Genetic Regulation of the 2D to 3D Growth Transition in the Moss Physcomitrella patens

Abstract

SummaryOne of the most important events in the history of life on earth was the colonization of land by plants; this transition coincided with and was most likely enabled by the evolution of 3-dimensional (3D) growth. Today, the diverse morphologies exhibited across the terrestrial biosphere arise from the differential regulation of 3D growth processes during development. In many plants, 3D growth is initiated during the first few divisions of the zygote, and therefore, the genetic basis cannot be dissected because mutants do not survive. However, in mosses, which are representatives of the earliest land plants, 3D shoot growth is preceded by a 2D filamentous phase that can be maintained indefinitely. Here, we used the moss Physcomitrella patens to identify genetic regulators of the 2D to 3D transition. Mutant screens yielded individuals that could only grow in 2D, and through an innovative strategy that combined somatic hybridization with bulk segregant analysis and genome sequencing, the causative mutation was identified in one of them. The NO GAMETOPHORES 1 (NOG1) gene, which encodes a ubiquitin-associated protein, is present only in land plant genomes. In mutants that lack PpNOG1 function, transcripts encoding 3D-promoting PpAPB transcription factors [1] are significantly reduced, and apical initial cells specified for 3D growth are not formed. PpNOG1 acts at the earliest identified stage of the 2D to 3D transition, possibly through degradation of proteins that suppress 3D growth. The acquisition of NOG1 function in land plants could thus have enabled the evolution and development of 3D morphology.

Physcomitrella patens Reute mCherry as a tool for efficient crossing within and between ecotypes

“…Most recently, the traceable Gd and Vx strains were used successfully to identify the causal sterile mutation in a novel somatic hybridisation coupled SNP approach (Moody et al . ,b).…”

Geometric cues forecast the switch from two‐ to three‐dimensional growth in Physcomitrella patens

“…Persistent APB activity marks the gametophore initial cell, whereas APB expression rapidly diminishes in branch protonemal cells. Additionally, mutations in the NO GAMETOPHORE 1-REFERENCE (Ppnog1-R) gene causes defects in early gametophore formation (Moody et al, 2018). Deletion of another gene, DEFECTIVE KERNEL 1 (DEK1), causes multiple early gametophore initiation events followed by aberrant gametophore development.…”

“…Geometric cues in gametophore initial cells are independent of exogenously supplied cytokinin and consistent in gametophore mutants Under standard growth conditions it is challenging to investigate fate transitions as only c. 5% of emerging branching cells ultimately commit to gametophore fate. Therefore, similar to other studies focused on gametophore development (Ashton et al, 1979;Aoyama et al, 2012;Moody et al, 2018), we supplemented the liquid medium with exogenous cytokinin, BAP, to induce gametophore initiation. To investigate whether the observed differences in cell width and division plane were influenced by exogenous cytokinin treatment, we compared the width and angle of the division plane in the absence and presence of the synthetic cytokinin BAP (Fig.…”

“…Next, we asked whether the geometric cues predicting cell fate persist in mutants that possess gametophore development phenotypes. In Δdek1 and Ppnog1-R mutants, gametophore initiation is induced and repressed, respectively (Perroud et al, 2014;Moody et al, 2018). To inhibit branching and therefore synchronize gametophore induction, plant tissues were cultured under unilateral red light for 2 wk, where the Δdek1 mutant showed a growth phenotype with bulbous filamentous cells (Fig.…”

Development of a method for protonema proliferation of peat moss (Sphagnum squarrosum) through regeneration analysis

“…Mosses are good materials for studying the progression from one-dimensional to three-dimensional structures. Recently, a gene involved in the transformation of the protonema into the gametophore in Physcomitrella was identified (Moody et al, 2018). In Sphagnum, a unique two-dimensional thallose protonema like the prothallus of ferns can develop from the filamentous protonema.…”