Nitric Oxide Signaling and Its Association with Ubiquitin-Mediated Proteasomal Degradation in Plants

Abstract

Nitric oxide (NO) is a versatile signaling molecule with diverse roles in plant biology. The NO-mediated signaling mechanism includes post-translational modifications (PTMs) of target proteins. There exists a close link between NO-mediated PTMs and the proteasomal degradation of proteins via ubiquitylation. In some cases, ubiquitin-mediated proteasomal degradation of target proteins is followed by an NO-mediated post-translational modification on them, while in other cases NO-mediated PTMs can regulate the ubiquitylation of the components of ubiquitin-mediated proteasomal machinery for promoting their activity. Another pathway that links NO signaling with the ubiquitin-mediated degradation of proteins is the N-degron pathway. Overall, these mechanisms reflect an important mechanism of NO signal perception and transduction that reflect a close association of NO signaling with proteasomal degradation via ubiquitylation. Therefore, this review provides insight into those pathways that link NO-PTMs with ubiquitylation.

Keywords: S-nitrosylation; nitric oxide; proteasome; proteolysis; ubiquitylation.

Figure 1

An exemplified model for understanding the N-degron pathway involving ubiquitin proteasomal degradation of ERF-VII (for example, RELATED TO AP2 3, RAP2.3) TF as a part of the NO sensing mechanism in plants. The N-terminal methionine is cleaved by MAPs exposing the second residue, cysteine (Cys). Cysteine gets oxidized by the action of PCOs. In this step, the role of NO is also reported, so possible NO-mediated oxidation of cysteine residue via PTMs still needs to be explored. The oxidized cysteine (Cys*) of the target protein then undergoes arginylation by Arg-tRNA and is catalyzed by ATE1, which helps in its recognition by PRT6 N-recognin for its ubiquitin-mediated proteolysis. MAPs—aminopeptidases; PCOs—plant cysteine oxidases; PTMs—post-translational modifications; ATE1—arginyl-transferases; PRT6—proteolysis 6 E3 ligases. The model structure of RAP2.3 was obtained from UniProt (https://www.uniprot.org/uniprot/P42736#structure accessed on 19 December 2021). The structure of Arg-tRNA^Arg and ATE1 is reprinted (adapted) with permission from [65].

Figure 2

Nitric oxide signaling associated with ubiquitin-mediated proteolysis in plants: (a) represents the N-degron pathway (already described in detail in Figure 1); (b) under certain environmental conditions, NO can trigger ubiquitin-mediated proteasomal degradation of some proteins via S-nitrosylation, for example, APX1 and ABI5; (c) meanwhile, NO can also protect certain proteins by preventing their degradation via S-nitrosylation; (d) NO-mediated PTMs, such as tyrosine nitration, also leads to the proteolytic degradation via ubiquitin-mediated PTMs. Limited evidence is available for these pathways in plants; therefore, the dashed lines and question marks are used which represent further clarification of these signaling pathways in plants. SNO represents S-nitrosothiol; NO₂-Tyr represents tyrosine nitration. The structure of Arg-tRNA^Arg and ATE1 is reprinted (adapted) with permission from [65].