Transcriptional Framework of Male Gametogenesis in the LiverwortMarchantia polymorphaL.

Abstract

In land plants, there are two types of male gametes: one is a non-motile sperm cell which is delivered to the egg cell by a pollen tube, and the other is a motile sperm cell with flagella. The molecular mechanism underlying the sexual reproduction with the egg and pollen-delivered sperm cell is well understood from studies using model plants such as Arabidopsis and rice. On the other hand, the sexual reproduction with motile sperm has remained poorly characterized, due to the lack of suitable models. Marchantia polymorpha L. is a model basal land plant with sexual reproduction involving an egg cell and bi-flagellated motile sperm. To understand the differentiation process of plant motile sperm, we analyzed the gene expression profile of developing antheridia of M. polymorpha. We performed RNA-sequencing experiments and compared transcript profiles of the male sexual organ (antheridiophore and antheridium contained therein), female sexual organ (archegoniophore) and a vegetative organ (thallus). Transcriptome analysis showed that the antheridium expresses nearly half of the protein-coding genes predicted in the genome, but it also has unique features. The antheridium transcriptome shares some common features with male gamete transcriptomes of angiosperms and animals, and homologs of genes involved in male gamete formation and function in angiosperms and animals were identified. In addition, we showed that some of them had distinct expression patterns in the spermatogenous tissue of developing antheridia. This study provides a transcriptional framework on which to study the molecular mechanism of plant motile sperm development in M. polymorpha as a model.

An adenylyl cyclase with a phosphodiesterase domain in basal plants with a motile sperm system

“…When entering the sexual reproductive phase, the male and female gametophytes develop individual sexual organs, the antheridium and archegonium, on special gametophores called the antheridiophore and archegoniophore, respectively45. It has been shown that a number of specific genes are expressed in the antheridium of M. polymorpha 41. In our Mp CAPE promoter- GUS experiment, the promoter activity was specifically detected in the antheridium (Fig.…”

“…The fact that AC has a dominant function in sperm physiology and has been genetically inherited during the evolution of mammals may suggest a possible role for cAMP in the reproductive organ development of M. polymorpha . A recent paper has shown the expression of a cAMP-dependent protein kinase and cyclic nucleotide-gated ion channel in the antheridium of M. polymorpha 41. It is likely that these proteins function as signalling factors downstream of MpCAPE.…”

An Evolutionarily Conserved Plant RKD Factor Controls Germ Cell Differentiation

“…SCs divide both transversely and vertically, eventually giving rise to numerous sperm mother cells (SMCs). An SMC divides diagonally to form two triangular spermatids, which then differentiate into flagellated sperm cells (Figure 2A) [21,22]. By contrast, multiple archegonia are formed below the lobes of each archegoniophore via tightly regulated cell-division sequences ( Figure 2B).…”

Microscopy of Physcomitrella patens sperm cells

“…Due to their small size, P. patens antheridia can be easily fixed and observed as whole-mount samples without the requirement for microscopic sections e.g. performed of M. polymorpha antheridia [25]. In particular the attachment of released spermatozoids to polylysine-coated slides considerably reduces the necessary preparation time for the observation of sperms.…”

“…While the light-microscopic analysis of the sperms is documented in many moss species, e.g. [19–24], and has become a recent focus in the liverwort Marchantia polymorpha [25, 26], the methodology is not established for P. patens . We assume the lack of detailed protocols is the major obstacle preventing research on P. patens sperms and discuss possible reasons so far hindering the establishment of suitable protocols.…”