Positional cues regulate dorsal organ formation in the liverwort Marchantia polymorpha

Abstract

Bryophytes and vascular plants represent the broadest evolutionary divergence in the land plant lineage, and comparative analyses of development spanning this divergence therefore offer opportunities to identify truisms of plant development in general. In vascular plants, organs are formed repetitively around meristems at the growing tips in response to positional cues. In contrast, leaf formation in mosses and leafy liverworts occurs from clonal groups of cells derived from a daughter cell of the apical stem cell known as merophytes, and cell lineage is a crucial factor in repetitive organ formation.However, it remains unclear whether merophyte lineages are a general feature of repetitive organ formation in bryophytes as patterns of organogenesis in thalloid liverworts are unclear. To address this question, we developed a clonal analysis method for use in the thalloid liverwort Marchantia polymorpha, involving random lowfrequency induction of a constitutively expressed nuclear-targeted fluorescent protein by dual heat-shock and dexamethasone treatment. M. polymorpha thalli ultimately derive from stem cells in the apical notch, and the lobes predominantly develop from merophytes cleft to the left and right of the apical cell(s). Sector induction in gemmae and subsequent culture occasionally generated fluorescent sectors that bisected thalli along the midrib and were maintained through several bifurcation events, likely reflecting the border between lateral merophytes. Such thallus-bisecting sectors traversed dorsal air pores and gemma cups, suggesting that these organs arise independently of merophyte cell lineages in response to local positional cues.

The BES1/BZR1-family transcription factor MpBES1 regulates cell division and differentiation in Marchantia polymorpha

“…A single stem cell divides in four planes to produce dorsal, ventral, and bilateral merophytes that proliferate and differentiate in response to local cues as they become separated from the meristem. 24 To take a closer look at the meristematic regions, we stained proliferating nuclei in 3-day-old gemmae of WT and of a b-estradiol-inducible amiR-MpBES1 line (amiR-MpBES1 ind ; Figures S2E and S2F) with 5-ethynyl-2 0 -deoxyuridine (EdU) (Figure 3A). Induced expression of the amiR-MpBES1 led to a reduced number of cells at the notches undergoing DNA duplication (Figures 3A and 3B) and an increased proportion of gemmae with only one active meristem (Figure 3C).…”

Gemma cup and gemma development in Marchantia polymorpha

“…1d). Clonal analysis revealed that a gemma cup comprises at least three independent cell lineages: the dorsal progeny of the apical cell and flanking lateral merophytes (Suzuki et al ., 2020; Box 1). The floor is a region where the periclinal cell divisions that generate protodermal and subprotodermal cell layers of the air chamber are suppressed and, instead, consecutive elongated epidermal cells are observed.…”

An Evolutionarily Conserved Coreceptor Gene Is Essential for CLAVATA Signaling in Marchantia polymorpha

“…Gemma cups are specialized structures for vegetative propagation, found in certain species of Marchantiopsida (Yasui et al, 2019;Kato et al, 2020). Gemma cup formation initiates at the cells in the dorsal epidermis close to the apical cells (Suzuki et al, 2020). We show that gain-of-function of MpCLE2 results in the delay of gemma cup formation.…”