulting in the development of flat thalli. Using time-resolved transcriptomics, we identified genes that were rapidly induced upon light exposure. Among these genes were all six members of the M. polymorpha BBX gene family. Mutants harbouring loss-of-function mutations in two of the six MpBBX transcription factors developed defective thallus tropisms. Mp bbx1 loss-of-function mutants formed hyponastic thalli, while Mp bbx5 loss-of-function mutants developed epinastic thalli. Double mutants Mpbbx1 Mp bbx5 grew flat, supporting the hypothesis that they function antagonistically. Together, these data indicate that phototropin-mediated blue light and phytochrome-mediated red light signalling antagonistically modulate thallus tropism, and that BBX transcription factors also act antagonistically to regulate thallus flatness.