Melatonin mediates elevated carbon dioxide-induced photosynthesis and thermotolerance in tomato.

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.

Functions of Redox Signaling in Pollen Development and Stress Response.

Cellular redox homeostasis is crucial for normal plant growth and development. Each developmental stage of plants has a specific redox mode and is maintained by various environmental cues, oxidants, and antioxidants. Reactive oxygen species (ROS) and reactive nitrogen species are the chief oxidants in plant cells and participate in cell signal transduction and redox balance. The production and removal of oxidants are in a dynamic balance, which is necessary for plant growth. Especially during reproductive development, pollen development depends on ROS-mediated tapetal programmed cell death to provide nutrients and other essential substances. The deviation of the redox state in any period will lead to microspore abortion and pollen sterility. Meanwhile, pollens are highly sensitive to environmental stress, in particular to cell oxidative burst due to its peculiar structure and function. In this regard, plants have evolved a series of complex mechanisms to deal with redox imbalance and oxidative stress damage. This review summarizes the functions of the main redox components in different stages of pollen development, and highlights various redox protection mechanisms of pollen in response to environmental stimuli. In continuation, we also discuss the potential applications of plant growth regulators and antioxidants for improving pollen vigor and fertility in sustaining better agriculture practices.

HsfA1a confers pollen thermotolerance through upregulating antioxidant capacity, protein repair, and degradation in Solanum lycopersicum L.

The heat shock transcription factors (Hsfs) play critical roles in plant responses to abiotic stresses. However, the mechanism of Hsfs in the regulation of pollen thermotolerance and their specific biological functions and signaling remain unclear. Herein, we demonstrate that HsfA1a played a key role in tomato pollen thermotolerance. Pollen thermotolerance was reduced in hsfA1a mutants but was increased by hsfA1a overexpression, based on pollen viability and germination. Analyzing the whole transcriptome by RNA-seq data, we found that HsfA1a mainly regulated the genes involved in oxidative stress protection, protein homeostasis regulation and protein modification, as well as the response to biological stress in anthers under heat stress. The accumulation of reactive oxygen species in anthers was enhanced in hsfA1a mutants but decreased in HsfA1a-overexpressing lines. Furthermore, HsfA1a bound to the promoter region of genes involved in redox regulation (Cu/Zn-SOD, GST8, and MDAR1), protein repair (HSP17.6A, HSP70-2, HSP90-2, and HSP101) and degradation (UBP5, UBP18, RPN10a, and ATG10) and regulated the expression of these genes in tomato anthers under heat stress. Our findings suggest that HsfA1a maintains pollen thermotolerance and cellular homeostasis by enhancing antioxidant capacity and protein repair and degradation, ultimately improving pollen viability and fertility.