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Cortical microtubules optimize cell-wall crystallinity to drive unidirectional growth in Arabidopsis

Fujita , Miki; Himmelspach, Regina; Hocart, Charles; Williamson, Richard; Mansfield, Shawn; Wasteneys, Geoffrey O

Description

The shape of plants depends on cellulose, a biopolymer that self-assembles into crystalline, inextensible microfibrils (CMFs) upon synthesis at the plasma membrane by multi-enzyme cellulose synthase complexes (CSCs). CSCs are displaced in directions predicted by underlying parallel arrays of cortical microtubules, but CMFs remain transverse in cells that have lost the ability to expand unidirectionally as a result of disrupted microtubules. These conflicting findings suggest that microtubules...[Show more]

dc.contributor.authorFujita , Miki
dc.contributor.authorHimmelspach, Regina
dc.contributor.authorHocart, Charles
dc.contributor.authorWilliamson, Richard
dc.contributor.authorMansfield, Shawn
dc.contributor.authorWasteneys, Geoffrey O
dc.date.accessioned2015-12-10T23:32:25Z
dc.identifier.issn0960-7412
dc.identifier.urihttp://hdl.handle.net/1885/68834
dc.description.abstractThe shape of plants depends on cellulose, a biopolymer that self-assembles into crystalline, inextensible microfibrils (CMFs) upon synthesis at the plasma membrane by multi-enzyme cellulose synthase complexes (CSCs). CSCs are displaced in directions predicted by underlying parallel arrays of cortical microtubules, but CMFs remain transverse in cells that have lost the ability to expand unidirectionally as a result of disrupted microtubules. These conflicting findings suggest that microtubules are important for some physico-chemical property of cellulose that maintains wall integrity. Using X-ray diffraction, we demonstrate that abundant microtubules enable a decrease in the degree of wall crystallinity during rapid growth at high temperatures. Reduced microtubule polymer mass in the mor1-1 mutant at high temperatures is associated with failure of crystallinity to decrease and a loss of unidirectional expansion. Promotion of microtubule bundling by over-expressing the RIC1 microtubule-associated protein reduced the degree of crystallinity. Using live-cell imaging, we detected an increase in the proportion of CSCs that track in microtubule-free domains in mor1-1, and an increase in the CSC velocity. These results suggest that microtubule domains affect glucan chain crystallization during unidirectional cell expansion. Microtubule disruption had no obvious effect on the orientation of CMFs in dark-grown hypocotyl cells. CMFs at the outer face of the hypocotyl epidermal cells had highly variable orientation, in contrast to the transverse CMFs on the radial and inner periclinal walls. This suggests that the outer epidermal mechanical properties are relatively isotropic, and that axial expansion is largely dependent on the inner tissue layers.
dc.publisherBlackwell Publishing Ltd
dc.sourceThe Plant Journal
dc.subjectKeywords: Cell expansion; cell wall; cellulose microfibrils; cellulose synthase complex; Crystallinities; Microtubules; Cell membranes; Cellulose; Chemical properties; Expansion; Mechanical properties; Plants (botany); Tissue; X ray diffraction; Biomechanics; Arabi cell expansion; cell wall; cell-wall crystallinity; cellulose microfibrils; cellulose synthase complex; microtubules
dc.titleCortical microtubules optimize cell-wall crystallinity to drive unidirectional growth in Arabidopsis
dc.typeJournal article
local.description.notesImported from ARIES
local.identifier.citationvolume66
dc.date.issued2011
local.identifier.absfor060705 - Plant Physiology
local.identifier.ariespublicationf2965xPUB1843
local.type.statusPublished Version
local.contributor.affiliationFujita , Miki, University of British Columbia
local.contributor.affiliationHimmelspach, Regina, College of Medicine, Biology and Environment, ANU
local.contributor.affiliationHocart, Charles, College of Medicine, Biology and Environment, ANU
local.contributor.affiliationWilliamson, Richard, College of Medicine, Biology and Environment, ANU
local.contributor.affiliationMansfield, Shawn, University of British Columbia
local.contributor.affiliationWasteneys, Geoffrey O, University of British Columbia
local.description.embargo2037-12-31
local.bibliographicCitation.issue6
local.bibliographicCitation.startpage915
local.bibliographicCitation.lastpage928
local.identifier.doi10.1111/j.1365-313X.2011.04552.x
local.identifier.absseo970106 - Expanding Knowledge in the Biological Sciences
dc.date.updated2016-02-24T08:18:28Z
local.identifier.scopusID2-s2.0-79958231688
local.identifier.thomsonID000292103900001
CollectionsANU Research Publications

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