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Review
. 2022 Jun 30;11(7):1311.
doi: 10.3390/antiox11071311.

Light Intensity- and Spectrum-Dependent Redox Regulation of Plant Metabolism

Péter Borbély  1 , Anna Gasperl  2 , Tamás Pálmai  1 , Mohamed Ahres  1 , Muhammad Ahsan Asghar  1 , Gábor Galiba  1   3 , Maria Müller  2 , Gábor Kocsy  1
Affiliations
Review

Light Intensity- and Spectrum-Dependent Redox Regulation of Plant Metabolism

Péter Borbély et al. Antioxidants (Basel). .

Abstract

Both light intensity and spectrum (280-800 nm) affect photosynthesis and, consequently, the formation of reactive oxygen species (ROS) during photosynthetic electron transport. ROS, together with antioxidants, determine the redox environment in tissues and cells, which in turn has a major role in the adjustment of metabolism to changes in environmental conditions. This process is very important since there are great spatial (latitude, altitude) and temporal (daily, seasonal) changes in light conditions which are accompanied by fluctuations in temperature, water supply, and biotic stresses. The blue and red spectral regimens are decisive in the regulation of metabolism because of the absorption maximums of chlorophylls and the sensitivity of photoreceptors. Based on recent publications, photoreceptor-controlled transcription factors such as ELONGATED HYPOCOTYL5 (HY5) and changes in the cellular redox environment may have a major role in the coordinated fine-tuning of metabolic processes during changes in light conditions. This review gives an overview of the current knowledge of the light-associated redox control of basic metabolic pathways (carbon, nitrogen, amino acid, sulphur, lipid, and nucleic acid metabolism), secondary metabolism (terpenoids, flavonoids, and alkaloids), and related molecular mechanisms. Light condition-related reprogramming of metabolism is the basis for proper growth and development of plants; therefore, its better understanding can contribute to more efficient crop production in the future.

Keywords: antioxidants; blue light; carbon assimilation; elongated hypocotyl5; far-red light; light intensity; lipid metabolism; nitrogen assimilation; photoreceptors; reactive oxygen species; red light; secondary metabolism; sulphur assimilation.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Effect of light intensity on reactive oxygen species and antioxidants. (a) The presence or absence of light in shoots and roots, respectively, greatly affects reactive oxygen species (ROS) accumulation and antioxidant levels under various environmental conditions. (b) Rapid alterations in light intensity (3–6 h) trigger a systemic ROS response (ROS wave) mediated by H2O2 and respiratory burst oxidase homolog protein D (RBOHD). Long-term response (1–7 days) of ROS homeostasis to low light or high light is also light intensity-dependent, but it is also influenced by the other environmental conditions (temperature, water availability). SOD: superoxide dismutase; CAT: catalase; GR: glutathione reductase; GSH: reduced glutathione; APX: ascorbate peroxidase; PhyB: phytochrome B; PPFD: photosynthetic photon flux density; SA: salicylic acid; ABA: abscisic acid; PQ pool: plastoquinone pool; RH: relative humidity; POD: guaiacol peroxidase; γECS: γ-glutamylcysteine synthase; GST: glutathione-S-transferase; AsA: ascorbic acid.
Figure 2
Figure 2
Influence of light quality on reactive oxygen species and antioxidants. Both blue and red light may act as an enhancer or a repressor of ROS accumulation, which is highly dependent on the origin (temperate or tropical climate) of the plant species, but other factors may also influence their effect on ROS. Generally, under stress conditions, blue light enhances ROS production, while red light diminishes it. ROS might have different roles in the cell death process caused by monochromic blue- or red-light illumination. The low red:far-red ratio (R:FR) exerts a beneficial effect on ROS homeostasis under stress. CRY: cryptochrome; MDA: malondialdehyde; PSII: photosystem II; HY5 elongated hypocotyl 5; SOD: superoxide dismutase; CAT: catalase; GR: glutathione reductase; GSH: reduced glutathione; APX: ascorbate peroxidase; POD: guaiacol peroxidase; γEC: γ-glutamyl-cysteine; GSSG: glutathione disulphide; CySS: cystine; CysGly: cysteinylglycine; GSSG/GSH: glutathione disulphide/glutathione ratio; CySS/Cys: cystine/cysteine ratio; PCD: programmed cell death.
Figure 3
Figure 3
Effects of excess white and far-red light on the subcellular production of reactive oxygen species (ROS), with special emphasis on hydrogen peroxide (H2O2) and its compartment-specific detoxification by antioxidants (ascorbate, AsA; and glutathione, GSH) and enzymes in plants. Line drawing proposing a model of the effects of excess white light (white thunderbolt) and far-red light (dark red thunderbolt) on the subcellular accumulation of H2O2 (and other ROS). Possible signalling pathways are indicated by dotted arrows. APX, ascorbate peroxidase; C, chloroplast; Cat, catalase; M, mitochondria; N, nucleus; P, peroxisome; POD, guaiacol-type peroxidase; V, vacuole.
Figure 4
Figure 4
The effect of light intensity and spectrum on carbohydrate metabolism. Monochromic red or blue lights may inhibit or enhance the enzymes of the Calvin–Benson cycle. Most of these enzymes are HY-5 and/or Trx-regulated. Interestingly, several enzymes of carbohydrate catabolism are light repressed, while others are light enhanced. Light-associated redox regulation of the Calvin–Benson cycle is better known than in the case of tricarboxylic acid (TCA) cycle. Rubisco: ribulose-1,5-bisphosphate carboxylase oxygenase; GAPDH: glyceraldehyde-3-phosphate dehydrogenase; FBP: fructose-1,6-bisphosphatase; Fd: ferredoxin; SBP: sedoheptulose-1,7-bisphosphatase; RPK: ribulose-5-phosphate kinase; Trx: thioredoxin; HY5: elongated hypocotyl 5; HL: high light; GAPC: cytosolic GAPDH; GAPC-SOH: oxidised GAPC; GAPC-SSG: glutathionylated GAPC; Grx: glutaredoxine; PFK: phosphofructokinase; TrxL2: Trx-like2; MDH: malate dehydrogenase; NAD-ME: NAD-dependent malic enzyme; FUM: fumarase; CS: citrate synthase; IDH: isocitrate dehydrogenase; ACO: aconitase; PDC: pyruvate dehydrogenase complex; 2-OGDH: 2-oxoglutarate dehydrogenase; OAA: oxaloacetate; 2OG: 2-oxoglutarate; PhyA: phytochrome A; AcCoA: acetyl-CoA; Fru-6-P: fructose-6-phosphate; Fru-1,6-P2: fructose-1,6-bisphosphate; G3P: glyceraldehyde-3-phosphate; 1,3DPGA: 1,3-diphosphoglycerate.
Figure 5
Figure 5
Light intensity- and spectrum-associated coordination of carbon, nitrate, and sulphate assimilation. The control of the three metabolic pathways is interconnected through the effect of light on the redox system and the HY5 transcription factor. The redox system regulates them through the NAD(P)H/NAD(P)+ and GSH/GSSG redox couples and HY5 through its binding to the promoter of the genes related to these processes. White, blue, red, and dark red arrows indicate the effect of white, blue, red, and far-red light, respectively. Upwards arrows: induction, downwards arrows: repression, horizontal line: no effect. Continuous lines: direct connection, dashed lines: indirect connections with additional intermediates. APR: adenosine phosphosulphate reductase, APX: ascorbate peroxidase, Cop1: constitutive photomorphogenic1, GAPDH: glyceraldehyde phosphate dehydrogenase, GR: glutathione reductase, GST: glutathione S-transferase, NR: nitrate reductase, PDH: pyruvate dehydrogenase, PK: pyruvate kinase, PIF: phytochrome-interacting factor, PSY: phytoene synthase.
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