Diversity, development and evolution of archegonia in land plants

Abstract

We review the diversity and development of archegonia, the female reproductive organs of land-plant gametophytes. The archegonium is a uniquely land-plant structure, and studies of its evolution benefit from use of a comparative approach in a phylogenetic context. Archegonia of most land plants share a common developmental motif, here termed a T-shaped pattern. A primary axial cell produces a primary cover cell and a central cell by horizontal division. The upper cell usually divides vertically and the lower one horizontally. In mosses such as Atrichum, the T-shaped stage is shifted towards the end of archegonium development, whereas in vascular plants it appears at the beginning of development, but these stages are still probably homologous. The fully exposed archegonia are traditionally viewed as an ancestral (plesiomorphic) condition in land plants, but there is no direct support for this view. We speculate that the fully exposed condition is derived and synapomorphic for setaphytes (mosses and liverworts). The fully sunken hornwort archegonia may be similar to the ancestral type of land-plant archegonia. Developmental evidence suggests that archegonium necks of setaphytes and tracheophytes are not homologous to each other. The neck wall of pteridophytes is composed of four-celled tiers, and one such tier is present in gymnosperms with motile male gametes. Neck-cell arrangement is much more plastic in archegonia of gymnosperms with sperm cell delivery by pollen tube (siphonogamy), in which the neck plays a role similar to pollen-tube transmitting tissue of angiosperms. Angiosperm synergids are probably homologues of gymnosperm neck cells, and the angiosperm egg cell is probably homologous to the ventral canal cell of gymnosperms. Developmental genetic bases of archegonium diversity in land plants remain to be understood. Even descriptive developmental data are currently missing or controversial for some key lineages of land plants.

Evolutionarily Conserved CKI1-Mediated Two-Component Signaling is Required for Female Germline Specification inMarchantia polymorpha

“…8 The development of archegonia in M. polymorpha has been described in previous histological studies, which showed that a single archegonial initial cell undergoes threedimensional growth with precisely regulated cell divisions in different planes to form a mature archegonium (Figures 1B and S3D). 3,16,27,28 We first observed the fluorescence pattern in MpBNB-Citrine expressing archegonia carrying the native MpCKI1 allele (Figure 3A). produced normal archegoniophores and egg-bearing archegonia, suggesting that CKI1mediated signaling, but not canonical cytokinin-initiated signaling, is important for female gametogenesis (Figures S4B-S4D).…”

“…1 In angiosperms, one central cell and one egg cell are differentiated in the embryo sac as female gametes for double fertilization, while in non-flowering plants, only one egg cell is generated in the female sexual organ, called the archegonium. 2,3 The central cell specification of Arabidopsis thaliana is controlled by the histidine kinase CYTOKININ-INDEPENDENT 1 (CKI1), which is a two-component signaling (TCS) activator sharing downstream regulatory components with the cytokinin signaling pathway. [4][5][6][7] Our phylogenetic analysis suggested that CKI1 orthologs broadly exist in land plants.…”

Evolution and patterning of the ovule in seed plants

“…Within the megagametophyte, the egg cell is located closest to the micropyle; its fertilization results in a zygote that subsequently forms the embryo in the developing seed. In most land plants, the egg cells are produced within archegonia that develop within the megagametophyte, but in angiosperms the megagametophyte is so reduced that an archegonium is either absent or imperceptible, resulting in contrasting theories about the possible derivation of the angiosperm megagametophyte from an archegoniate structure (Favre-Duchartre, 1984;Rudall, 2006;Sokoloff & Remizowa, 2020).…”

The use of plant ontologies in comparative and evolutionary studies should be flexible

“…All analyses need not necessarily be based on inferred homology assessments. For example, the angiosperm egg nucleus is likely homologous to the non‐angiosperm ventral canal cell nucleus (reviewed by Sokoloff and Remizowa, 2021). This interpretation is important in an evolutionary context, especially with respect to the enigmatic origin of angiosperms.…”

“…It should be analyzed as such and compared to egg cells of other land plants in studies that focus on gene expression patterns governing fertilization. Archegonium necks of bryophytes and pteridophytes are not homologous to each other (see Renzaglia et al, 2000; Sokoloff and Remizowa, 2021), but studies related to sperm attraction and movement can use an ontology that includes a general term “archegonium neck”.…”