A Transcriptome Atlas of Physcomitrella patens Provides Insights into the Evolution and Development of Land Plants

Abstract

Identifying the genetic mechanisms that underpin the evolution of new organ and tissue systems is an aim of evolutionary developmental biology. Comparative functional genetic studies between angiosperms and bryophytes can define those genetic changes that were responsible for developmental innovations. Here, we report the generation of a transcriptome atlas covering most phases in the life cycle of the model bryophyte Physcomitrella patens, including detailed sporophyte developmental progression. We identified a comprehensive set of sporophyte-specific transcription factors, and found that many of these genes have homologs in angiosperms that function in developmental processes such as flowering and shoot branching. Deletion of the PpTCP5 transcription factor results in development of supernumerary sporangia attached to a single seta, suggesting that it negatively regulates branching in the moss sporophyte. Given that TCP genes repress branching in angiosperms, we suggest that this activity is ancient. Finally, comparison of P. patens and Arabidopsis thaliana transcriptomes led us to the identification of a conserved core of transcription factors expressed in tip-growing cells. We identified modifications in the expression patterns of these genes that could account for developmental differences between P. patens tip-growing cells and A. thaliana pollen tubes and root hairs.

Origin and function of stomata in the moss Physcomitrella patens

“…However, PpSMF2 expression is very low compared to PpSMF1 and it is therefore unsurprising there is no aberrant phenotype in ΔPpSMF2 mutants despite key regulatory motifs being present. Conservation of functional motifs of PpSMF1 and PpSCRM1, which are both strongly expressed in the sporophyte 21 , taken together with our experimental data (Figures 1–3), suggests that a heterodimeric bHLH partnership first existed in the ancestor of mosses and flowering plants which could both initiate and complete stomatal development.…”

“…Both analyses robustly reject a (co-)orthologous relationship of the SMF genes in Physcomitrella and Selaginella with the MUTE/SPCH clade, as suggested by our earlier phylogenetic analysis 6 . Reasoning that genes encoding stomatal regulators would be preferentially expressed in the stomatal-bearing sporophyte, we interrogated microarray datasets 20 and P. patens transcriptome atlas results 21 that identified PpSMF1, PpSMF2 and PpSCRM1 as strong candidates because of their up-regulation in the sporophyte relative to protonemal tissue, as supported by qRT-PCR (Figures 1 f–h; Supp. Info.…”

“…Figures 1–2). Additionally, PpSCRM1 is the most highly expressed of the four PpSCRM paralogues across P. patens tissues including developing sporophytes 21 (Supp. Info.…”

Sporophyte formation and life cycle completion in moss requires heterotrimeric G-proteins

“…While the morphological details of the moss sporophyte, its developmental time line, and the transcriptional profile are relatively well described (Cove et al, 2009;Vidali and Bezanilla, 2012;Hiss et al, 2014;Scanlon, 2015a, 2015b;Ortiz-Ramirez et al, 2016), the mechanistic details and signal transduction pathways involved during sporophyte formation are largely unknown. Our results provide a clue to the types of proteins that might be involved in the signaling event that takes place during sporophyte formation.…”

Functional Characterization of UDP-apiose Synthases from Bryophytes and Green Algae Provides Insight into the Appearance of Apiose-containing Glycans during Plant Evolution

“…No PpUAS transcript was detected on a 1% (w/v) agarose gel even after a second round of PCR amplification using a 0.2 M concentration of each forward and reverse primer (supplemental Table S2) and an annealing temperature of 56°C. The recently released P. patens Electronic Fluorescent Pictograph browser (54,55) indicates that PpUAS (gene ID Pp1s379_19V6.1) is only expressed at substantial levels in stage S3 sporophyte and archegonia. Thus, a synthetic ORF gene corresponding to PpUAS was obtained (GenScript, Piscataway, NJ).…”