Progress in Plant Nitric Oxide Studies: Implications for Phytopathology and Plant Protection

Abstract

Nitric oxide (NO) is a gaseous free radical known to modulate plant metabolism through crosstalk with phytohormones (especially ABA, SA, JA, and ethylene) and other signaling molecules (ROS, H₂S, melatonin), and to regulate gene expression (by influencing DNA methylation and histone acetylation) as well as protein function through post-translational modifications (cysteine S-nitrosation, metal nitrosation, tyrosine nitration, nitroalkylation). Recently, NO has gained attention as a molecule promoting crop resistance to stress conditions. Herein, we review innovations from the NO field and nanotechnology on an up-to-date phytopathological background.

Keywords: nanomaterials; nitric oxide; phytopathogens; plant immunity; stress signaling.

Figure 1

Overview of NO production (black arrows) and conversion (red arrows) pathways in plants. Enzymatic and non-enzymatic reductive pathways using nitrate and nitrite reduction (left): NO is produced by the cytosolic nitrate reductase (NR), nitrite: NO reductase (NiNOR), nitrate reductase-nitric oxide forming nitrite reductase (NR-NOFNiR), xanthine oxidoreductase (XOR), and mitochondrial cytochrome c oxidase (COX). Oxidative pathways of NO synthesis include an NOS-like enzyme using L-Arg as a substrate, undescribed metabolism of hydroxylamine (HA) and polyamines (PAs), and the production of NO from oximes catalyzed by peroxidase (POD). Pathways of NO conversion (right): The reaction of NO with molecular oxygen (O₂) leads to the formation of nitrate (NO₃⁻) and nitrite (NO₂⁻). Phytoglobins (Phytogb) can act as NO dioxygenases and metabolize NO to NO₃⁻. Truncated hemoglobin (THB) modulates NO levels and NR activity. The transfer of the NO⁺ group to the cysteine residue of reduced glutathione (GSH) forms stable S-nitrosoglutathione (GSNO). The interaction of reactive nitrogen species with free sulfhydryl groups of protein Cys results in S-nitrosation. The enzyme S-nitrosoglutathione reductase (GSNOR) breaks down GSNO to form oxidized glutathione (GSSG) and ammonia (NH₃). GSNO can be cleaved by the thioredoxin system consisting of thioredoxin reductase (TRXR) and thioredoxin h5 (TRXh5). Aldo-keto reductases (AKRs) form a new class of enzymes involved in NO homeostasis. During prolonged immune activation, GSNOR is regulated through reactive oxygen species (ROS) oxidation. NO reacts with the superoxide anion radical (O₂⁻) to form peroxynitrite (ONOO⁻), which can cause nitration of tyrosine residues in proteins.

Figure 2

Nitric oxide (NO) is involved in plant interactions with microbes. (A) During pathogenesis, NO is produced by the infected plant as well as by bacteria, oomycetes, and fungi themselves. NO production by phytopathogenic protozoa has not been reported. (B) Pattern-triggered immunity (PTI), based on molecular pattern recognition receptors (PRRs) at the plant cell surface, is co-activated with effector-triggered immunity (ETI) involving nucleotide-binding leucine-rich repeat receptors (NLRs). The mutual potentiation of PTI and ETI leads to effective defense (modified according to https://plantae.org/not-pti-or-eti-pti-and-eti-nature (assessed on 4 February 2025)). NO may induce (arrow) or hinder (stop) signaling pathways, ROS production, or callose deposition differentially if produced early (red) or later (orange) following recognition (for details, see Section 6). HDA, histone deacetylase; MAP(KK)Ks, mitogen-activated protein (kinase kinase) kinases; RBOH, respiratory burst oxidase homolog; RLCK, receptor-like cytoplasmic kinase; ROS, reactive oxygen species; TF, transcription factor.

Figure 2

Nitric oxide (NO) is involved in plant interactions with microbes. (A) During pathogenesis, NO is produced by the infected plant as well as by bacteria, oomycetes, and fungi themselves. NO production by phytopathogenic protozoa has not been reported. (B) Pattern-triggered immunity (PTI), based on molecular pattern recognition receptors (PRRs) at the plant cell surface, is co-activated with effector-triggered immunity (ETI) involving nucleotide-binding leucine-rich repeat receptors (NLRs). The mutual potentiation of PTI and ETI leads to effective defense (modified according to https://plantae.org/not-pti-or-eti-pti-and-eti-nature (assessed on 4 February 2025)). NO may induce (arrow) or hinder (stop) signaling pathways, ROS production, or callose deposition differentially if produced early (red) or later (orange) following recognition (for details, see Section 6). HDA, histone deacetylase; MAP(KK)Ks, mitogen-activated protein (kinase kinase) kinases; RBOH, respiratory burst oxidase homolog; RLCK, receptor-like cytoplasmic kinase; ROS, reactive oxygen species; TF, transcription factor.