Transcriptional Landscapes of Divergent Sporophyte Development in Two Mosses, Physcomitrium (Physcomitrella) patens and Funaria hygrometrica

Abstract

Understanding the molecular basis of morphological shifts is a fundamental question of evolutionary biology. New morphologies may arise through the birth/death of genes (gene gain/loss) or by reutilizing existing gene sets. Yet, the relative contribution of these two processes to radical morphological shifts is still poorly understood. Here, we use the model system of two mosses, Funaria hygrometrica and Physcomitrium (Physcomitrella) patens, to investigate the molecular mechanisms underlying contrasting sporophyte architectures. We used comparative analysis of time-series expression data for four stages of sporophyte development in both species to address this question in detail. We found that large-scale differences in sporophytic architecture are mainly governed by orthologous (i.e., shared) genes frequently experiencing temporal gene expression shifts between the two species. While the absolute number of species-specific genes expressed during sporophyte development is somewhat smaller, we observed a significant increase of their proportion in preferentially sporophyte expressed genes, suggesting a fundamental role in the sporophyte phase. However, further functional studies are necessary to determine their contribution to diverging sporophyte morphologies. Our results add to the growing set of studies suggesting that radical changes in morphology may rely on the heterochronic expression of conserved regulators.

Genome dynamics in mosses: Extensive synteny coexists with a highly dynamic gene space

“…Despite extensive collinearity of homologous gene copies, we confirmed previous hypotheses that both the F. hygrometrica and the P. patens genome contain a large proportion of species-specific (lineage-specific) genes (30, 81). Our analyses also show that these species-specific genes have no detectable homologs in the other species’ genome and therefore likely arose de novo or emerged as specific following the loss through deletion or excision of the homolog in the other species’ genome.…”

“…Our study provides a solid basis for a more extensive exploration of genome dynamics within the Funariaceae, to test for the generality of our observations. Moreover, availability of a high-quality genome sequence for two species representing end points of the morphological and ecological diversity within the Funariaceae will open the way for detailed investigations on the genetic basis of phenotypic diversity within the family (30,(33)(34)(35)41,81).…”

Mosses: Accessible Systems for Plant Development Studies

“…Beyond P. patens, mosses have garnered special interest for their physiology and development, involvement in carbon sequestration, abiotic stresses management and biotic interactions. Eight species have had their nuclear genome sequenced and drafted in the last few years, and at least thirteen others are currently being sequenced [120][121][122][123][124][125][126][127]. Furthermore, the mitochondrial and/or plastid genomes of more than forty other moss species (not cited) has been published in the last six years, which may precede their nuclear genome study as with P. patens.…”

A Physcomitrella PIN protein acts in spermatogenesis and sporophyte retention

“…The sporophyte foot is secured in a maternal cavity (vaginula) and covered at its base with haustorial cells, important for the uptake of nutrients provided by the gametophore (Regmi et al, 2017). Formation of sporophytes is a complex process and regulated by a number of genetic elements (Mosquna et al, 2009;Horst et al, 2016;Ortiz-Ramírez et al, 2016;Lopez-Obando et al, 2016;Hashida et al, 2020;Kirbis et al, 2020;Sakakibara et al, 2008;Takechi et al, 2021. However, auxin remains a crucial player in sporophyte growth (Fujita et al, 2008), with the two Physcomitrella PIN genes PpPINA and PpPINB showing functional activity in the development of sporophytes (Bennett et al, 2014b), whereas the role of the canonical PpPINC remains unclear.…”