Fundamental mechanisms of the stem cell regulation in land plants: lesson from shoot apical cells in bryophytes

Abstract

Key message This review compares the molecular mechanisms of stem cell control in the shoot apical meristems of mosses and angiosperms and reveals the conserved features and evolution of plant stem cells. Abstract The establishment and maintenance of pluripotent stem cells in the shoot apical meristem (SAM) are key developmental processes in land plants including the most basal, bryophytes. Bryophytes, such as Physcomitrium (Physcomitrella) patens and Marchantia polymorpha, are emerging as attractive model species to study the conserved features and evolutionary processes in the mechanisms controlling stem cells. Recent studies using these model bryophyte species have started to uncover the similarities and differences in stem cell regulation between bryophytes and angiosperms. In this review, we summarize findings on stem cell function and its regulation focusing on different aspects including hormonal, genetic, and epigenetic control. Stem cell regulation through auxin, cytokinin, CLAVATA3/EMBRYO SURROUNDING REGION-RELATED (CLE) signaling and chromatin modification by Polycomb Repressive Complex 2 (PRC2) and PRC1 is well conserved. Several transcription factors crucial for SAM regulation in angiosperms are not involved in the regulation of the SAM in mosses, but similarities also exist. These findings provide insights into the evolutionary trajectory of the SAM and the fundamental mechanisms involved in stem cell regulation that are conserved across land plants.

Control of Arabidopsis shoot stem cell homeostasis by two antagonistic CLE peptide signalling pathways

“…receptors, MpTDR and MpCLV1, respectively (Hata & Kyozuka, 2021). By the complementation of clv3 mutants through expression of CLE40 from the CLV3 promoter it was shown previously that CLE40 and CLV3 are able to activate the same downstream receptors (Hobe et al, 2003).…”

“…So far, the antagonistic effects of Arabidopsis CLV3 and CLE40 on meristem size can only be compared to the antagonistic functions of MpCLE1 and MpCLE2 on the gametophytic meristems of M. polymorpha , which signal through two distinct receptors, MpTDR and MpCLV1, respectively (Hata & Kyozuka, 2021). By the complementation of clv3 mutants through expression of CLE40 from the CLV3 promoter it was shown previously that CLE40 and CLV3 are able to activate the same downstream receptors (Hobe et al, 2003).…”

“…Broadly expressed CLE peptides were here found to restrict stem cell identity, and act in division plane control (Whitewoods et al, 2018). Proliferation of the apical notch cell in the liverwort Marchantia polymorpha is promoted by MpCLE2 peptide which acts from outside the stem cell domain via the receptor MpCLV1, while cell proliferation is confined by MpCLE1 peptide through a different receptor (Hata & Kyozuka, 2021; Hirakawa et al, 2019, 2020; Takahashi et al, 2021). Thus, antagonistic control of stem cell activities through diverse CLE peptides is conserved between distantly related land plants.…”

Homeostasis in shoot apical meristems: The balance between stem cells and differentiated cells

“…The role of auxin in the development of SAM was previously thought to be solely for differentiation into organ formation [57,58]. However, recent studies have shown that auxin is also effective in maintaining the meristematic structure in SAM [59,60]. The structures that work in this regard are called AUXIN RESPONSE FACTORs (ARFs) [61,62].…”

Calpain DEK1 acts as a developmental switch gatekeeping cell fate transitions

“…Generally, its evolutionary position as a representative of the earliest diverging clade of land plants, the available reference genome and high-quality annotation resources (Lang et al, 2018), the well-established molecular toolbox and the comprehensive transcriptomics resources covering the entire life cycle (e.g. Frank and Scanlon, 2015;Perroud et al, 2018;Kirbis et al, 2020) make it an attractive model of choice for land plant evo-devo studies like ours (Rensing et al, 2020;Hata and Kyozuka, 2021;Keijzer et al, 2021). Specifically, the simple morphological structures in the early development of the moss, comprising mostly single-cell-layered tissues, is not impeded in the DEK1 null mutants (Perroud et al, 2014;Demko et al, 2014;Johansen et al, 2016) and thus facilitate transcriptional and phenotypic profiling along a longer developmental time course including the 2D to 3D transition of the moss' simplex shoot meristem.…”