Multilevel Regulation of Peroxisomal Proteome by Post-Translational Modifications

Abstract

Peroxisomes, which are ubiquitous organelles in all eukaryotes, are highly dynamic organelles that are essential for development and stress responses. Plant peroxisomes are involved in major metabolic pathways, such as fatty acid β-oxidation, photorespiration, ureide and polyamine metabolism, in the biosynthesis of jasmonic, indolacetic, and salicylic acid hormones, as well as in signaling molecules such as reactive oxygen and nitrogen species (ROS/RNS). Peroxisomes are involved in the perception of environmental changes, which is a complex process involving the regulation of gene expression and protein functionality by protein post-translational modifications (PTMs). Although there has been a growing interest in individual PTMs in peroxisomes over the last ten years, their role and cross-talk in the whole peroxisomal proteome remain unclear. This review provides up-to-date information on the function and crosstalk of the main peroxisomal PTMs. Analysis of whole peroxisomal proteomes shows that a very large number of peroxisomal proteins are targeted by multiple PTMs, which affect redox balance, photorespiration, the glyoxylate cycle, and lipid metabolism. This multilevel PTM regulation could boost the plasticity of peroxisomes and their capacity to regulate metabolism in response to environmental changes.

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

“…In fact, the activation of yeast peroxine Pex11p depends on redox changes in its cysteins (Knoblach & Rachubinski, 2010; Schrader, Bonekamp, & Islinger, 2012). Other PTMs can not be ruled out however, as PEX11a has been identified as a putative target of phosphorylation in Arabidopsis (Kataya, Muench, & Moorhead, 2019; Sandalio et al, 2019). Further proteomic analysis is required to clarify the PTM dependence of PEX11a on the rapid regulation of peroxule formation and the possible involvement of NO.…”

“…In addition, NO reacts rapidly with reactive oxygen species (ROS) and also regulates ROS production and removal through the protein post‐translational modification of enzymatic sources and antioxidant systems, respectively (Lindermayr & Durner, 2015; Romero‐Puertas & Sandalio, 2016). NO also regulates peroxisomal proteins, antioxidants and ROS‐producing compounds under both normal and stressful conditions caused by heavy metals such as Cd (Gupta & Sandalio, 2012; Ortega‐Galisteo et al, 2012; Sandalio, Gotor, Romero, & Romero‐Puertas, 2019).…”

Hydrogen Sulfide: From a Toxic Molecule to a Key Molecule of Cell Life

“…Furthermore, ethylene biosynthesis is regulated by persulfidation of 1-aminocyclopropane-1-carboxylic acid oxidase (ACO1) in tomato [116]. Recently, a peroxisomal proteome study in Arabidopsis revealed that the interplay of different PTMs such as s-nitrosation, nitration, persulfidation, and acetylation regulates redox signaling to protect proteins against oxidative damage [117]. From an evolutionary point of view, it is reasonable to assume that ancestral purple and green sulfur bacteria lived in an H 2 S-rich atmosphere; and therefore bacteria developed H 2 S-mediated signaling processes to resist oxidative stress.…”

Thioredoxin Network in Plant Mitochondria: Cysteine S-Posttranslational Modifications and Stress Conditions

“…Snitrosylation and therefore, GSNOR, can regulate a large amount of cellular functions and signaling events due to the capacity of alter the activity, stability, conformation, interactions with other molecules or subcellular localization of the S-nitrosated proteins, playing an essential role to protect cells under nitrosative stress (Sevilla et al, 2015a;Romero-Puertas and Sandalio, 2016;Corpas et al, 2019a). Persulfidation H 2 S can exert its function through persulfidation, a PTM affecting the thiol group of cysteine (-SH) in proteins to be modified into a persulfide group (-SSH) (Gotor et al, 2019;Sandalio et al, 2019). H 2 S reacts with either disulfides or sulfenic acids to yield persulfides which are highly reactive to ROS, being oxidized to perthiosulfenic acids (-SSOH), perthiosulfinic (-SSO 2 H), and perthiosulfonic (-SSO 3 H) acids ( Figure 1).…”