Antagonism between blue- and red-light signaling controls thallus flatness in Marchantia polymorpha

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 orientation, with red-light signaling promoting epinasty and blue-light signaling promoting hyponasty. We found that loss-of-function mutations in the blue-light receptor MpPHOT led to epinasty, while loss-of-function mutations in the red-light receptor MpPHY resulted in hyponasty. We hypothesize that these antagonistic activities of blue- and red-light signaling 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 harboring loss-of-function mutations in two of the six MpBBX transcription factors developed defective thallus growth orientation. Mpbbx1 loss-of-function mutants formed hyponastic thalli, while Mpbbx5 loss-of-function mutants developed epinastic thalli. Double mutants Mpbbx1 and Mpbbx5 grew flat, supporting the hypothesis that they function antagonistically. Together, these data indicate that phototropin-mediated blue-light and phytochrome-mediated red-light signaling antagonistically modulate thallus growth orientation and that BBX transcription factors also act antagonistically to regulate thallus flatness.