Update: on selected ROP cell polarity mechanisms in plant cell morphogenesis

Abstract

The unequal (asymmetric) distribution of cell structures and proteins within a cell is designated as cell polarity. Cell polarity is a crucial prerequisite for morphogenetic processes such as oriented cell division and directed cell expansion. Rho-related plants (ROPs) are required for cellular morphogenesis through the reorganization of the cytoskeleton and vesicle transport in various tissues. Here, I review recent advances in ROP-dependent tip growth, vesicle transport, and tip architecture. I report on the regulatory mechanisms of ROP upstream regulators found in different cell types. It appears that these regulators assemble in nanodomains with specific lipid compositions and recruit ROPs for activation in a stimulus-dependent manner. Current models link mechanosensing/mechanotransduction to ROP polarity signaling involved in feedback mechanisms via the cytoskeleton. Finally, I discuss ROP signaling components that are upregulated by tissue-specific transcription factors and exhibit specific localization patterns during cell division, clearly suggesting ROP signaling in division plane alignment. Advances box: Progress has been made in the characterization of upstream regulators of ROPase signaling in diverse tissues, revealing a common theme of RopGEF phosphoregulation by diverse kinases initiating various ROP signaling cascadesNovel insights link mechanosensing/signal transduction pathways, ROP signaling, and cell wall-reinforcing feedback mechanismsIn response to different stimulants, ROP GTPases are recruited to distinct, pre-existing nanodomains composed of specific lipids and RopGEFs. Thus, one ROP GTPase may respond differently to different stimuliMaintenance of tip architecture in tip-growing cells requires secretory and endocytic trafficking, but the precise site of endocytosis may differ between cell types/speciesCell polarity signaling molecules locate at the cortical division site, or are particularly excluded from it; analysis of respective mutant phenotypes implicate the respective genes in division plane selection in different tissue contexts and diverse plant taxa, suggesting evolutionary conservation

Plant cell polarity: The many facets of sidedness

“…In maize stomatal development, ROP proteins are polarized with the receptor proteins to specify the asymmetric division of the subsidiary cells ( Humphries et al 2011 ). Müller updates the recent progress in the analysis of ROP signaling for formative cell divisions in early phloem progenitor and root meristem cells ( Müller 2023 ). Several components and regulators of the ROP signaling pathway show dynamic and specific relationships with the assembly and disassembly of the preprophase band in the cortical division zone ( Stöckle et al 2016 ; Kumari et al 2021 ).…”

“…Polarized plasma membrane domains integrate hormonal, mechanical, and position cues to organize subcellular structures and functions for cell wall remodeling, growth, or defense. As reviewed by Müller ( Müller 2023 ), both tip-growing cells, such as the pollen tube and root hair, and multipolar expanding cells, such as pavement cells, provide excellent platforms to study how regulators of cell polarity orchestrate cellular events in cytoskeletal organization, endomembrane trafficking dynamics, and mechanical signaling to polarize a plant cell for its functional form. Müller first reviews recent advances in understanding tip architecture and ROP-dependent tip growth, highlighting how upstream ROP regulator RopGEFs are regulated by diverse kinases to initiate ROP signaling.…”

“…She shares insights linking cell wall mechanics, mechanosensing, ROP signaling, and cell wall reinforcing feedback mechanisms in pavement cell morphogenesis that requires the existence of two opposing pathways in the lobe and indentation regions of an expanding pavement cell. Pan et al ( Pan et al 2023 ) and Müller ( Müller 2023 ) both highlight new advances suggesting the involvement of auxin-triggered TMK activation of ROP6 nanoclustering on the indentation/concave side ( Pan et al 2020 ) and brassinosteroids-mediated inhibition of the BR-INSENSITIVE 2 kinase signaling to activate ROP2 on the lobe/convex side ( Lauster et al 2022 ; Zhang et al 2022 ).…”

“…Several components and regulators of the ROP signaling pathway show dynamic and specific relationships with the assembly and disassembly of the preprophase band in the cortical division zone ( Stöckle et al 2016 ; Kumari et al 2021 ). Inspired by the recent work demonstrating ROP's function in spatial patterning of cell division in the liverwort Marchantia polymorph ( Rong et al 2022 ), she suggests ROP GTPases could contribute to division orientation more broadly ( Müller 2023 ), possibly linking local cell behavior to tissue wide polarity field ( Mansfield et al 2018 ).…”