Ethylene and hydrogen peroxide regulate formation of a sterol-enriched domain essential for wall labyrinth assembly in transfer cells

Zhang, Huiming; Devine, Luke B; Xia, Xue; Offler, Christina E.; Patrick, John W.

doi:10.1093/jxb/erz003

Cited by 5 publications

(13 citation statements)

References 57 publications

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“…In the case of UWL formation (Fig. 7), our previous studies suggested that the PM-located apo H 2 O 2 signal acted by inducing a microtubule/actin-independent polarized vesicle docking system, embedded in sterol-enriched domains, located along the entire outer periclinal region of the ETC PM (Zhang et al , 2019). In contrast, the concurrent VfrbohB/PAO/Prx original wall-generated apo H 2 O 2 signal, residing in the cell wall matrix, played no role in UWL construction.…”

Section: Discussionmentioning

confidence: 90%

“…This was shown to be guided by an extensive transmembrane polymeric platform formed by Casparian Strip domain proteins (CASPS) (Lee et al , 2013). In contrast, for trans -differentiating ETCs, apo H 2 O 2 would appear to direct spatial organization of lipid-enriched domains in the outer periclinal region of the PM (Zhang et al , 2019).…”

Section: Discussionmentioning

confidence: 99%

“…S8; Figs 6E, F, 7B). The array of potential PM-localized apo H 2 O 2 targets accounting for assembly of WI papillae included the directed incorporation of sterols that form lipid-enriched microenvironments in which clusters of Ca 2+ -permeable channels are assembled (Zhang et al , 2019). In combination with ethylene, the apo H 2 O 2 signal activated Ca 2+ -permeable channels to form plumes of elevated [Ca 2+ ] cyt (Zhang et al, 2015 a , b ).…”

Section: Discussionmentioning

confidence: 99%

“…In combination with ethylene, the apo H 2 O 2 signal activated Ca 2+ -permeable channels to form plumes of elevated [Ca 2+ ] cyt (Zhang et al, 2015 a , b ). These plumes in turn mediated remodelling of the actin network to direct a polarized delivery of vesicles carrying wall building materials to sterol-enriched docking loci at which WI papillae were constructed (Zhang et al ., 2017 a , b ; 2019).…”

Section: Discussionmentioning

confidence: 99%

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Enzymes contributing to the hydrogen peroxide signal dynamics that regulate wall labyrinth formation in transfer cells

Xia

Zhang

Offler

et al. 2019

Journal of Experimental Botany

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Transfer cells are characterized by an amplified plasma membrane area supported on a wall labyrinth composed of a uniform wall layer (UWL) from which wall ingrowth (WI) papillae arise. Adaxial epidermal cells of developing Vicia faba cotyledons, when placed in culture, undergo a rapid (hours) trans-differentiation to a functional epidermal transfer cell (ETC) phenotype. The trans-differentiation event is controlled by a signalling cascade comprising auxin, ethylene, apoplasmic reactive oxygen species (apoROS), and cytosolic Ca2+. Apoplasmic hydrogen peroxide (apoH2O2) was confirmed as the apoROS regulating UWL and WI papillae formation. Informed by an ETC-specific transcriptome, a pharmacological approach identified a temporally changing cohort of H2O2 biosynthetic enzymes. The cohort contained a respiratory burst oxidase homologue, polyamine oxidase, copper amine oxidase, and a suite of class III peroxidases. Collectively these generated two consecutive bursts in apoH2O2 production. Spatial organization of biosynthetic/catabolic enzymes was deduced from responses to pharmacologically blocking their activities on the cellular and subcellular distribution of apoH2O2. The findings were consistent with catalase activity constraining the apoH2O2 signal to the outer periclinal wall of the ETCs. Strategic positioning of class III peroxidases in this outer domain shaped subcellular apoH2O2 signatures that differed during assembly of the UWL and WI papillae.

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Section: Discussionmentioning

confidence: 90%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Enzymes contributing to the hydrogen peroxide signal dynamics that regulate wall labyrinth formation in transfer cells

Xia

Zhang

Offler

et al. 2019

Journal of Experimental Botany

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“…The latter is mediated by apo H 2 O 2 upregulating a cytoskeleton‐independent mechanism of docking/fusion of vesicles carrying cargoes of phytosterols while blocking their endocytosis in the outer periclinal region of the ETC plasma membrane (Fig. 4c; Zhang et al ., 2019). In line with these roles, catalytic activities of plasma membrane‐localized Prxs are evenly spread across the plasma membrane lining the outer periclinal wall during UWL formation.…”

Section: Unmasking Master Regulators and Signals Directing Wall Labyrmentioning

confidence: 99%

Transfer cells: what regulates the development of their intricate wall labyrinths?

Offler

Patrick

2020

New Phytologist

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Transfer cells (TCs) support high nutrient rates into, or at symplasmic discontinuities within, the plant body. Their transport capacity is conferred by an amplified plasma membrane surface area, enriched in nutrient transporters, supported on an intricately invaginated wall labyrinth (WL). Thus, development of the WL is at the heart of TC function. Enquiry has shifted from describing WL architecture and formation to discovering mechanisms regulating WL assembly. Experimental systems used to examine these phenomena are critiqued. Considerable progress has been made in identifying master regulators that commit stem cells to a TC fate (e.g. the maize Myeloblastosis (MYB)-related R1-type transcription factor) and signals that induce differentiated cells to undergo trans-differentiation to a TC phenotype (e.g. sugar, auxin and ethylene). In addition, signals that provide positional information for assembly of the WL include apoplasmic hydrogen peroxide and cytosolic Ca 2+ plumes. The former switches on, and specifies the intracellular site for WL construction, while the latter creates subdomains to direct assembly of WL invaginations. Less is known about macromolecule species and their spatial organization essential for WL assembly. Emerging evidence points to a dependency on methyl-esterified homogalacturonan accumulation, unique patterns of cellulose and callose deposition and spatial positioning of arabinogalactan proteins.

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Effect of biofertilizers and rhizospheric bacteria on growth and root ultrastucture of lettuce

Montesdeoca-Flores,

Alfayate-Casañas,

Hernández-Bolaños

et al. 2023

Hortic. Environ. Biotechnol.

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Biofertilization is a technique that uses plant and animal wastes to add organic matter and nutrients to the soil. It can also use microorganisms that can metabolize these by-products to facilitate their absorption by the plant roots. In this study, we tested the effects of rhizospheric bacteria inoculation (T1), a combination of rhizospheric bacteria with liquid fertilizer (T2) and uncombined liquid fertilizer (T3), on the growth, nutritional content, root tissue, and root cells of lettuce plants. The results showed significant positive differences in all treatments compared to control plants, in terms of morphological, nutritional, and productivity parameters. The combination of rhizospheric bacteria with liquid SEFEL fertilizer (T2) yielded the best results, showing increased fresh and dry weight, and diameter. There were no differences between treatments for nutritional content, but each treatment outperformed the control by more than 700% for all macronutrients. The best result was phosphorus content for T1, with 1272.22% more than control. Regarding root structure and ultrastructure, there was no variation in tissue organization compared to control plants, but increases in root hairs (T1), development of transfer cells (T2), and secondary growth (T3) were observed. Additionally, colonization of roots by rhizospheric bacteria was confirmed in all three treatments. In conclusion, this study suggests that inoculating with rhizospheric bacteria is a viable and environmentally friendly biofertilization for lettuce plants.

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Ethylene and hydrogen peroxide regulate formation of a sterol-enriched domain essential for wall labyrinth assembly in transfer cells

Abstract: Ethylene and extracellular hydrogen peroxide co-regulate formation of a sterol-enriched plasma membrane domain in trans-differentiating epidermal transfer cells that functions to co-ordinate construction of their wall labyrinth.

Cited by 5 publications

References 57 publications

Enzymes contributing to the hydrogen peroxide signal dynamics that regulate wall labyrinth formation in transfer cells

Enzymes contributing to the hydrogen peroxide signal dynamics that regulate wall labyrinth formation in transfer cells

Transfer cells: what regulates the development of their intricate wall labyrinths?

Effect of biofertilizers and rhizospheric bacteria on growth and root ultrastucture of lettuce

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