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

Abstract

Nutrient partitioning within plants is primarily regulated at sites of intense apo-/symplasmic nutrient exchange such as loading/ unloading of vascular systems and loading of developing seeds.1 Space constraints at these sites necessitate high nutrient fluxes per transport cell thus creating potential "transport bottlenecks" by substrate saturation of their membrane transporters. A striking solution to this problem has been the evolution of a cell design where plasma membrane surface areas are substantially amplified (up to 20x) by constructing intricately-invaginated ingrowth walls that form scaffolds to support amplified plasma membrane areas 2 and hence accommodate high transport rates (e.g., see refs. 3, 4). These specialized cells, called transfer cells (TCs), are formed by trans-differentiating from a range of differentiated cell types. Their ingrowth walls are polarized to the direction of the intricate, and often polarized, ingrowth walls of transfer cells (tCs) amplify their plasma membrane surface areas to confer a transport function of supporting high rates of nutrient exchange across apo-/symplasmic interfaces. the tC ingrowth wall comprises a uniform wall layer on which wall ingrowths are deposited. Signals and signal cascades inducing trans-differentiation events leading to formation of tC ingrowth walls are poorly understood. Vicia faba cotyledons offer a robust experimental model to examine tC induction as, when placed into culture, their adaxial epidermal cells rapidly (h) and synchronously form polarized ingrowth walls accessible for experimental observations. using this model, we recently reported findings consistent with extracellular hydrogen peroxide, produced through a respiratory burst oxidase homolog/superoxide dismutase pathway, initiating cell wall biosynthetic activity and providing directional information guiding deposition of the polarized uniform wall. our conclusions rested on observations derived from pharmacological manipulations of hydrogen peroxide production and correlative gene expression data sets. a series of additional studies were undertaken, the results of which verify that extracellular hydrogen peroxide contributes to regulating ingrowth wall formation and is generated by a respiratory burst oxidase homolog/superoxide dismutase pathway. Keywords: cell wall peroxidase, hydrogen peroxide, respiratory burst oxidase, trans-differentiation, transfer cell, cell wall, Vicia faba Abbreviations: BHA, butylated hydroxyanisole; DAB, 3',3'-diaminobenzidine; DDC, diethyldithiocarbamate; DPI, diphenyleneiodonium; EIN3, Ethylene Insensitive 3; ERFs, Ethylene Response Factors,; HXK, hexokinase; ROS, reactive oxygen species; rboh, respiratory burst oxidase homologue; SEM, scanning electron microscopy; SOD, superoxide dismutase; TC, transfer cell; TEM, transmission electron microscopy nutrient transport and comprise a uniform wall on which wall ingrowths (WIs) are deposited. 2 Despite the key physiological significance of TCs in nutrient transport and plant productivity, the regulatory...

Differential transcriptional networks associated with key phases of ingrowth wall construction in trans-differentiating epidermal transfer cells of Vicia faba cotyledons

“…Extracellular ROS, produced by ethylene-induced respiratory burst oxidases (rbohs), regulate biosynthesis and polarized deposition of the uniform wall in epidermal TCs [ 6 , 32 ]. Similarly, rboh expression co-occurs with wall ingrowth formation in barley BETCs [ 8 ].…”

“…Interestingly, ROS-related gene expression was dominated by those involved in extra- and intracellular ROS homeostasis (Additional file 11 ) suggesting that ingrowth wall formation depends upon a spatio/temporal fine-tuning of ROS. For instance, antioxidant capacity could be down regulated by ascorbic acid oxidation catalyzed by an extracellular L-ascorbate oxidase ([ 33 ]; Additional file 11 ) whilst concurrent ROS degradation by peroxidation [ 32 ] could be mediated by carboxymethylenebutenolidase-like protein (Additional file 11 ), secreted to the cell wall [ 34 ]. In contrast to epidermal TCs, differentially expressed peroxidases were not detected in barley BETCs [ 8 ] and were strongly down-regulated in nematode giant TCs [ 10 ].…”

High-resolution confocal imaging of wall ingrowth deposition in plant transfer cells: Semi-quantitative analysis of phloem parenchyma transfer cell development in leaf minor veins of Arabidopsis

“…These observations suggest that early stages of reticulate ingrowth deposition can be highly localized to discrete regions within an individual PP TC, and then continued deposition causes consolidation of these patches into more continuous regions of ingrowth deposition. The signals directing such localized patches of ingrowth deposition are unknown, but in non-vascular TC types the reactive oxygen species hydrogen peroxide has been implicated as a polarizing signal directing wall ingrowth deposition [ 5 , 30 , 31 ]. Recently, localized plumes of Ca 2+ have been implicated in directing the highly localized deposition of individual papillae wall ingrowths in epidermal TCs of V. faba cotyledons [ 32 ].…”

Plasticity in sunflower leaf and cell growth under high salinity

“…Recently, Xia et al . () demonstrated that extracellular hydrogen peroxide directs ingrowth wall formation in epidermal transfer cells of Vicia faba cotyledons. Salt stress has been shown to reduce production of reactive oxygen species (ROS) in maize leaves (Rodríguez et al .…”