Abstract
The 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 2-dimensional to 3-dimensional growth. Using a transcriptomics approach, we integrate PpTPL into the regulatory network governing 3D growth and 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 formation of caulonemata were crucial innovations that facilitated the colonization of land by plants; a major transformative event in the history of life on Earth. We conclude that PpTPL, which existed before the land plants, was co-opted into new developmental pathways facilitating phytoterrestrialisation and the evolution of land plants.
| Original language | English |
|---|---|
| Pages (from-to) | 1331-1344 |
| Number of pages | 14 |
| Journal | Plant Journal |
| Volume | 115 |
| Issue number | 5 |
| Early online date | 8 Jun 2023 |
| DOIs | |
| Publication status | Published - 27 Aug 2023 |
Bibliographical note
Funding Information:This work was funded by a Leverhulme Trust Research Project Grant (RPG-2016-412: A New Dimension for Plants) and a Biotechnology and Biological Sciences Research Council grant (BB/T001194/1: Finding the Balance: Repression of Plant Gene Expression) awarded to BD. Transgenic P. patens lines were generated and validated via the Leeds Moss Transformation Service, provided by Andrew Cuming and Yasuko Kamisugi. We are also grateful to N. Sugimoto, M. Hasebe and Y. Sato (NIBB, Japan) for advice on bud development assays. We thank Dr. Alastair Plant for images of tpl-1 seedlings in Figure S2 and are also grateful to James Roland and the Leeds Plant Growth Suite for assistance with experiments and growing plants. Finally, we thank Dr. Tom Bennett (University of Leeds) for critical feedback on the manuscript.
Funding Information:
This work was funded by a Leverhulme Trust Research Project Grant (RPG‐2016‐412: A New Dimension for Plants) and a Biotechnology and Biological Sciences Research Council grant (BB/T001194/1: Finding the Balance: Repression of Plant Gene Expression) awarded to BD. Transgenic lines were generated and validated via the Leeds Moss Transformation Service, provided by Andrew Cuming and Yasuko Kamisugi. We are also grateful to N. Sugimoto, M. Hasebe and Y. Sato (NIBB, Japan) for advice on bud development assays. We thank Dr. Alastair Plant for images of seedlings in Figure S2 and are also grateful to James Roland and the Leeds Plant Growth Suite for assistance with experiments and growing plants. Finally, we thank Dr. Tom Bennett (University of Leeds) for critical feedback on the manuscript. P. patens tpl‐1
Publisher Copyright:
© 2023 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.