Peroxisomal polyamine oxidase and NADPH-oxidase cross-talk for ROS homeostasis which affects respiration rate in Arabidopsis thaliana

Abstract

Homeostasis of reactive oxygen species (ROS) in the intracellular compartments is of critical importance as ROS have been linked with nearly all cellular processes and more importantly with diseases and aging. PAs are nitrogenous molecules with an evolutionary conserved role in the regulation of metabolic and energetic status of cells. Recent evidence also suggests that polyamines (PA) are major regulators of ROS homeostasis. In Arabidopsis the backconversion of the PAs spermidine (Spd) and spermine to putrescine and Spd, respectively, is catalyzed by two peroxisomal PA oxidases (AtPAO). However, the physiological role of this pathway remains largely elusive. Here we explore the role of peroxisomal PA backconversion and in particular that catalyzed by the highly expressed AtPAO3 in the regulation of ROS homeostasis and mitochondrial respiratory burst. Exogenous PAs exert an NADPH-oxidase dependent stimulation of oxygen consumption, with Spd exerting the strongest effect. This increase is attenuated by treatment with the NADPH-oxidase blocker diphenyleneiodonium iodide (DPI). Loss-of-function of AtPAO3 gene results to increased NADPH-oxidase-dependent production of superoxide anions (O2•− ), but not H2O2, which activate the mitochondrial alternative oxidase pathway (AOX). On the contrary, overexpression of AtPAO3 results to an increased but balanced production of both H2O2 and O2•− . These results suggest that the ratio of O2•− /H2O2 regulates respiratory chain in mitochondria, with PA-dependent production of O2•− by NADPH-oxidase tilting the balance of electron transfer chain in favor of the AOX pathway. In addition, AtPAO3 seems to be an important component in the regulating module of ROS homeostasis, while a conserved role for PA backconversion and ROS across kingdoms is discussed.

Speculation: Polyamines are important in abiotic stress signaling

“…However, O 2˙-dismutates spontaneously or enzymatically to H 2 O 2 . The ratio of O 2˙-to H 2 O 2 is an important signal in transcription [48], and might be the mediator of polyamines in plant adaptation to unfavorable conditions (Fig. 2).…”

Characterization, expression, and functional analysis of polyamine oxidases and their role in selenium‐induced hydrogen peroxide production in Brassica rapa

“…For example, a type II PAO (AtPAO3)-derived H 2 O 2 acts as an upstream signal to modulate Ca 2+ channels for the regulation of pollen tube growth and respiration rate in A. thaliana. 23,24 Ethylene-induced stomatal closure is dependent on H 2 O 2 generated from two type II PAOs (AtPAO2 and AtPAO4) in Arabidopsis guard cells. 25 Abscisic acid (ABA) induces H 2 O 2 production through a type I PAO in maize.…”

Deregulation of apoplastic polyamine oxidase affects development and salt response of tobacco plants

“…For native electrophoresis and enzyme activity stainings, proteins were electrophoretically resolved using native PAGE and then stained. For SOD activity staining the procedure was carried out according to Andronis et al (2014). SOD enzyme activity was determined by incubating the gel in 50 mM potassium phosphate buffer (pH 7.4) containing 2 mg/mL NBT for 30 min in dark, and then in another 50 mM potassium phosphate buffer (pH 7.4) containing 0.1 mg/mL riboflavin and 0.25 % TEMED for 20 min in dark.…”