All Publications
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Plant cell wall-plasma membrane attachments mediate stress resilience through cellulose synthase complexes and remorins.
Cell
2026
Abstract
The outer cell surface of an organism is the frontline for detecting and responding to environmental stimuli. In plants, this interface consists of the plasma membrane that lies beneath the cell wall and remains associated with it through attachment sites. These wall-membrane attachments become evident upon hyperosmotic shock, when severe water loss causes the membrane to retract from the wall. Despite their long-standing observation, the molecular identity and function of these attachments remain poorly understood. Here, we identified two mechanisms governing wall-membrane attachments: one dependent on the cellulose synthase complex (CSC), whose density at the plasma membrane positively correlates with resistance to hyperosmotic stress, and the other on remorin (REM), which acts antagonistically to the CSC mechanism. Using proximity-labeling proteomics, we identified SHOU4/4L as REM-associated proteins that mediate this antagonism. Together, our findings reveal how wall-membrane attachments are patterned to mediate plant cell resilience under water stress.
View details for DOI 10.1016/j.cell.2026.05.009
View details for PubMedID 42229423
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Correlating physiology and structure with fluorescent biosensors and cryo-ET
CELL PRESS. 2026: 11a
View details for Web of Science ID 001717073300054
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Visualizing spatial and temporal responses of plant cells to the environment
CELL PRESS. 2024: 420A
View details for Web of Science ID 001194120702441
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Environmental biosensors for cryogenic correlative light and electron microscopy
CELL PRESS. 2024: 419A
View details for Web of Science ID 001194120702437
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Mutations in the Pectin Methyltransferase QUASIMODO2 Influence Cellulose Biosynthesis and Wall Integrity in Arabidopsis thaliana.
The Plant cell
2020
Abstract
Pectins are abundant in the cell walls of dicotyledonous plants, but how they interact with other wall polymers and influence wall integrity and cell growth has remained mysterious. Here, we verified that QUASIMODO2 (QUA2) is a pectin methyltransferase and determined that QUA2 is required for normal pectin biosynthesis. To gain further insight into how pectin affects wall assembly and integrity maintenance, we investigated cellulose biosynthesis, cellulose organization, cortical microtubules, and wall integrity signaling in two mutant alleles of Arabidopsis thaliana QUA2, qua2 and tsd2. In both mutants, crystalline cellulose content is reduced, cellulose synthase particles move more slowly, and cellulose organization is aberrant. NMR analysis shows higher mobility of cellulose and matrix polysaccharides in the mutants. Microtubules in mutant hypocotyls have aberrant organization, and depolymerize more readily upon treatment with oryzalin or external force. The expression of genes related to wall integrity, wall biosynthesis, and microtubule stability is dis-regulated in both mutants. These data provide insights into how homogalacturonan is methylesterified upon its synthesis, the mechanisms by which pectin functionally interacts with cellulose, and how these interactions are translated into intracellular regulation to maintain the structural integrity of the cell wall during plant growth and development.
View details for DOI 10.1105/tpc.20.00252
View details for PubMedID 32883711
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A Wall with Integrity: Surveillance and Maintenance of the Plant Cell Wall Under Stress.
The New phytologist
2019
Abstract
The structural and functional integrity of the wall needs to be constantly monitored and fine-tuned to allow for growth while preventing mechanical failure. Many studies have advanced our understanding of the pathways contributing to cell wall biosynthesis and how these pathways are regulated by external and internal cues. Recent evidence also supports a model in which certain aspects of the wall itself may act as growth-regulating signals. Molecular components of the signaling pathways that sense and maintain cell wall integrity have begun to be revealed, including signals arising in the wall, sensors that detect changes at the cell surface, and downstream signal transduction modules. Abiotic and biotic stress conditions set new contexts to study cell wall integrity, but the nature and consequences of wall disruptions by various stressors require further investigations. A deeper understanding of cell wall signaling will provide insights into the growth regulatory mechanisms that allow plants to survive in a changing environment. This article is protected by copyright. All rights reserved.
View details for DOI 10.1111/nph.16166
View details for PubMedID 31486535
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Synergistic Pectin Degradation and Guard Cell Pressurization Underlie Stomatal Pore Formation.
Plant physiology
2019
Abstract
Stomatal pores are vital for the diffusion of gasses into and out of land plants and are, therefore, gatekeepers for photosynthesis and transpiration. Although much published literature has described the intercellular signaling and transcriptional regulators involved in early stomatal development, little is known about the cellular details of the local separation between sister guard cells that give rise to the stomatal pore, or how formation of this pore is achieved. Using 3D time-lapse imaging, we found that stomatal pore formation in Arabidopsis thaliana is a highly dynamic process involving pore initiation and enlargement, and traverses a set of morphological milestones in 3D. Confocal imaging data revealed an enrichment of exocytic machinery, de-methyl-esterified pectic homogalacturonan (HG), and an HG-degrading enzyme at future pore sites, suggesting that both localized HG deposition and degradation might function in pore formation. By manipulating HG modification via enzymatic, chemical, and genetic perturbations in seedling cotyledons, we found that augmenting HG modification promotes pore formation, whereas preventing HG de-methyl-esterification delays pore initiation and inhibits pore enlargement. Through mechanical modeling and experimentation, we tested whether pore formation is an outcome of sister guard cells being pulled away from each other upon turgor increase. Osmotic treatment to reduce turgor pressure did not prevent pore initiation, but did lessen pore enlargement. Together, these data provide evidence that HG delivery and modification, and guard cell pressurization, make functional contributions to stomatal pore initiation and enlargement.
View details for DOI 10.1104/pp.19.00135
View details for PubMedID 30804009
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Mechanical Effects of Cellulose, Xyloglucan, and Pectins on Stomatal Guard Cells of Arabidopsis thaliana
FRONTIERS IN PLANT SCIENCE
2018; 9
View details for DOI 10.3389/fpls.2018.01566
View details for Web of Science ID 000449281200001
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Predicting Division Planes of Three-Dimensional Cells by Soap-Film Minimization
PLANT CELL
2018; 30 (10): 2255-2266
Abstract
One key aspect of cell division in multicellular organisms is the orientation of the division plane. Proper division plane establishment contributes to normal plant body organization. To determine the importance of cell geometry in division plane orientation, we designed a three-dimensional probabilistic mathematical model to directly test the century-old hypothesis that cell divisions mimic soap-film minima. According to this hypothesis, daughter cells have equal volume and the division plane occurs where the surface area is at a minimum. We compared predicted division planes to a plant microtubule array that marks the division site, the preprophase band (PPB). PPB location typically matched one of the predicted divisions. Predicted divisions offset from the PPB occurred when a neighboring cell wall or PPB was directly adjacent to the predicted division site to avoid creating a potentially structurally unfavorable four-way junction. By comparing divisions of differently shaped plant cells (maize [Zea mays] epidermal cells and developing ligule cells and Arabidopsis thaliana guard cells) and animal cells (Caenorhabditis elegans embryonic cells) to divisions simulated in silico, we demonstrate the generality of this model to accurately predict in vivo division. This powerful model can be used to separate the contribution of geometry from mechanical stresses or developmental regulation in predicting division plane orientation.
View details for DOI 10.1105/tpc.18.00401
View details for Web of Science ID 000450000500007
View details for PubMedID 30150312
View details for PubMedCentralID PMC6241264
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Balancing Strength and Flexibility: How the Synthesis, Organization, and Modification of Guard Cell Walls Govern Stomatal Development and Dynamics
FRONTIERS IN PLANT SCIENCE
2018; 9
View details for DOI 10.3389/fpls.2018.01202
View details for Web of Science ID 000442093900001
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POLYGALACTURONASE INVOLVED IN EXPANSION3 Functions in Seedling Development, Rosette Growth, and Stomatal Dynamics in <i>Arabidopsis thaliana</i>
PLANT CELL
2017; 29 (10): 2413-2432
Abstract
Plant cell separation and expansion require pectin degradation by endogenous pectinases such as polygalacturonases, few of which have been functionally characterized. Stomata are a unique system to study both processes because stomatal maturation involves limited separation between sister guard cells and stomatal responses require reversible guard cell elongation and contraction. However, the molecular mechanisms for how stomatal pores form and how guard cell walls facilitate dynamic stomatal responses remain poorly understood. We characterized POLYGALACTURONASE INVOLVED IN EXPANSION3 (PGX3), which is expressed in expanding tissues and guard cells. PGX3-GFP localizes to the cell wall and is enriched at sites of stomatal pore initiation in cotyledons. In seedlings, ablating or overexpressing PGX3 affects both cotyledon shape and the spacing and pore dimensions of developing stomata. In adult plants, PGX3 affects rosette size. Although stomata in true leaves display normal density and morphology when PGX3 expression is altered, loss of PGX3 prevents smooth stomatal closure, and overexpression of PGX3 accelerates stomatal opening. These phenotypes correspond with changes in pectin molecular mass and abundance that can affect wall mechanics. Together, these results demonstrate that PGX3-mediated pectin degradation affects stomatal development in cotyledons, promotes rosette expansion, and modulates guard cell mechanics in adult plants.
View details for DOI 10.1105/tpc.17.00568
View details for Web of Science ID 000414861100013
View details for PubMedID 28974550
View details for PubMedCentralID PMC5774581
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Functional Analysis of Cellulose and Xyloglucan in the Walls of Stomatal Guard Cells of Arabidopsis
PLANT PHYSIOLOGY
2016; 170 (3): 1398-1419
Abstract
Stomatal guard cells are pairs of specialized epidermal cells that control water and CO2 exchange between the plant and the environment. To fulfill the functions of stomatal opening and closure that are driven by changes in turgor pressure, guard cell walls must be both strong and flexible, but how the structure and dynamics of guard cell walls enable stomatal function remains poorly understood. To address this question, we applied cell biological and genetic analyses to investigate guard cell walls and their relationship to stomatal function in Arabidopsis (Arabidopsis thaliana). Using live-cell spinning disk confocal microscopy, we measured the motility of cellulose synthase (CESA)-containing complexes labeled by green fluorescent protein (GFP)-CESA3 and observed a reduced proportion of GFP-CESA3 particles colocalizing with microtubules upon stomatal closure. Imaging cellulose organization in guard cells revealed a relatively uniform distribution of cellulose in the open state and a more fibrillar pattern in the closed state, indicating that cellulose microfibrils undergo dynamic reorganization during stomatal movements. In cesa3(je5) mutants defective in cellulose synthesis and xxt1 xxt2 mutants lacking the hemicellulose xyloglucan, stomatal apertures, changes in guard cell length, and cellulose reorganization were aberrant during fusicoccin-induced stomatal opening or abscisic acid-induced stomatal closure, indicating that sufficient cellulose and xyloglucan are required for normal guard cell dynamics. Together, these results provide new insights into how guard cell walls allow stomata to function as responsive mediators of gas exchange at the plant surface.
View details for DOI 10.1104/pp.15.01066
View details for Web of Science ID 000375420300018
View details for PubMedID 26729799
View details for PubMedCentralID PMC4775103
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Integrating cell biology, image analysis, and computational mechanical modeling to analyze the contributions of cellulose and xyloglucan to stomatal function
PLANT SIGNALING & BEHAVIOR
2016; 11 (6): e1183086
Abstract
Cell walls are likely to be essential determinants of the amazing strength and flexibility of the guard cells that surround each stomatal pore in plants, but surprisingly little is known about cell wall composition, organization, and dynamics in guard cells. Recent analyses of cell wall organization and stomatal function in the guard cells of Arabidopsis thaliana mutants with defects in cellulose and xyloglucan have allowed for the development of new hypotheses about the relative contributions of these components to guard cell function. Advanced image analysis methods can allow for the automated detection of key structures, such as microtubules (MTs) and Cellulose Synthesis Complexes (CSCs), in guard cells, to help determine their contributions to stomatal function. A major challenge in the mechanical modeling of dynamic biological structures, such as guard cell walls, is to connect nanoscale features (e.g., wall polymers and their molecular interactions) with cell-scale mechanics; this challenge can be addressed by applying multiscale computational modeling that spans multiple spatial scales and physical attributes for cell walls.
View details for DOI 10.1080/15592324.2016.1183086
View details for Web of Science ID 000378740600010
View details for PubMedID 27220916
View details for PubMedCentralID PMC4973784
https://orcid.org/0000-0002-0291-0062