Nitric Oxide and Photosynthesis Interplay in Plant Interactions with Pathogens

Abstract

Nitric oxide and reactive nitrogen species are key signalling molecules with pleiotropic effects in plants. They are crucial elements of the redox regulation of plant stress responses to abiotic and biotic stresses. Nitric oxide is known to enhance photosynthetic efficiency under abiotic stress, and reactive nitrogen species-mediated alterations in photosynthetic metabolism have been shown to confer resistance to abiotic stresses. However, knowledge about the role of reactive nitrogen species in plant immune responses remains limited. In this review, we highlight recent advancements in understanding the role of NO in regulating stomatal movement, which contributes to resistance against pathogens. We will examine the involvement of NO in the regulation of photosynthesis, which provides energy, reducing equivalents and carbon skeletons for defence, as well as the significance of protein S-nitrosylation in relation to immune responses. The role of NO synthesis induced in pathogenic organisms during plant-pathogen interactions, along with S-nitrosylation of pathogen effectors to counteract their pathogenesis-promoting activity, is also reported. We will discuss the progress in understanding the interactions between reactive nitrogen species and photosynthetic metabolism, focusing on enhancing crop plants' productivity and resistance in challenging environmental conditions.

Keywords: S-nitrosylation; chloroplasts; immune response; infection; plant–pathogen interaction; reactive nitrogen species; stomata immunity.

Figure 1

Simplified diagram showing the pathways of nitric oxide (NO) synthesis and transformation in plant cells. There are two main pathways for NO production in plants: the oxidative (arginine-dependent) and reductive (nitrite-dependent) pathways, involving different non-enzymatic or enzymatic mechanisms. NO synthesis in plant cells occurs primarily through nitrate reductase (NR)-mediated nitrite reduction. Plasma membrane nitrate reductase (PM-NR) is involved in the reduction of nitrate to nitrite, and then the enzyme nitrite: NO reductase (Ni-NOR/PM-NiNOR) can release NO into the apoplastic space. Reactive nitrogen species/NO interaction with free cysteine sulfhydryl groups leads to S-nitrosylation. On the other hand, peroxynitrite (ONOO⁻) mediates the nitration of tyrosine residues in proteins. Nitration and S-nitrosylation are necessary post-translational protein modifications mediated by NO, which are involved in plant signalling processes, similar to NO, GSNO, and nitro-fatty acids (NO₂-FA). Abbreviations: cETC—chloroplastic electron transport chain; CYS—cysteine; CYS-S-NO—S-nitrosothiols; FA—fatty acid; GSH—glutathione; GSNO—S-nitrosoglutathione; mETC—mitochondrial electron transport chain; NO—nitric oxide; NiNOR—nitrite-NO reductase; NOS—nitric oxide synthase; PM—plasma membrane; PM-NR—plasma membrane nitrate reductase; XOR—xanthine oxidoreductase.

Figure 2

Nitric oxide action on stomata and its target sites in chloroplasts during plant–pathogen interactions. Plant cells overproduce NO upon pathogen/PAMPs sensing. NO from the nitrosative burst mediates stomatal closure to restrict microbial pathogen entry at the sites of infection, which is a part of the plant’s innate immunity response, termed stomatal immunity. Some bacterial pathogens manipulate stomatal aperture to promote pathogenicity. While stomatal closure is crucial for defence, it also restricts the uptake of CO₂, resulting in decreased photosynthesis rates and lower production of assimilates. The reduced availability of sugars limits pathogen proliferation, since pathogens rely on sugars for their growth and infection. In chloroplasts, NO increases chlorophyll content and tightly controls photosynthetic activity. The NO target sites in the photosynthetic electron transport chain include the oxygen-evolving complex, ATP synthase, cyt b₆f complex, PSI, and PSII. NO mediates post-transcriptional regulations of photosynthetic genes, including key enzymes of the Calvin cycle, with Rubisco and Rubisco activase being under dual NO-triggered regulations via S-nitrosylation and tyrosine nitration. NO production promotes the expression of antioxidant enzymes, e.g., APX and SOD, preventing cellular damage and balancing the redox equilibrium. These NO-mediated regulations not only restrict microbial pathogen entry through stomatal closure, but also optimise photosynthesis under biotic stress and modulate the chloroplast-derived stress signalling, shaping the local and systemic responses to pathogens. Abbreviations: APX—ascorbate peroxidase; PAMP—pathogen-associated molecular pattern; PSI—photosystem I; PSII—photosystem II; SOD—superoxide dismutase.

Figure 3

Multiple functions of S-nitrosylation in plants following pathogen infection. In response to infection, upon recognition of the pathogen, reactive nitrogen species, including nitric oxide (NO), are rapidly produced in plant cells, leading to nitrosative burst. The reaction of NO with glutathione (GSH) leads to the production of S-nitrosoglutathione (GSNO), which acts as a mobile reservoir of NO bioactivity. NO may bind covalently to specific reactive cysteine thiols of various proteins to form S-nitrosothiols (SNO), which are stored in the plant cell. Under biotic stress, S-nitrosylation controls the production and detoxification of reactive oxygen species (ROS). S-nitrosylated proteins are involved in regulating metabolism, growth, and developmental processes, as well as programmed cell death, and salicylic acid (SA) and other phytohormone signalling, which are integrated into the plant defence response. Abbreviations: ROS—reactive oxygen species; SA—salicylic acid.

Figure 4

Schematic presentation of nitric oxide (NO) action mechanisms during plant–pathogen interactions. After infection, plants exhibit defensive reactions, classified as local or systemic defence reactions. Plant cells perceive pathogen-expressed PAMPs or effectors (via various receptors) and initiate pattern/effector-triggered immunity (PTI or ETI). After the perception of PAMP or effectors, reactive oxygen and nitrogen species (RONS) production increases, including ROS synthesis by plasma membrane NADPH-oxidase homolog, RBOHD. The reaction of NO with glutathione (GSH) leads to the production of S-nitrosoglutathione (GSNO), controlled by S-nitrosoglutathione reductase (GSNOR). RONS production can lead to a hypersensitive response (HR) at the site of infection. NPR1 protein is considered to be a crucial regulator of salicylic acid-mediated gene expression in systemic acquired resistance (SAR). The complex interactions of NO with other signalling pathways, including reactive oxygen species-mediated redox regulation, hormone signalling (such as stress hormones JA or ET), and post-translational protein modifications, lead to changes in defence gene expression and modulate the local and systemic defence responses. Abbreviations: APX—ascorbate peroxidase; ET—ethylene; ETI—effector-triggered immunity; GSH—glutathione; GSNO—S-nitrosoglutathione; GSNOR—S-nitrosoglutathione reductase; GSSG—glutathione disulfide; H₂O₂—hydrogen peroxide; JA—jasmonic acid; NO—nitric oxide; ONOO⁻—peroxynitrite; NH₃—ammonium; NPR1—nonexpresser of pathogenesis-related genes1, transcription factor; NR—nitrate reductase; PAMPs—pathogen-associated molecular patterns; PrxII—peroxiredoxinII; PTI—pattern-triggered immunity; PTM—post-translational modifications; RBOH—respiratory burst oxidase homolog protein; RONS—reactive oxygen and nitrogen species; SAR—systemic acquired resistance; SOD—superoxide dismutase; TGA—family of basic leucine zipper transcription factors (binding TGACG motif).