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

Abstract

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.

Evolutionary Conservation and Expression Patterns of Neutral/Alkaline Invertases in Solanum

“…Digital expression profiling is a particularly powerful and efficient method for large-scale gene-expression analysis [48][49][50][51][52][53][54][55], and it contributes to understanding gene functions. We therefore analyzed the expression profiles of the CIN gene family at different types of tissue and developmental stages from S. lycopersicum and S. tuberosum on the basis of in silico analysis (Figure 8).…”

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

“…The fraction of apo H 2 O 2 synthesized by plasma membrane‐localized Prxs regulates both the UWL (see Box 2 Fig. 3b) and WI papillae construction (Xia et al ., 2020) as well as the polarized sterol enrichment of the plasma membrane. 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.…”

“…Across both oxidative bursts, the apo H 2 O 2 pool is polarized to the outer periclinal walls of developing ETCs on which the WL is deposited (Fig. 4c; Andriunas et al ., 2012; Xia et al ., 2020).…”

“…Thereafter, activities of the plasma membrane‐located Prxs, along with copper amine oxidases, are redistributed to become enriched around the tips of developing WI papillae (Fig. 4dii; Xia et al ., 2020). The respective mechanism(s) regulating the plasma membrane‐Prx and CAT1 activities is predominately (75%) and solely post‐translational, with the remainder for the Prxs being transcriptional (Xia et al ., 2020).…”

“…4dii; Xia et al ., 2020). The respective mechanism(s) regulating the plasma membrane‐Prx and CAT1 activities is predominately (75%) and solely post‐translational, with the remainder for the Prxs being transcriptional (Xia et al ., 2020). The regulatory elements controlling their activities and subcellular distribution are unknown (Fig.…”