Do microtubules orient plant cell wall microfibrils?

Emons, A.M.C.; Derksen, J.; Sassen, M. M. A.

doi:10.1034/j.1399-3054.1992.840325.x

Cited by 37 publications

(50 citation statements)

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“…A role for microtubules in aligning microfibrils is supported by a substantial body of evidence (Baskin, 2001;Burk and Ye, 2002;Gardiner et al, 2003). Nevertheless, some have argued that the parallelism between microtubules and microfibrils represents a correlated response to an unknown polarizing principle rather than a causal relation (Emons et al, 1992). Furthermore, microfibril alignment by microtubules is at odds with some recent results.…”

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confidence: 43%

Disorganization of Cortical Microtubules Stimulates Tangential Expansion and Reduces the Uniformity of Cellulose Microfibril Alignment among Cells in the Root of Arabidopsis

et al. 2004

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To test the role of cortical microtubules in aligning cellulose microfibrils and controlling anisotropic expansion, we exposed Arabidopsis thaliana roots to moderate levels of the microtubule inhibitor, oryzalin. After 2 d of treatment, roots grow at approximately steady state. At that time, the spatial profiles of relative expansion rate in length and diameter were quantified, and roots were cryofixed, freeze-substituted, embedded in plastic, and sectioned. The angular distribution of microtubules as a function of distance from the tip was quantified from antitubulin immunofluorescence images. In alternate sections, the overall amount of alignment among microfibrils and their mean orientation as a function of position was quantified with polarized-light microscopy. The spatial profiles of relative expansion show that the drug affects relative elongation and tangential expansion rates independently. The microtubule distributions averaged to transverse in the growth zone for all treatments, but on oryzalin the distributions became broad, indicating poorly organized arrays. At a subcellular scale, cellulose microfibrils in oryzalin-treated roots were as well aligned as in controls; however, the mean alignment direction, while consistently transverse in the controls, was increasingly variable with oryzalin concentration, meaning that microfibril orientation in one location tended to differ from that of a neighboring location. This conclusion was confirmed by direct observations of microfibrils with field-emission scanning electron microscopy. Taken together, these results suggest that cortical microtubules ensure microfibrils are aligned consistently across the organ, thereby endowing the organ with a uniform mechanical structure.How do plants build organs with specific and heritable shapes? A part of the answer to this question lies in the control of growth. It is not growth rate per se that is crucial for morphogenesis but the directionality of growth. If growth rate were the same in all directions, i.e. isotropic, plant organs would be spherical; organs attain shapes other than spherical because their component cells grow at different rates in different directions, i.e. anisotropically. Understanding how cells control the anisotropy of their expansion is essential for understanding morphogenesis.Expansion anisotropy is characterized by the direction in which the maximal growth rate occurs and by the degree to which the maximum differs from the minimum. The direction of maximal expansion rate is known to be controlled by the direction of net alignment of cellulose microfibrils. Within a growing cell wall, microfibrils are aligned, on average, perpendicularly to the direction of maximal expansion rate, and the aligned cellulose microfibrils confer a mechanical anisotropy on the cell wall, which translates into expansion anisotropy (Green, 1980;Taiz, 1984). The wall can be considered a composite material with strong, rod-shaped particles (microfibrils) embedded in a compliant matrix. Such materials deform perpendic...

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confidence: 43%

Disorganization of Cortical Microtubules Stimulates Tangential Expansion and Reduces the Uniformity of Cellulose Microfibril Alignment among Cells in the Root of Arabidopsis

et al. 2004

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“…The possibility that cellulose may influence the orientation of microtubules was hypothesized by Emons et al (1992). The first evidence for a bidirectional flow of information between microtubules and microfibrils (or CESA) was reported by Fisher and Cyr (1998), who observed that the cortical microtubule arrays of tobacco protoplasts could not acquire parallel order while in the presence of the CESA inhibitor isoxaben, leading the authors to propose a biophysical model for feedback into microtubule orientation.…”

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confidence: 99%

Genetic Evidence That Cellulose Synthase Activity Influences Microtubule Cortical Array Organization

et al. 2008

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To identify factors that influence cytoskeletal organization we screened for Arabidopsis (Arabidopsis thaliana) mutants that show hypersensitivity to the microtubule destabilizing drug oryzalin. We cloned the genes corresponding to two of the 131 mutant lines obtained. The genes encoded mutant alleles of PROCUSTE1 and KORRIGAN, which both encode proteins that have previously been implicated in cellulose synthesis. Analysis of microtubules in the mutants revealed that both mutants have altered orientation of root cortical microtubules. Similarly, isoxaben, an inhibitor of cellulose synthesis, also altered the orientation of cortical microtubules while exogenous cellulose degradation did not. Thus, our results substantiate that proteins involved in cell wall biosynthesis influence cytoskeletal organization and indicate that this influence on cortical microtubule stability and orientation is correlated with cellulose synthesis rather than the integrity of the cell wall.

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“…Alternatively, the coalignment of microtubules and cellulose microfibrils may be determined by cellular geometry (Emons and Mulder, 1998). Disruption in cell growth induced by pharmacological drugs can influence cell morphology, resulting in simultaneous alteration in the orientations of microtubules and cellulose mirofibrils (Emons et al, 1992). Furthermore, Fisher and Cyr (1998) suggested that cellulose biosynthesis is required for microtubule organization and stabilization and the cellulose microfibrils and cortical microtubules become coordinated during cell wall formation .…”

Section: Microtubule Orientation and Cell Expansionmentioning

confidence: 99%

Knockout of the AtCESA2 Gene Affects Microtubule Orientation and Causes Abnormal Cell Expansion in Arabidopsis

Chu¹,

Chen²,

Zhang³

et al. 2006

Plant Physiol.

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Complete cellulose synthesis is required to form functional cell walls and to facilitate proper cell expansion during plant growth. AtCESA2 is a member of the cellulose synthase A family in Arabidopsis (Arabidopsis thaliana) that participates in cell wall formation. By analysis of transgenic seedlings, we demonstrated that AtCESA2 was expressed in all organs, except root hairs. The atcesa2 mutant was devoid of AtCESA2 expression, leading to the stunted growth of hypocotyls in seedlings and greatly reduced seed production in mature plants. These observations were attributed to alterations in cell size as a result of reduced cellulose synthesis in the mutant. The orientation of microtubules was also altered in the atcesa2 mutant, which was clearly observed in hypocotyls and petioles. Complementary expression of AtCESA2 in atcesa2 could rescue the mutant phenotypes. Together, we conclude that disruption of cellulose synthesis results in altered orientation of microtubules and eventually leads to abnormal plant growth. We also demonstrated that the zinc finger-like domain of AtCESA2 could homodimerize, possibly contributing to rosette assemblies of cellulose synthase A within plasma membranes.

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Do microtubules orient plant cell wall microfibrils?

Cited by 37 publications

References 0 publications

Disorganization of Cortical Microtubules Stimulates Tangential Expansion and Reduces the Uniformity of Cellulose Microfibril Alignment among Cells in the Root of Arabidopsis

Disorganization of Cortical Microtubules Stimulates Tangential Expansion and Reduces the Uniformity of Cellulose Microfibril Alignment among Cells in the Root of Arabidopsis

Genetic Evidence That Cellulose Synthase Activity Influences Microtubule Cortical Array Organization

Knockout of the AtCESA2 Gene Affects Microtubule Orientation and Causes Abnormal Cell Expansion in Arabidopsis

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