Opposite polarity programs regulate asymmetric subsidiary cell divisions in grasses

Zhang, Dan; Spiegelhalder, Roxane P; Abrash, Emily; Nunes, Tiago D. G.; Hidalgo, Inés; Gil, M. Ximena Anleu; Jesenofsky, Barbara; Lindner, Heike; Bergmann, Dominique C.; Raissig, Michael T.

doi:10.7554/elife.79913

Cited by 24 publications

(26 citation statements)

References 70 publications

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“…Embryonic calli derived from Bd21-3 and bdpox-1 parental plants were transformed with AGL1 Agrobacterium tumefaciens containing the binary expression vectors, selected based on hygromycin resistance, and regenerated as described in Zhang et al (2022) 8 . In short, young, transparent embryos were isolated and grown for three weeks on callus induction media (CIM; per L: 4.43g Linsmaier & Skoog basal media (LS; Duchefa #L0230), 30g sucrose, 600μl CuSO4 (1mg/ ml, Sigma/Merck #C3036), 500μl 2,4-D (5mg/ml in 1M KOH, Sigma/Merck #D7299), pH 5.8, plus 2.1g of Phytagel (Sigma/Merck #P8169)).…”

Section: Methodsmentioning

confidence: 99%

“…25 mature leaf zones (25-30 mm from the base of 2 nd leaves) per replicate were collected from three wild-type (Bd21-3) replicates and from three bdmute replicates (7 days after germination seedlings grown on ½ MS plates at 20 o C with ~100 µmol photons m -2 s -1 light) were carefully collected, snap-frozen in liquid nitrogen and grounded using mortar and pistil. RNA extraction, library preparation, RNA-sequencing and data analysis was essentially performed as described in Zhang et al (2022) 8 . To be specific, total RNA was isolated using Qiagen's RNeasy Plant Mini kit with on-column DNAse digestion according to the manufacturer's instructions.…”

Section: Rna-sequencingmentioning

confidence: 99%

“…179 genes were downregulated in bdmute (Supplementary Dataset) and we selected ~50 candidate genes for a reverse genetic screening. Candidates were chosen according to their annotated gene function, their expression being lower in the developmental zone 8 and the availability of mutants from a collection of sodium azide (NaN 3 ) mutagenized and fully resequenced lines 9 .…”

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confidence: 99%

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Regulation of hair cell and stomatal size by a hair-cell specific peroxidase in the grassBrachypodium distachyon

Nunes

Slawinska

Zhang

et al. 2022

Preprint

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The leaf epidermis is the outermost cell layer forming the interface between plants and the atmosphere that must accomplish contrasting functions; it must provide a robust barrier against biotic and abiotic stressors while simultaneously facilitating efficient exchange of carbon dioxide and water. To achieve these opposing requirements, the plant epidermis developed a wide range of specialized cell types such as stomata and hair cells (=trichomes). While factors forming these individual cell types are known, it is poorly understood how their number and size is coordinated. Here, we identified a role for BdPRX76/BdPOX, a class III peroxidase, in regulating both stomata and hair cell size in the model grass Brachypodium distachyon. In bdpox mutants stomata were longer, yet prickle hair cells were smaller. Because stomatal density remained unchanged, the negative correlation between stomatal size and density was disrupted and resulted in higher stomatal conductance and lower intrinsic water-use efficiency. Reporter lines revealed that BdPOX was exclusively expressed in hair cells suggesting that BdPOX cell-autonomously promotes hair cell size and non-cell-autonomously restricts stomatal length. Cell wall autofluorescence and lignin stainings indicated a role for BdPOX in lignification or crosslinking of related phenolic compounds at the hair cell base. Ectopic expression of BdPOX in the stomatal lineage increased phenolic content in guard cell walls and restricted stomatal elongation. Together, we reveal a developmental coordination between hair cells and stomata that optimizes epidermal functionality. We propose that a cell-type-specific disruption of this coordination leads to compensatory developmental defects in other epidermal cell types.

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Section: Methodsmentioning

confidence: 99%

Section: Rna-sequencingmentioning

confidence: 99%

mentioning

confidence: 99%

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Regulation of hair cell and stomatal size by a hair-cell specific peroxidase in the grassBrachypodium distachyon

Nunes

Slawinska

Zhang

et al. 2022

Preprint

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“…Two opposite polarity domains – a proximal domain at the GMC/SMC interface and a distal domain at the apical, basal and distal membrane – guide nuclear migration and specify the cortical division site (Fig. 1c; Zhang et al ., 2022). SCAR/WAVE regulatory complex proteins (Facette et al ., 2015), receptor‐like kinases of the PANGLOSS (PAN) family (Cartwright et al ., 2009; Zhang et al ., 2012), and Rho family GTPases (ROPs; Humphries et al ., 2011) sequentially accumulate within the proximal domain (Fig.…”

Section: Development Of Paracytic Subsidiary Cells In Grassesmentioning

confidence: 99%

“…The distal polarity domain was recently described in B. distachyon and is formed by a grass POLAR homolog (Fig. 1c; Zhang et al ., 2022). POLAR polarization is controlled by the proximal domain and seems to guide the positioning of the cortical division site rather than nuclear migration (Zhang et al ., 2022).…”

Section: Development Of Paracytic Subsidiary Cells In Grassesmentioning

confidence: 99%

From grasses to succulents – development and function of distinct stomatal subsidiary cells

Cheng

Raissig

2023

New Phytologist

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Stomata are breathing pores on leaves that balance photosynthetic carbon dioxide uptake and water vapor loss. Stomatal morphology and complexity are rather diverse when considering stomatal subsidiary cells (SCs). Subsidiary cells are adjacent to the central guard cells (GCs) and are morphologically distinct from other epidermal cells. Yet, how various SCs develop and whether and how they support stomatal gas exchange physiology outside of the grass family is largely unknown. Here, we discuss the development, ontogeny, and putative function of paracytic vs anisocytic SCs, which can be found in grasses and Crassulaceae succulents, respectively. First, we highlight recent advances in understanding how grasses form stomatal SCs. We then summarize novel insights into stomatal development in SC-less Arabidopsis to speculate on how this stomatal program might be rewired to enable anisocytic SC formation. Finally, we discuss the functional relevance of paracytic SCs in grasses and the putative roles of anisocytic SCs in succulents.

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Cell wall anisotropy plays a key role in Zea mays stomatal complex movement: the possible role of the cell wall matrix

Gkolemis,

Giannoutsou,

Adamakis

et al. 2023

Plant Mol Biol

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The opening of the stomatal pore in Zea mays is accomplished by the lateral displacement of the central canals of the dumbbell-shaped guard cells (GCs) towards their adjacent deflating subsidiary cells that retreat locally. During this process, the central canals swell, and their cell wall thickenings become thinner. The mechanical forces driving the outward displacement of the central canal are applied by the asymmetrically swollen bulbous ends of the GCs via the rigid terminal cell wall thickenings of the central canal and the polar ventral cell wall (VW) ends. During stomatal pore closure, the shrinking bulbous GC ends no longer exert the mechanical forces on the central canals, allowing them to be pushed back inwards, towards their initial position, by the now swelling subsidiary cells. During this process, the cell walls of the central canal thicken. Examination of immunolabeled specimens revealed that important cell wall matrix materials are differentially distributed across the walls of Z. mays stomatal complexes. The cell walls of the bulbous ends and of the central canal of the GCs, as well as the cell walls of the subsidiary cells were shown to be rich in methylesterified homogalacturonans (HGs) and hemicelluloses. Demethylesterified HGs were, in turn, mainly located at the terminal cell wall thickenings of the central canal, at the polar ends of the VW, at the lateral walls of the GCs and at the periclinal cell walls of the central canal. During stomatal function, a spatiotemporal change on the distribution of some of the cell wall matrix materials is observed. The participation of the above cell wall matrix polysaccharides in the well-orchestrated response of the cell wall during the reversible movements of the stomatal complexes is discussed.

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Opposite polarity programs regulate asymmetric subsidiary cell divisions in grasses

Cited by 24 publications

References 70 publications

Regulation of hair cell and stomatal size by a hair-cell specific peroxidase in the grassBrachypodium distachyon

Regulation of hair cell and stomatal size by a hair-cell specific peroxidase in the grassBrachypodium distachyon

From grasses to succulents – development and function of distinct stomatal subsidiary cells

Cell wall anisotropy plays a key role in Zea mays stomatal complex movement: the possible role of the cell wall matrix

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