Modulation of Protein S-Nitrosylation by Isoprene Emission in Poplar

Abstract

ORCID IDs: 0000-0002-3422-4083 (J.M.-P.); 0000-0001-8410-5624 (J.B.); 0000-0002-9825-867X (J.-P.S.).Researchers have been examining the biological function(s) of isoprene in isoprene-emitting (IE) species for two decades. There is overwhelming evidence that leaf-internal isoprene increases the thermotolerance of plants and protects them against oxidative stress, thus mitigating a wide range of abiotic stresses. However, the mechanisms of abiotic stress mitigation by isoprene are still under debate. Here, we assessed the impact of isoprene on the emission of nitric oxide (NO) and the S-nitroso-proteome of IE and non-isoprene-emitting (NE) gray poplar (Populus 3 canescens) after acute ozone fumigation. The short-term oxidative stress induced a rapid and strong emission of NO in NE compared with IE genotypes. Whereas IE and NE plants exhibited under nonstressful conditions only slight differences in their S-nitrosylation pattern, the in vivo S-nitroso-proteome of the NE genotype was more susceptible to ozone-induced changes compared with the IE plants. The results suggest that the nitrosative pressure (NO burst) is higher in NE plants, underlining the proposed molecular dialogue between isoprene and the free radical NO. Proteins belonging to the photosynthetic light and dark reactions, the tricarboxylic acid cycle, protein metabolism, and redox regulation exhibited increased S-nitrosylation in NE samples compared with IE plants upon oxidative stress. Because the posttranslational modification of proteins via S-nitrosylation often impacts enzymatic activities, our data suggest that isoprene indirectly regulates the production of reactive oxygen species (ROS) via the control of the S-nitrosylation level of ROS-metabolizing enzymes, thus modulating the extent and velocity at which the ROS and NO signaling molecules are generated within a plant cell.It has been demonstrated that isoprene protects plants against a plethora of abiotic stresses (Singsaas et al., 1997;Behnke et al., 2007;Velikova et al., 2008;Vickers et al., 2009b). Since the discovery of the positive influence of isoprene emission on plants' photosynthetic processes in the early 1990s (Sharkey and Singsaas, 1995), many efforts have been made to explain the primary mechanism of isoprene functioning. Most attention was given to the hypothesis that isoprene improves the thermotolerance of the photosynthetic machinery by stabilizing chloroplast (thylakoid) membranes during short, high-temperature episodes (Sharkey and Singsaas, 1995;Loreto and Schnitzler, 2010). Successive studies underlined that isoprene helps maintain high rates of chloroplastic electron transport and CO 2 assimilation during heat stress and accelerates recovery from stress (Singsaas and Sharkey, 2000;Velikova et al., 2006;Behnke et al., 2010b;Way et al., 2011).One mechanistic explanation is that isoprene molecules are dissolved in thylakoid membrane and prevent membrane lipid denaturation following oxidative stress (Sharkey and Yeh, 2001). It was suggested that isoprene acts directly to st...

Root isoprene formation alters lateral root development

“…The PPDB (The Plant Proteome Database) was used to allocate in MapMan BIN categories (Thimm et al, 2004;Usadel et al, 2009). The differences in the proteome of IE and NE genotypes were analysed using Orthogonal Partial Least Square regression (OPLS) statistical methods as previously described in details (Vanzo et al, 2016;Velikova et al, 2014). The results were validated by "full cross-validation" (Eriksson et al, 2006) and in Arabidopsis (Figure 1; Figure S2).…”

Isoprene research – 60 years later, the biology is still enigmatic

“…In that case, the non-emitting poplars were slightly more sensitive to abiotic stress. These genetic tools are being used with microarray technology (Behnke et al 2010;Harvey & Sharkey 2016), proteomics (Vanzo et al 2016), metabolomics (Way et al 2013) and metabolic flux analyses (Ghirardo et al 2014). The suppression of isoprene emission through genetic alteration causes changes in gene expression, especially some transcription factors associated with abiotic stress resistance, changes gene expression related to anthocyanin production and changes nitrosylation state of some proteins.…”

Physiological significance of isoprenoids and phenylpropanoids in drought response of Arundinoideae species with contrasting habitats and metabolism

“…; Vanzo et al . ), thereby indirectly providing a general antioxidant action (for review, see Vickers et al . ; Loreto & Schnitzler ).…”

“…Secondary metabolites (volatile and nonvolatile) are often efficient scavengers of excessive reducing power under stressful conditions (Agati et al 2012;Harrison et al 2013;Esteban et al 2015). It has been suggested that, among volatile isoprenoids, isoprene regulates both reactive oxygen and nitrogen species formation (Behnke et al 2010a(Behnke et al , 2010bVelikova et al 2012;Vanzo et al 2016), thereby indirectly providing a general antioxidant action (for review, see Vickers et al 2009;Loreto & Schnitzler 2010). It is also shown that isoprene stabilizes thylakoid membrane structure and its function is closely associated with structural organization and functioning of plastidial membranes (Velikova et al 2011Pollastri et al 2014).…”