Salinity promotes opposite patterns of carbonylation and nitrosylation of C4 phosphoenolpyruvate carboxylase in sorghum leaves

Abstract

Carbonylation inactivates sorghum C PEPCase while nitrosylation has little impact on its activity but holds back carbonylation. This interplay could be important to preserve photosynthetic C PEPCase activity in salinity. Previous work had shown that nitric acid (NO) increased phosphoenolpyruvate carboxylase kinase (PEPCase-k) activity, promoting the phosphorylation of phosphoenolpyruvate carboxylase (PEPCase) in sorghum leaves (Monreal et al. in Planta 238:859-869, 2013b). The present work investigates the effect of NO on C PEPCase in sorghum leaves and its interplay with carbonylation, an oxidative modification frequently observed under salt stress. The PEPCase of sorghum leaves could be carbonylated in vitro and in vivo, and this post-translational modification (PTM) was accompanied by a loss of its activity. Similarly, PEPCase could be S-nitrosylated in vitro and in vivo, and this PTM had little impact on its activity. The S-nitrosylated PEPCase showed increased resistance towards subsequent carbonylation, both in vitro and in vivo. Under salt shock, carbonylation of PEPCase increased in parallel with decreased S-nitrosylation of the enzyme. Subsequent increase of S-nitrosylation was accompanied by decreased carbonylation. Taken together, the results suggest that S-nitrosylation could contribute to maintain C PEPCase activity in stressed sorghum plants. Thus, salt-induced NO synthesis would be protecting photosynthetic PEPCase activity from oxidative inactivation while promoting its phosphorylation, which will guarantee its optimal functioning in suboptimal conditions.

Nitric oxide improves tolerance to arsenic stress in Isatis cappadocica desv. Shoots by enhancing antioxidant defenses

“…Similar results have been obtained in previous studies of different plant species (Singh et al 2009, Hasanuzzaman and Fujita, 2013, Singh et al 2013, Farnese et al 2017. The supply of NO could also protect proteins from carbonylation induced by excess ROS, such it has been reported in citrus and sorghum under salinity (Tanou et al 2012, Baena et al 2017). On the other hand, the reduction in NO concentration by Hb or the NOS inhibitor L-NAME intensifies the accumulation of H2O2 and MDA, indicating that NO plays an important role in regulating ROS accumulation induced by As.…”

Nitric oxide is essential for cadmium‐induced peroxule formation and peroxisome proliferation

“…S ‐nitrosylated CAT is higher under control conditions in NO‐related mutants as compared to WT seedlings, suggesting that CAT is protected from oxidation by S ‐nitrosylation. Similarly, in sorghum leaves, salt stress promotes opposite patterns of carbonylation and S ‐nitrosylation of C4 phosphoenolpyruvate carboxylase (PEPCase; Baena, Feria, Echeverría, Monreal, & García‐Mauriño, 2017); in addition, specific patterns of carbonylation and S ‐nitrosylation under salt stress conditions are essential for citrus plant vigour (Tanou et al, 2014). It has also been suggested that S ‐nitrosylation of antioxidant enzymes prevents irreversible protein carbonylation during recalcitrant seed desiccation tolerance in Antiaris toxicaria (Bai et al, 2011).…”

Multilevel Regulation of Peroxisomal Proteome by Post-Translational Modifications

“…Cross-talk between NO, H 2 S, ABA, and polyamines is involved in acclimation processes in citrus plants (reviewed in [140]). Another example of protection against carbonylation by S -nitrosylation is C4 phosphoenolpyruvate carboxylase in sorgum under salinity stress conditions [141]. Some studies also corroborate the protective role played by S -nitrosylation in mammalian cells under oxidative stress conditions, which prevents protein carbonylation [72,142].…”