Cell geometry guides the dynamic targeting of apoplastic GPI-linked lipid transfer protein to cell wall elements and cell borders in Arabidopsis thaliana.

Chris Ambrose,Allan Debono,Geoffrey Wasteneys,Miguel A Blazquez

doi:10.1371/journal.pone.0081215

Abstract

During cellular morphogenesis, changes in cell shape and cell junction topology are fundamental to normal tissue and organ development. Here we show that apoplastic Glycophosphatidylinositol (GPI)-anchored Lipid Transfer Protein (LTPG) is excluded from cell junctions and flat wall regions, and passively accumulates around their borders in the epidermal cells of Arabidopsis thaliana. Beginning with intense accumulation beneath highly curved cell junction borders, this enrichment is gradually lost as cells become more bulbous during their differentiation. In fully mature epidermal cells, YFP-LTPG often shows a fibrous cellulose microfibril-like pattern within the bulging outer faces. Physical contact between a flat glass surface and bulbous cell surface induces rapid and reversible evacuation from contact sites and accumulation to the curved wall regions surrounding the contact borders. Thus, LTPG distribution is dynamic, responding to changes in cell shape and wall curvature during cell growth and differentiation. We hypothesize that this geometry-based mechanism guides wax-carrying LTPG to functional sites, where it may act to “seal” the vulnerable border surrounding cell-cell junctions and assist in cell wall fortification and cuticular wax deposition.

Highlights

Epidermal cells demarcate the physical boundary between organism and environment
To observe the cellular distribution of LTPG, we imaged a fusion between citrine yellow fluorescent protein (YFP) and LTPG, driven by the native LTPG promoter in a complemented ltpg-1 mutant background [15], and examined the distribution in multiple cell types using a confocal microscope
In mature cotyledon and leaf epidermal cells, YFP-LTPG often showed a striated distribution pattern on the outer periclinal cell faces, resembling the pattern of cellulose microfibrils found in this cell type [6] (Figure 1A, B)

Summary

Introduction

Epidermal cells demarcate the physical boundary between organism and environment. In aerial plant tissues, the epidermis serves to minimize water loss, restrict pathogen invasion, and facilitate organ growth. Anticlinal walls demarcate the areas of contact between epidermal cells (i.e. junctions), and are crucial components in epidermal functioning. Considering the epidermis as a structural composite akin to a brick wall, anticlinal wall junctions represent the mortar, and are structurally prone to mechanical stresses [1]. For this same reason, anticlinal wall junctions present the easiest route for an invading fungal hypha [2] and often separate and form holes in the leaf epidermises of Arabidopsis mutants with impaired cell adhesion [3]. The leaf epidermal cells of many species have wavy anticlinal walls, which are believed to enhance the structural integrity of the organ. Similar wavy boundaries have been observed in the nacre of seashells, where they assist in dissipating applied load forces over a larger area, thereby reducing the formation and propagation of cracks [4]

Methods

Results

Conclusion