Nitric oxide triggers a transient metabolic reprogramming in Arabidopsis

Abstract

Nitric oxide (NO) regulates plant growth and development as well as responses to stress that enhanced its endogenous production. Arabidopsis plants exposed to a pulse of exogenous NO gas were used for untargeted global metabolomic analyses thus allowing the identification of metabolic processes affected by NO. At early time points after treatment, NO scavenged superoxide anion and induced the nitration and the S-nitrosylation of proteins. These events preceded an extensive though transient metabolic reprogramming at 6 h after NO treatment, which included enhanced levels of polyamines, lipid catabolism and accumulation of phospholipids, chlorophyll breakdown, protein and nucleic acid turnover and increased content of sugars. Accordingly, lipid-related structures such as root cell membranes and leaf cuticle altered their permeability upon NO treatment. Besides, NO-treated plants displayed degradation of starch granules, which is consistent with the increased sugar content observed in the metabolomic survey. The metabolic profile was restored to baseline levels at 24 h post-treatment, thus pointing up the plasticity of plant metabolism in response to nitroxidative stress conditions.

Nitric Oxide Increases the Physiological and Biochemical Stability of Soybean Plants under High Temperature

“…Regulation of amino-acid levels could participate in signaling and production of other metabolites [53], including polyamines. León et al [54] observed extensive metabolic and transient reprogramming 6 h after treatment with NO in Arabidopsis thaliana (L.) Heynh, including increased polyamines levels that are considered good indicators of NO activation processes, dedicated to remedy oxidative stress and regulate plant growth and development. A second hypothesis may be associated not with decreased synthesis of these amino acids, but with reduction of protein degradation, resulting in lower concentrations of free amino acids.…”

Signal Dynamics and Interactions during Flooding Stress

“…For instance, chemically blocking the hypoxia-induced NO burst at the onset of hypoxia strongly impaired hypoxia survival in maize root tips (Mugnai et al, 2012). In addition to its role in regulating ERFVII abundance, NO also may exert a regulatory role during flooding or hypoxia, by posttranslational modification of proteins via S-or metal-nitrosylation and Tyr nitration (for review, see Astier et al, 2011;León et al, 2016). Exogenous NO application in Arabidopsis effectively S-nitrosylated proteins involved in respiration, metabolism, signaling, and stress responses (Lindermayr et al, 2005;Astier et al, 2011;León et al, 2016).…”

“…In addition to its role in regulating ERFVII abundance, NO also may exert a regulatory role during flooding or hypoxia, by posttranslational modification of proteins via S-or metal-nitrosylation and Tyr nitration (for review, see Astier et al, 2011;León et al, 2016). Exogenous NO application in Arabidopsis effectively S-nitrosylated proteins involved in respiration, metabolism, signaling, and stress responses (Lindermayr et al, 2005;Astier et al, 2011;León et al, 2016). S-Nitrosylated proteins potentially involved in flooding signaling and adaptation include ERFVIIs, cytochrome c oxidase (COX), aconitase, phytoglobins, and the H 2 O 2 scavenger APX1 (Millar and Day, 1996;Perazzolli et al, 2004;Gupta et al, 2012;Gibbs et al, 2014;Begara-Morales et al, 2016).…”

Present knowledge and controversies, deficiencies, and misconceptions on nitric oxide synthesis, sensing, and signaling in plants

“…S‐nitrosylation modifications led to a decrease in cellular glycolysis enzymes, ATP synthase activities, content of acetyl coenzyme A, ATP, ADP‐glucose and UDP‐glucose, which all together eventually inhibited polysaccharide‐biosynthesis and caused monosaccharide accumulation (Zhang et al, ). Accordingly, NO‐treated plants displayed less starch granules and increased sugar content (León, Costa, & Castillo, ). Regarding another primary metabolic pathway, nitrate assimilation seems to be also controlled by NO through negative transcriptional regulation on NR and high affinity nitrate transporter encoding genes in wheat (Adavi & Sathee, ), a process that seems to be dependent on the N compound source (Balotf et al, ).…”