SOL1 and SOL2 Regulate Fate Transition and Cell Divisions in the Arabidopsis Stomatal Lineage
Preprint posted on August 17, 2018 https://www.biorxiv.org/content/early/2018/08/17/394940
Article now published in Development at http://dx.doi.org/10.1242/dev.171066
Background: Arabidopsis stomatal development is controlled by the sequential action of three bHLH transcription factors
Stomata are epidermal pores that enable controlled gas exchange across the leaf’s surface while restricting water loss and are thus crucial for a plant’s survival. In Arabidopsis, they are formed by a distinctive set of cell divisions and cell state transitions. Protodermal cells enter the stomatal cell lineage through an asymmetric entry division that gives rise to a smaller cell, the meristemoid, and a larger stomatal lineage ground cell (SLGC). The meristemoid has limited self-renewing capability, it can undergo further asymmetric amplifying divisions and thereby produce additional SLGCs. Eventually, the meristemoid then differentiates into a guard mother cell (GMC), which divides once symmetrically to give rise to the two guard cells (GCs) that form a stoma (Fig. 1). The surrounding SLGCs can either differentiate into pavement cells – the puzzle-shaped basic cell type of the epidermis – or can themselves undergo another asymmetric division, giving rise to a satellite meristemoid. This division is referred to as a spacing division as the new meristemoid is formed away from the existing meristemoid/stoma, ensuring that two stomata are always separated by at least one non-stomatal cell (“one cell spacing rule”).
Cell divisions and cell state transitions in the stomatal lineage are controlled by the sequential action of three closely related bHLH transcription factors1, 2: SPEECHLESS (SPCH) promotes entry, amplifying and spacing divisions; MUTE represses meristemoid identity in the GMC and triggers its symmetric division to form GCs; eventually, FAMA prevents further division of the GCs and locks them in a differentiated state. How these processes are controlled downstream of these transcription factors has only begun to be understood. In their preprint, Simmons, Davies et al. report the cysteine-rich repeat (CXC)-hinge-CXC (CHC) proteins TSO-LIKE1 (SOL1) and SOL2 as novel SPCH targets, whose function is required for several cell state transitions throughout the stomatal lineage.
Key findings: SOL1 and SOL2 are required for multiple cell state transitions in the stomatal lineage
Genes directly bound and upregulated by SPCH had been identified in a previous study by the Bergmann lab3. Two of these direct targets – SOL1 and SOL2 – are homologues of animal DNA-binding components of DREAM complexes, protein complexes involved in cell cycle regulation and cell differentiation4. As the SOLs’ function in Arabidopsis was unknown, the authors investigated a potential function of SOL1 and SOL2 in stomatal development.
Expression of SOL transcriptional and translational reporters was detected in meristemoids and GMCs, following the expression of SPCH-CFP and MUTE-CFP reporters, respectively. Time lapse imaging further pinned down the precise timing of SOL protein accumulation – their signals disappeared just before the division of the meristemoid or GMC, suggesting that their accumulation is tightly linked to the cell cycle.
To further understand SOL function, the authors went on to characterise T-DNA insertion mutants. While single sol1 and sol2 mutants showed no apparent defect in epidermal patterning, a sol1 sol2 double mutant displayed an increased number of small meristemoid-like cells occurring in clusters in a young leaf’s epidermis and pairs of stomata in direct contact in the epidermis of mature leaves. Time lapse imaging revealed that these pairs can form in two different ways: (1) Two meristemoids in a cluster of four may differentiate into GMCs, with the subsequent symmetrical divisions giving rise to two stomata in contact; (2) GCs may divide symmetrically a second time to form four GCs. Thus, SOLs appear to have multiple roles: as downstream targets of SPCH they promote the transition of meristemoids into GMCs, but they are also required at the following stage (possibly downstream of MUTE), restricting the GMC to a single symmetric division (Fig. 2).
The closest paralogue of SOL1 and SOL2, TSO1, also turned out to be involved in stomatal development. Whereas tso1 single mutants did not display altered epidermal patterning, knock-down of TSO1 in the sol1 sol2 background led to the formation of single guard cells (SGCs) that failed to divide, a phenotype also generated by SOL2 overexpression. Thus, TSO1 appears to act partially in opposition to SOL1 and SOL2, promoting the final GMC division.
What I like about this preprint
How patterns emerge during tissue and organ formation is a fundamental question in developmental biology. The present study does a remarkable job at shining more light onto one of these processes: it identifies novel regulators of stomatal patterning downstream of known master regulators, gives us an idea about their function in early and late stages of the process and opens up several lines of research that can be followed from here on.
Open questions/future research: DREAMing of CHC protein function in Arabidopsis
With novel functions assigned to some Arabidopsis CHC proteins, this protein family may draw more interest in the future. Some open questions that may be addressed are:
- There are eight CHC proteins in Arabidopsis, five of them uncharacterised – do they they have a role in stomatal development as well?
- Animal CHC proteins are part of DREAM multiprotein complexes – is this also the case for the SOLs in plants?
- SOLs may function as repressors of the cell cycle – which targets do they control to achieve this function?
- Lack of SOLs slows the transition from meristemoid to GMC, but does not prevent it completely. Which proteins contribute to this transition alongside the SOLs?
- Han, SK, and Torii, KU (2016). Lineage-specific stem cells, signals and asymmetries during stomatal development. Development 143(8): 1259-70.
- Lau, OS, and Bergmann, DC (2012). Stomatal development: a plant’s perspective on cell polarity, cell fate transitions and intercellular communication. Development 139(20): 3683–3692
- Lau, OS, Davies, KA, Chang, J, Adrian, J, Rowe, MH, Ballenger, CE, Bergmann, DC (2014). Direct roles of SPEECHLESS in the specification of stomatal self-renewing cells. Science 345(6204): 1605-1609.
- Sadasivam, S, and DeCaprio, JA (2013). The DREAM complex: master coordinator of cell cycle-dependent gene expression. Nat Rev Cancer 13(8): 585-595
Posted on: 3rd September 2018Read preprint
Also in the developmental biology category:
Human-specific ARHGAP11B is necessary and sufficient for human-type basal progenitor levels in primate brain organoids
|Selected by||Ana Uzquiano|
The chromatin, topological and regulatory properties of pluripotency-associated poised enhancers are conserved in vivo
|Selected by||Sergio Menchero|
Ciliary control of meiotic chromosomal pairing mechanics and germ cell morphogenesis
|Selected by||Robert Mahen|
Also in the plant biology category:
Antiviral activity of bacterial TIR domains via signaling molecules that trigger cell death
|Selected by||Jonny Coates, Connor Rosen|
Creating Clear and Informative Image-based Figures for Scientific Publications
|Selected by||Mariana De Niz|
Major components in the KARRIKIN INSENSITIVE2-ligand signaling pathway are conserved in the liverwort, Marchantia polymorpha
The Physcomitrium (Physcomitrella) patens PpKAI2L receptors for strigolactones and related compounds highlight MAX2 dependent and independent pathways
|Selected by||Facundo Romani|
preListsdevelopmental biology category:in the
EMBL Conference: From functional genomics to systems biology
Preprints presented at the virtual EMBL conference "from functional genomics and systems biology", 16-19 November 2020
|List by||Jesus Victorino|
Single Cell Biology 2020
A list of preprints mentioned at the Wellcome Genome Campus Single Cell Biology 2020 meeting.
|List by||Alex Eve|
Society for Developmental Biology 79th Annual Meeting
Preprints at SDB 2020
|List by||Irepan Salvador-Martinez, Martin Estermann|
A collection of preprints presented during the virtual meeting of the Federation of European Neuroscience Societies (FENS) in 2020
|List by||Ana Dorrego-Rivas|
Planar Cell Polarity – PCP
This preList contains preprints about the latest findings on Planar Cell Polarity (PCP) in various model organisms at the molecular, cellular and tissue levels.
|List by||Ana Dorrego-Rivas|
Recent research from the field of cell polarity is summarized in this list of preprints. It comprises of studies focusing on various forms of cell polarity ranging from epithelial polarity, planar cell polarity to front-to-rear polarity.
|List by||Yamini Ravichandran|
Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20
|List by||Maiko Kitaoka, Madhuja Samaddar, Miguel V. Almeida, Sejal Davla, Jennifer Ann Black, Dey Lab|
A curated list of preprints related to Gastruloids (in vitro models of early development obtained by 3D aggregation of embryonic cells). Preprint missing? Don't hesitate to let us know.
|List by||Paul Gerald L. Sanchez and Stefano Vianello|
ASCB EMBO Annual Meeting 2019
A collection of preprints presented at the 2019 ASCB EMBO Meeting in Washington, DC (December 7-11)
|List by||Madhuja Samaddar, Ramona Jühlen, Amanda Haage, Laura McCormick, Maiko Kitaoka|
EDBC Alicante 2019
Preprints presented at the European Developmental Biology Congress (EDBC) in Alicante, October 23-26 2019.
|List by||Sergio Menchero, Jesus Victorino, Teresa Rayon, Irepan Salvador-Martinez|
EMBL Seeing is Believing – Imaging the Molecular Processes of Life
Preprints discussed at the 2019 edition of Seeing is Believing, at EMBL Heidelberg from the 9th-12th October 2019
|List by||Dey Lab|
SDB 78th Annual Meeting 2019
A curation of the preprints presented at the SDB meeting in Boston, July 26-30 2019. The preList will be updated throughout the duration of the meeting.
|List by||Alex Eve|
Lung Disease and Regeneration
This preprint list compiles highlights from the field of lung biology.
|List by||Rob Hynds|
Young Embryologist Network Conference 2019
Preprints presented at the Young Embryologist Network 2019 conference, 13 May, The Francis Crick Institute, London
|List by||Alex Eve|
Pattern formation during development
The aim of this preList is to integrate results about the mechanisms that govern patterning during development, from genes implicated in the processes to theoritical models of pattern formation in nature.
|List by||Alexa Sadier|
BSCB/BSDB Annual Meeting 2019
Preprints presented at the BSCB/BSDB Annual Meeting 2019
|List by||Dey Lab|
A compilation of cutting-edge research that uses the zebrafish as a model system to elucidate novel immunological mechanisms in health and disease.
|List by||Shikha Nayar|