Calcium-dependent depletion zones in the cortical microtubule array coincide with sites of, but do not regulate, wall ingrowth papillae deposition in epidermal transfer cells.

Hui-Ming Zhang,Christina E Offler,Mark J Talbot,John W Patrick,David W Mccurdy

doi:10.1093/jxb/erv317

Abstract

Trans-differentiation to a transfer-cell morphology is characterized by the localized deposition of wall ingrowth papillae that protrude into the cytosol. Whether the cortical microtubule array directs wall ingrowth papillae formation was investigated using a Vicia faba cotyledon culture system in which their adaxial epidermal cells were spontaneously induced to trans-differentiate to transfer cells. During deposition of wall ingrowth papillae, the aligned cortical microtubule arrays in precursor epidermal cells were reorganized into a randomized array characterized by circular depletion zones. Concurrence of the temporal appearance, spatial pattern, and size of depletion zones and wall ingrowth papillae was consistent with each papilla occupying a depletion zone. Surprisingly, microtubules appeared not to regulate construction of wall ingrowth papillae, as neither depolymerization nor stabilization of cortical microtubules changed their deposition pattern or morphology. Moreover, the size and spatial pattern of depletion zones was unaltered when the formation of wall ingrowth papillae was blocked by inhibiting cellulose biosynthesis. In contrast, the depletion zones were absent when the cytosolic calcium plumes, responsible for directing wall ingrowth papillae formation, were blocked or dissipated. Thus, we conclude that the depletion zones within the cortical microtubule array result from localized depolymerization of microtubules initiated by elevated cytosolic Ca(2+) levels at loci where wall ingrowth papillae are deposited. The physiological significance of the depletion zones as a mechanism to accommodate the construction of wall ingrowth papillae without compromising maintenance of the plasma membrane-microtubule inter-relationship is discussed.

Highlights

As part of their differentiation, numerous plant cell types trans-differentiate from many cell types, conferring on them deposit specialized cell walls that relate to their final func- an enhanced capacity for membrane exchange of nutrients. tion
‘Organized’ arrays are composed of parallel thick cortical microtubule (CMT) bundles characteristic of those found in expanding plant cells (Fig. 2A; see Deinum and Mulder, 2013)
These depletion zones were surrounded by a possible combination of fine fragmented CMTs and tubulin monomers sometimes appearing like a collar (Fig. 2C)

Summary

Introduction

As part of their differentiation, numerous plant cell types trans-differentiate from many cell types, conferring on them deposit specialized cell walls that relate to their final func- an enhanced capacity for membrane exchange of nutrients. tion. Depending on the species and cell type, the papillae branch and fuse, resulting in a fenestrated layer of wall material and, by repeating this sequence of wall deposition, form a multi-layered wall labyrinth (Talbot et al, 2001). Such a multi-layered ingrowth wall labyrinth, polarized to their outer periclinal wall, characterizes the abaxial epidermal transfer cells of Vicia faba cotyledons. This study reports the use of this cotyledon culture system to investigate whether microtubule organization plays a role in directing the construction of wall ingrowth papillae during transfer-cell trans-differentiation

Methods

Results

Conclusion