Patterning mechanisms of cytoskeletal and cell wall systems during leaf trichome morphogenesis

Yanagisawa, Makoto; Desyatova, Anastasia; Belteton, Samuel A.; Mallery, Eileen L.; Turner, Joseph A.; Szymanski, Daniel B.

doi:10.1038/nplants.2015.14

Cited by 110 publications

(172 citation statements)

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“…This pattern also is consistent with predicted cell wall stress patterns, as the magnitude of cell wall stress was predicted to be reduced near three-way junctions, where the cell wall is mechanically reinforced by adjacent cells (analogous to a supported beam; Sampathkumar et al, 2014). Cell wall stress also depends on cell wall thickness (Yanagisawa et al, 2015). Perhaps the localized clustering of microtubules in the thin sections of the anticlinal wall (Supplemental Fig.…”

Section: Discussionsupporting

confidence: 71%

“…Collectively, the above results suggest that stress patterns in the cell wall, due in part to tissue geometry, may pattern the microtubule system and explain why simple parameters like local cell curvature do not explain microtubule patterns. Finite element computational modeling combined with multivariate live-cell imaging is a powerful method with which to analyze how cytoplasmic components, cell wall mechanical properties, and wall stress interact during polarized diffuse growth (Yanagisawa et al, 2015). The development of realistic finite element growth models of pavement cell clusters has the potential to guide experiments that unravel the interactions and feedback controls among cell geometry, cell signaling, and cell wall patterning during epidermal morphogenesis.…”

Section: Discussionmentioning

confidence: 99%

“…Cellulose microfibrils are highly anisotropic with considerable tensile strength; as a result, bundles of aligned fibers in the cell wall can resist strain most effectively parallel to the fiber network and promote orthogonal strain (Baskin, 2005). Clear thresholds for microfibril alignment can explain the highly anisotropic strain of leaf trichomes (Yanagisawa et al, 2015).…”

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confidence: 99%

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Reassessing the Roles of PIN Proteins and Anticlinal Microtubules during Pavement Cell Morphogenesis

et al. 2017

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The leaf epidermis is a biomechanical shell that influences the size and shape of the organ. Its morphogenesis is a multiscale process in which nanometer-scale cytoskeletal protein complexes, individual cells, and groups of cells pattern growth and define macroscopic leaf traits. Interdigitated growth of neighboring cells is an evolutionarily conserved developmental strategy. Understanding how signaling pathways and cytoskeletal proteins pattern cell walls during this form of tissue morphogenesis is an important research challenge. The cellular and molecular control of a lobed cell morphology is currently thought to involve PIN-FORMED (PIN)-type plasma membrane efflux carriers that generate subcellular auxin gradients. Auxin gradients were proposed to function across cell boundaries to encode stable offset patterns of cortical microtubules and actin filaments between adjacent cells. Many models suggest that long-lived microtubules along the anticlinal cell wall generate local cell wall heterogeneities that restrict local growth and specify the timing and location of lobe formation. Here, we used Arabidopsis (Arabidopsis thaliana) reverse genetics and multivariate long-term time-lapse imaging to test current cell shape control models. We found that neither PIN proteins nor long-lived microtubules along the anticlinal wall predict the patterns of lobe formation. In fields of lobing cells, anticlinal microtubules are not correlated with cell shape and are unstable at the time scales of cell expansion. Our analyses indicate that anticlinal microtubules have multiple functions in pavement cells and that lobe initiation is likely controlled by complex interactions among cell geometry, cell wall stress patterns, and transient microtubule networks that span the anticlinal and periclinal walls.Plant leaves are thin, mechanically durable organs. Their size and shape influence the efficiency of photosynthetic light capture and strongly influence crop yield (Zhu et al., 2010). The growth properties of the leaf epidermis can influence the morphology of the organ (Savaldi-Goldstein et al., 2007); therefore, there is a strong desire to understand how the division and growth of epidermal cells contribute to polarized growth at the level of tissues and organs. In the plant kingdom, an undulating cell shape is commonly generated in the leaf epidermis as polyhedral cells exit the cell division cycle and undergo an extended phase of polarized expansion (Panteris et al., 1993;Panteris and Galatis, 2005;Andriankaja et al., 2012). Interdigitated growth may give the leaf mechanical stability (Onoda et al., 2015;Sahaf and Sharon, 2016) and/or influence polarized growth at spatial scales that extend beyond that of individual cells (Elsner et al., 2012;Remmler and Rolland-Lagan, 2012).The biomechanics of the lobing process is complex. As in all other plant cell types, turgor pressure provides the driving force for pavement cell morphogenesis, and the physical connectivity of adjacent cells strongly influences the resulting mechanical stre...

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Section: Discussionsupporting

confidence: 71%

Section: Discussionmentioning

confidence: 99%

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confidence: 99%

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Reassessing the Roles of PIN Proteins and Anticlinal Microtubules during Pavement Cell Morphogenesis

et al. 2017

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“…Analogous extremes of dendritic F‐actin enrichment are not widely observed in higher plant cells, suggesting that these structures are either prohibitively dynamic or rarified amongst a brighter population of stable bundled cables. The apical tip of developing trichome branches is an exception (Yanagisawa et al ., 2015) and demonstrates that relatively isolated and nebulous arrays of branch‐rich actin can have significant impacts on cell morphogenesis. Our genetic data therefore probably indicate the action of a distinct subset of dynamic F‐actin arrays that will prove to be a test for live‐cell imaging approaches.…”

Section: Discussionmentioning

confidence: 99%

Actin filament reorganisation controlled by the SCAR/WAVE complex mediates stomatal response to darkness

Isner

Costa

et al. 2017

New Phytologist

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Summary Stomata respond to darkness by closing to prevent excessive water loss during the night. Although the reorganisation of actin filaments during stomatal closure is documented, the underlying mechanisms responsible for dark‐induced cytoskeletal arrangement remain largely unknown.We used genetic, physiological and cell biological approaches to show that reorganisation of the actin cytoskeleton is required for dark‐induced stomatal closure.The opal5 mutant does not close in response to darkness but exhibits wild‐type (WT) behaviour when exposed to abscisic acid (ABA) or CaCl2. The mutation was mapped to At5g18410, encoding the PIR/SRA1/KLK subunit of the Arabidopsis SCAR/WAVE complex. Stomata of an independent allele of the PIR gene (Atpir‐1) showed reduced sensitivity to darkness and F1 progenies of the cross between opal5 and Atpir‐1 displayed distorted leaf trichomes, suggesting that the two mutants are allelic. Darkness induced changes in the extent of actin filament bundling in WT. These were abolished in opal5. Disruption of filamentous actin using latrunculin B or cytochalasin D restored wild‐type stomatal sensitivity to darkness in opal5.Our findings suggest that the stomatal response to darkness is mediated by reorganisation of guard cell actin filaments, a process that is finely tuned by the conserved SCAR/WAVE–Arp2/3 actin regulatory module.

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“…In addition, unlike the role of formins in nucleating the unbranched actin filaments, the actin-related protein2/3 (ARP2/3) complex is known to form a branched actin network (Cheung and Wu, 2004). During Arabidopsis leaf trichome morphogenesis, the ARP2/3-generated actin meshwork and a microtubule-depletion zone are required for cell wall assembly to maintain the length of the elongating trichome branch (Yanagisawa et al, 2015), indicating the cooperation of the apical actin meshwork and the microtubule cytoskeleton in the establishment of cell wall pattern and shape. The differentiated function in tip growth regulation between the ARP2/3 complex and formins is likely to result from the different manners of actin nucleation.…”

Section: Tip Localization Of Rmd Is Essential For F-actin Organizatiomentioning

confidence: 99%

Rice Morphology Determinant-Mediated Actin Filament Organization Contributes to Pollen Tube Growth

Yang

Zhang

et al. 2018

Plant Physiol.

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Patterning mechanisms of cytoskeletal and cell wall systems during leaf trichome morphogenesis

Cited by 110 publications

References 49 publications

Reassessing the Roles of PIN Proteins and Anticlinal Microtubules during Pavement Cell Morphogenesis

Reassessing the Roles of PIN Proteins and Anticlinal Microtubules during Pavement Cell Morphogenesis

Actin filament reorganisation controlled by the SCAR/WAVE complex mediates stomatal response to darkness

Rice Morphology Determinant-Mediated Actin Filament Organization Contributes to Pollen Tube Growth

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