Neofunctionalisation of basic helix−loop−helix proteins occurred when embryophytes colonised the land

Abstract

ROOT HAIR DEFECTIVE SIX‐LIKE (RSL) genes control the development of structures from single cells at the surface of embryophytes (land plants) such as rhizoids and root hairs. RSL proteins constitute a subclass (VIIIc) of the basic helix–loop–helix (bHLH) class VIII transcription factor family. The Charophyceae form the only class of streptophyte algae with tissue‐like structures and rhizoids. To determine if the function of RSL genes in the control of cell differentiation in embryophytes was inherited from a streptophyte algal ancestor, we identified the single class VIII bHLH gene from the charophyceaen alga Chara braunii (CbbHLHVIII). CbbHLHVIII is sister to the RSL proteins; they constitute a monophyletic group. Expression of CbbHLHVIII does not compensate for loss of RSL functions in Marchantia polymorpha or Arabidopsis thaliana. In C. braunii CbbHLHVIII is expressed at sites of morphogenesis but not in rhizoids. This finding indicates that C. braunii class VIII protein is functionally different from land plant RSL proteins. This result suggests that the function of RSL proteins in cell differentiation at the plant surface evolved by neofunctionalisation in the land plants lineage after its divergence from its last common ancestor with C. braunii, at or before the colonisation of the land by embryophytes.

The evolutionary emergence of land plants

“…The mechanisms promoting rhizoid development are conserved between bryophyte groups, and also conserved with mechanisms regulating root hair development in flowering plant sporophytes [116][117][118] . The bHLH transcription factors involved predate the origin of land plants 119 , but a Chara braunii bHLHVIII sister gene to the land plant RSL gene clade functions non-equivalently to land plant genes, suggesting that neofunctionalisation was involved in the emergence of rhizoid-based rooting systems 120 .…”

A fundamental developmental transition in Physcomitrium patens is regulated by evolutionarily conserved mechanisms

“…RSL genes are found extensively in all land plant genomes and also within the charophyte algae (N. D. Pires et al, 2013). Phylogenetic studies have revealed that two classes of RSL genes (Classes I and II) exist in land plants, and that these likely arose in the charophyte lineage, or in the earliest colonizers of land (Bonnot et al, 2019; N. D. Pires et al, 2013). RSL genes regulate the development of epidermal structures, most notably root hairs and rhizoids, but also asexual propagules or secretory hairs in extant land plants (Jang & Dolan, 2011; Jang et al, 2011; Kim & Dolan, 2016; Masucci & Schiefelbein, 1994; B. Menand, Yi, et al, 2007; Proust et al, 2016; K. Yi et al, 2010).…”

“…RSL genes are found extensively in all land plant genomes and also within the charophyte algae (N. D. Pires et al, 2013). Phylogenetic studies have revealed that two classes of RSL genes (Classes I and II) exist in land plants, and that these likely arose in the charophyte lineage, or in the earliest colonizers of land (Bonnot et al, 2019;N. D. Pires et al, 2013).…”

Sunscreen mucilage: a photoprotective adaptation found in terrestrial green algae (Zygnematophyceae)

“…S1), exemplifying once more that the structurally simple, yet diverse 'saccoderm desmids' (traditionally Mesotaeniaceae) are still heavily understudied (Gontcharov et al, 2004;Gontcharov & Melkonian, 2010). However, these phylogenetically diverse life forms show clear cell morphological differences (Gontcharov, 2008) and, recently, gained importance for evolutionary inferences (Bonnot et al, 2019;Cheng et al, 2019;Liang et al, 2019;Xu et al, 2019;Philippe et al, 2020), so that a taxonomic revision of these algae is desirable.…”