Differential responsiveness of cortical microtubule orientation to suppression of cell expansion among the developmental zones of Arabidopsis thaliana root apex.

Emmanuel Panteris,Polydefkis Hatzopoulos,Ioannis-Dimosthenis S Adamakis,Gerasimos Daras,Stamatis Rigas,Meng-Xiang Sun

doi:10.1371/journal.pone.0082442

Emmanuel Panteris, Polydefkis Hatzopoulos + Show 4 more

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https://doi.org/10.1371/journal.pone.0082442

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Abstract

Τhe bidirectional relationship between cortical microtubule orientation and cell wall structure has been extensively studied in elongating cells. Nevertheless, the possible interplay between microtubules and cell wall elements in meristematic cells still remains elusive. Herein, the impact of cellulose synthesis inhibition and suppressed cell elongation on cortical microtubule orientation was assessed throughout the developmental zones of Arabidopsis thaliana root apex by whole-mount tubulin immunolabeling and confocal microscopy. Apart from the wild-type, thanatos and pom2-4 mutants of Cellulose SynthaseA3 and Cellulose Synthase Interacting1, respectively, were studied. Pharmacological and mechanical approaches inhibiting cell expansion were also applied. Cortical microtubules of untreated wild-type roots were predominantly transverse in the meristematic, transition and elongation root zones. Cellulose-deficient mutants, chemical inhibition of cell expansion, or growth in soil resulted in microtubule reorientation in the elongation zone, wherein cell length was significantly decreased. Combinatorial genetic and chemical suppression of cell expansion extended microtubule reorientation to the transition zone. According to the results, transverse cortical microtubule orientation is established in the meristematic root zone, persisting upon inhibition of cell expansion. Microtubule reorientation in the elongation zone could be attributed to conditional suppression of cell elongation. The differential responsiveness of microtubule orientation to genetic and environmental cues is most likely associated with distinct biophysical traits of the cells among each developmental root zone.

Highlights

The root is a plant organ growing axially due to highly anisotropic cell expansion
Cellulose microfibrils in root cell walls are strictly transverse to the root axis [1], providing the mechanical reinforcement for root morphogenesis
In cells preparing for formative divisions, either periclinal or tangentially anticlinal, cortical microtubules were transverse to the growth axis of each cell but not to the root axis (Figure 1d, arrow)

Summary

Introduction

Root cells originate from the mitotically active meristem and progressively elongate parallel to the root axis. This elongation pattern is imposed by cell wall reinforcement that prevents growth in any other direction. Cortical microtubule organization modulates cell wall pattern in various cell types to support plant morphogenesis [2,3,4,5]. In rapidly growing root cells of the elongation zone, cortical microtubules run parallel to cellulose microfibrils [1]. Live cell imaging experiments in hypocotyl cells provided evidence that cortical microtubules guide the movement of cellulose synthase complexes [8,9,10,11]. Cortical microtubules may influence cell wall properties by regulating cellulose microfibril length [17,18] or crystallinity [19,20,21]

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