The TOPLESS corepressor regulates developmental switches in the bryophyte Physcomitrium patens that were critical for plant terrestrialisation

Abstract

SUMMARYThe plant‐specific TOPLESS (TPL) family of transcriptional corepressors is integral to multiple angiosperm developmental processes. Despite this, we know little about TPL function in other plants. To address this gap, we investigated the roles TPL plays in the bryophyte Physcomitrium patens, which diverged from angiosperms approximately 0.5 billion years ago. Although complete loss of PpTPL function is lethal, transgenic lines with reduced PpTPL activity revealed that PpTPLs are essential for two fundamental developmental switches in this plant: the transitions from basal photosynthetic filaments (chloronemata) to specialised foraging filaments (caulonemata) and from two‐dimensional (2D) to three‐dimensional (3D) growth. Using a transcriptomics approach, we integrated PpTPL into the regulatory network governing 3D growth and we propose that PpTPLs represent another important class of regulators that are essential for the 2D‐to‐3D developmental switch. Transcriptomics also revealed a previously unknown role for PpTPL in the regulation of flavonoids. Intriguingly, 3D growth and the formation of caulonemata were crucial innovations that facilitated the colonisation of land by plants, a major transformative event in the history of life on Earth. We conclude that TPL, which existed before the land plants, was co‐opted into new developmental pathways, enabling phytoterrestrialisation and the evolution of land plants.

Multilevel analysis between Physcomitrium patens and Mortierellaceae endophytes explores potential long‐standing interaction among land plants and fungi

“…Comparisons based on common P. patens media sampled 41 libraries from gametophore tissues grown on BCD Agar (five), BCDAT (six), Hoagland (six), Knop agar (eight), Knop liquid (eight), PpNH4 protoplast solution (five), and soil (three). This was taken from five different projects (PRJNA751102, PRJNA880579, PRJNA723997, PRJNA259147, and PRJNA807682) (Data S7) (Causier et al, 2023;Garcias-Morales et al, 2023;Otero-Blanca et al, 2021;Perroud et al, 2018). Select SRA 'control' reads from each project were downloaded using SRA-toolkit (v3.0.3), trimmed with Fastp (v0.21.0), the P. patens transcriptome was again indexed and used for mapping reads with Salmon (v1.8.0), and finally quantified read files were merged using the salmon merge function (Supplementary Code S5).…”