Glucose and ethylene signalling pathways converge to regulate trans‐differentiation of epidermal transfer cells in Vicia narbonensis cotyledons

Abstract

SUMMARYTransfer cells are specialized transport cells containing invaginated wall ingrowths that provide an amplified plasma membrane surface area with high densities of transporter proteins. They trans-differentiate from differentiated cells at sites where enhanced rates of nutrient transport occur across apo/symplasmic boundaries. Despite their physiological importance, the signal(s) and signalling cascades responsible for initiating their trans-differentiation are poorly understood. In culture, adaxial epidermal cells of Vicia narbonensis cotyledons were induced to trans-differentiate to a transfer cell morphology. Manipulating their intracellular glucose concentrations by transgenic knock-down of ADP-glucose pyrophosphorylase expression and/or culture on a high-glucose medium demonstrated that glucose functioned as a negative regulator of wall ingrowth induction. In contrast, glucose had no detectable effect on wall ingrowth morphology. The effect on wall ingrowth induction of culture on media containing glucose analogues suggested that glucose acts through a hexokinase-dependent signalling pathway. Elevation of an epidermal cell-specific ethylene signal alone, or in combination with glucose analogues, countered the negative effect of glucose on wall ingrowth induction. Glucose modulated the amplitude of ethylene-stimulated wall ingrowth induction by downregulating the expression of ethylene biosynthetic genes and an ethylene insensitive 3 (EIN3)-like gene (EIL) encoding a key transcription factor in the ethylene signalling cascade. A model is presented describing the interaction between glucose and ethylene signalling pathways regulating the induction of wall ingrowth formation in adaxial epidermal cells.

New Insights into Roles of Cell Wall Invertase in Early Seed Development Revealed by Comprehensive Spatial and Temporal Expression Patterns of GhCWIN1 in Cotton

“…5 and 6) suggest a negative role of CWIN in TC differentiation. Consistent with this view is a recent report showing that Glc functions as a negative signal for TC WI induction in faba bean cotyledons (Andriunas et al, 2011). The high expression of GhCWIN1 in TCP at 1 to 5 DAA likely generates high amounts of Glc, which could help to hold these cells in an undifferentiated state.…”

Intersection of transfer cells with phloem biology—broad evolutionary trends, function, and induction

“…The capacity to peel the induced adaxial epidermis from cotyledons provides large quantities of material for cell-specific gene expression profiling at specified stages of ingrowth wall formation (e.g., Dibley et al, 2009). Exposure of sister cotyledons to pharmacological blockades (Figure 3) offers an experimental opportunity to investigate regulation of trans -differentiation events through the inductive signaling sequence (Zhou et al, 2010; Andriunas et al, 2011, 2012; Xia et al, 2012). Statistically robust quantification of ingrowth wall formation responses to pharmacological treatments can be derived from scoring large populations of synchronously trans -differentiating adaxial epidermal cells for presence of wall ingrowths in epidermal peels prepared by a dry-cleave method to visualize cytoplasmic faces of their outer periclinal walls by SEM/FESEM (Talbot et al, 2001).…”

“…The review commences by identifying key apoplasmic steps in the phloem transport pathway as a prelude to addressing questions about broad evolutionary trends in relation to TC occurrence, their spatial relationships with other phloem cell types, their functional significance in the phloem transport pathways and whether signaling cascades known to initiate trans -differentiation to a TC morphology in developing seeds (Dibley et al, 2009; Zhou et al, 2010; Andriunas et al, 2011, 2012) may be involved in induction of cells within the phloem to a TC morphology.…”

Extracellular hydrogen peroxide, produced through a respiratory burst oxidase/superoxide dismutase pathway, directs ingrowth wall formation in epidermal transfer cells of Vicia faba cotyledons

“…Glucose, sensed through HXK, acts as a gatekeeper of the ethylene signal by repressing ethylene biosynthesis and signaling. 9 Coincident with the ethylene burst, intracellular glucose levels decline 6 to a critical threshold at which repression on EIN3 abundance is released, promoting its accumulation in the presence of ethylene ( Fig. Two and see ref.…”

“…7 The auxin spike induces an ethylene signal transduced through the Ethylene Insensitive 3 (EIN3) pathway 8 antagonistically modulated by a converging hexokinase (HXK) pathway elicited by intracellular glucose. 9 The regulatory influence of ethylene on ingrowth wall assembly is mediated, in part, through a burst in extracellular hydrogen peroxide (H 2 O 2 ) production. The H 2 O 2 signal activates cell wall biosynthesis and provides a positional cue directing polarized deposition of the uniform wall, the attenuation of which comprises WI formation.…”