Nitric oxide-mediated modulation of photorespiratory enzymes and photochemical components in leaves of pea plants (Pisum sativum)

Abstract

The photorespiratory metabolism safeguards photosynthesis against abiotic and biotic stress. Nitric oxide (NO) and reactive oxygen species (ROS) levels rise in plants during abiotic stress. Low concentrations of NO or ROS are beneficial as signalling molecules, but they can be toxic to plant cells at high concentrations. ROS are known to modulate photorespiration; however, it is unclear whether NO affects photorespiratory enzymes and photochemical components simultaneously. We therefore used sodium nitroprusside (SNP) under dark, moderate light (ML), or high light (HL) conditions to simultaneously investigate its impact on photorespiratory enzymes and photochemical components. The NO levels were increased upon SNP exposure in Pisum sativum leaves, particularly under HL conditions. The NO release in leaves was confirmed when the NO scavenger cPTIO (2-(4-Carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide potassium salt) was present, since it decreased the majority of elevated NO. The nitrosative/oxidative stress in Pisum sativum leaves was confirmed by the increase in nitrosothiols and tyrosine-nitrated proteins, as well as reduced aconitase activity after SNP exposure at HL. The protein levels, mRNA levels, and the enzyme activities of the following four photorespiratory enzymes: glycolate oxidase (GO), hydroxypyruvate reductase (HPR), glycerate kinase (GK), and phosphoglycolate phosphatase (PGLP) were markedly increased under elevated NO conditions. Catalase (CAT), ascorbate peroxidase (APX), and superoxide dismutase (SOD) also showed increased activity, elevated protein and transcript levels upon exposure to SNP. Parallel studies on chlorophyll a fluorescence confirmed that NO restricted electron transport at both PSII and PSI, inhibited photosynthesis and respiration, and damaged photosynthetic pigments. We concluded from this study that NO at high concentrations upregulated photorespiratory enzymes while inhibiting photochemical components such as photosystem II and I (PSII/PSI) simultaneously.