Differential Growth in Periclinal and Anticlinal Walls during Lobe Formation in Arabidopsis Cotyledon Pavement Cells

Armour, William J.; Barton, Deborah; Law, Andrew M. K.; Overall, Robyn L.

doi:10.1105/tpc.114.126664

Cited by 98 publications

(151 citation statements)

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“…In Arabidopsis, an initial growth restriction model was driven largely by the detection of anticlinal microtubule bundles at the convex regions of lobed cell types (Fu et al, 2002). To our knowledge, the article of Armour et al (2015) is the only one to attempt to image microtubules in the same cell prior to and after lobe formation. They concluded that stable anticlinal microtubules predict lobe initiation sites.…”

Section: Development Of An Image-analysis Pipeline To Test For Correlmentioning

confidence: 99%

“…Existing genetic and pharmacological data indicate that microtubules are involved in lobe formation (Burk et al, 2001;Whittington et al, 2001;Qiu et al, 2002;ElDin El-Assal et al, 2004;Ambrose et al, 2007;Armour et al, 2015); however, the details of how microtubules pattern the cell are under debate (Panteris and Galatis, 2005;Xu et al, 2010;Szymanski, 2014). A growth restriction model for lobe initiation includes a component in which anticlinal microtubule bundles persist for extended periods of time prior to a symmetry-breaking event generating local cell wall thickening, and this local thickening resists strain and leads to adjacent cell outgrowth and lobe initiation (Panteris and Galatis, 2005).…”

Section: Development Of An Image-analysis Pipeline To Test For Correlmentioning

confidence: 99%

“…Using time-lapse imaging, it was shown that lobe initiation is not a continuous iterative process during cell expansion. Instead, it occurs predominantly during a permissive phase of seedling development up to ;2 d after germination (DAG; Zhang et al, 2011;Armour et al, 2015;Wu et al, 2016). Subsequently, the pavement cells expand for days and increase in area largely independent of lobe initiation (Zhang et al, 2011;Armour et al, 2015;Wu et al, 2016).…”

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confidence: 99%

“…A recent study analyzed microtubule localization as a function of lobe initiation and concluded that microtubules are stable features that mark lobe initiation sites (Armour et al, 2015). However, this analysis relied on imaging microtubules at a single time point before lobe initiation and lacked a plasma membrane marker to closely monitor the cell boundary.…”

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confidence: 99%

“…Instead, it occurs predominantly during a permissive phase of seedling development up to ;2 d after germination (DAG; Zhang et al, 2011;Armour et al, 2015;Wu et al, 2016). Subsequently, the pavement cells expand for days and increase in area largely independent of lobe initiation (Zhang et al, 2011;Armour et al, 2015;Wu et al, 2016). In highly lobed pavement cells, anticlinal microtubules often are concentrated at the convex region of the cell (Wasteneys et al, 1997;Zhang et al, 2011), and this microtubule arrangement may reflect the ability of the microtubule network to maintain polarized lobe outgrowth and rearrange in response to local cell geometry and the predicted patterns of cell wall stress (Sampathkumar et al, 2014).…”

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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: Development Of An Image-analysis Pipeline To Test For Correlmentioning

confidence: 99%