HAG1 and SWI3A/B control of male germ line development in P. patens suggests conservation of epigenetic reproductive control across land plants

Abstract

Key message Bryophytes as models to study the male germ line: loss-of-function mutants of epigenetic regulators HAG1 and SWI3a/b demonstrate conserved function in sexual reproduction. Abstract With the water-to-land transition, land plants evolved a peculiar haplodiplontic life cycle in which both the haploid gametophyte and the diploid sporophyte are multicellular. The switch between these phases was coined alternation of generations. Several key regulators that control the bauplan of either generation are already known. Analyses of such regulators in flowering plants are difficult due to the highly reduced gametophytic generation, and the fact that loss of function of such genes often is embryo lethal in homozygous plants. Here we set out to determine gene function and conservation via studies in bryophytes. Bryophytes are sister to vascular plants and hence allow evolutionary inferences. Moreover, embryo lethal mutants can be grown and vegetatively propagated due to the dominance of the bryophyte gametophytic generation. We determined candidates by selecting single copy orthologs that are involved in transcriptional control, and of which flowering plant mutants show defects during sexual reproduction, with a focus on the under-studied male germ line. We selected two orthologs, SWI3a/b and HAG1, and analyzed loss-of-function mutants in the moss P. patens. In both mutants, due to lack of fertile spermatozoids, fertilization and hence the switch to the diploid generation do not occur. Pphag1 additionally shows arrested male and impaired female gametangia development. We analyzed HAG1 in the dioecious liverwort M. polymorpha and found that in Mphag1 the development of gametangiophores is impaired. Taken together, we find that involvement of both regulators in sexual reproduction is conserved since the earliest divergence of land plants.

A Physcomitrella PIN protein acts in spermatogenesis and sporophyte retention

“…In mammals, this ability is gained in the epididymis, and is controlled by different external and internal factors (Pereira et al ., 2017; Björkgren & Sipilä, 2019; O'Flaherty, 2019). Due to the complexity of the process and a large number of influences, sperm populations are not homogeneous, but vary regarding phenotype, motility or activity (Gómez Montoto et al ., 2011; Genau et al ., 2021; Martins‐Bessa et al ., 2021). A key role in metazoan and Physcomitrella spermatogenesis is played by the evolutionary conserved DNA Topoisomerase 1α, which facilitates chromatin condensation towards the compact sperm head (Gu et al ., 2022).…”

A Physcomitrella PIN protein acts in spermatogenesis and sporophyte retention

“…In mammals, this ability is gained in the epididymis, and is controlled by different external and internal factors (Pereira et al ., 2017; O’Flaherty, 2019; Björkgren & Sipilä, 2019). Due to the complexity of the process and a large number of influences, sperm populations are not homogenous, but vary regarding phenotype, motility or activity (Gómez Montoto et al ., 2011; Genau et al ., 2021; Martins-Bessa et al ., 2021). A key role in metazoan and Physcomitrella spermatogenesis is played by the evolutionary conserved DNA Topoisomerase 1α, which facilitates chromatin condensation towards the compact sperm head (Gu et al ., 2022).…”

The greening ashore

“…In the focus are streptophyte algae such as Chara, Klebsormidium, Penium, and Spirogloea, bryophytes such as the hornwort Anthoceros, the liverwort Marchantia, and the moss Physcomitrium, and among the vascular but non-seed land plants the lycophyte Selaginella and the ferns Azolla and Ceratopteris, to mention a few. The fast and constant increase in the number of sequenced genomes (including those of the species listed), and the progressive establishment of tools for non-seed plant model organisms which now need to be put to good use [76], has already installed a new field of evo-devo research over the past few years that has provided an impressive list of new insights [4,37,38,70,77].…”