Melatonin mediates elevated carbon dioxide‐induced photosynthesis and thermotolerance in tomato

Abstract

Increasing carbon dioxide (CO2) promotes photosynthesis and mitigates heat stress‐induced deleterious effects on plants, but the regulatory mechanisms remain largely unknown. Here, we found that tomato (Solanum lycopersicum L.) plants treated with high atmospheric CO2 concentrations (600, 800, and 1000 µmol mol−1) accumulated increased levels of melatonin (N‐acetyl‐5‐methoxy tryptamine) in their leaves and this response is conserved across many plant species, including Arabidopsis, rice, wheat, mustard, cucumber, watermelon, melon, and hot pepper. Elevated CO2 (eCO2; 800 µmol mol−1) caused a 6.8‐fold increase in leaf melatonin content, and eCO2‐induced melatonin biosynthesis preferentially occurred through chloroplast biosynthetic pathways in tomato plants. Crucially, manipulation of endogenous melatonin levels by genetic means affected the eCO2‐induced accumulation of sugar and starch in tomato leaves. Furthermore, net photosynthetic rate, maximum photochemical efficiency of photosystem II, and transcript levels of chloroplast‐ and nuclear‐encoded photosynthetic genes, such as rbcL, rbcS, rbcA, psaD, petB, and atpA, significantly increased in COMT1 overexpressing (COMT1‐OE) tomato plants, but not in melatonin‐deficient comt1 mutants at eCO2 conditions. While eCO2 enhanced plant tolerance to heat stress (42°C) in wild‐type and COMT1‐OE, melatonin deficiency compromised eCO2‐induced thermotolerance in comt1 plants. The expression of heat shock proteins genes increased in COMT1‐OE but not in comt1 plants in response to eCO2 under heat stress. Further analysis revealed that eCO2‐induced thermotolerance was closely linked to the melatonin‐dependent regulation of reactive oxygen species, redox homeostasis, cellular protein protection, and phytohormone metabolism. This study unveiled a crucial mechanism of elevated CO2‐induced thermotolerance in which melatonin acts as an essential endogenous signaling molecule in tomato plants.

Genome-wide identification of the OMT gene family in Cucumis melo L. and expression analysis under abiotic and biotic stress

“…AtOMT3 is defined as AtASMT1, which increases melatonin levels, improves plant salt tolerance, and is closely related to Pst DC3000 resistance ( Shi, Wei & He, 2016 ; Zheng et al, 2017 ). AtOMT6 is an OMT protein on class II OMT protein that shows close homology with CmOMT8 and has been identified as AtCOMT1, which is associated with melatonin synthesis, regulating melatonin synthesis levels, and improving resistance to multiple stresses in plants, such as salt stress and heat stress ( Zheng et al, 2017 ; Hasan et al, 2023 ). In contrast, Chang et al (2021) reported that ClCOMT1 ( ClOMT3 ) is also closely homologous to CmOMT18 and could enhance abiotic stress resistance in Arabidopsis by increasing endogenous melatonin content.…”

Short-Term Evaluation of Woodland Strawberry in Response to Melatonin Treatment under Low Light Environment

“…ROS suppress carbon fixation by reducing the Calvin-Benson cycle enzymes' activity, resulting in reduced photosynthesis [10,11]. Recently, plant growth regulators have been broadly investigated as exogenous chemicals to reduce the damage caused by ROS, and thus promote photosynthesis, such as 5-aminolevulinic acid (ALA) [12,13], spermidine [14], and melatonin [15][16][17].…”

Identification of Hub Genes and Physiological Effects of Overexpressing the Photosynthesis-Related Gene Soly720 in Tomato under High-CO2 Conditions

“…In addition to direct response, there are other pathways through which cross-regulation and -response occur in plants under high-CO 2 conditions. For example, the melatonin content in tomato leaves is increased in a high-CO 2 environment, and endogenous melatonin levels affect the accumulation of sugars and starches [14]. Abscisic acid-deficient mutant plants show lower leaf stomatal conductance in a high-CO 2 environment than in normal conditions [15].…”