Melatonin Ameliorates Thermotolerance in Soybean Seedling through Balancing Redox Homeostasis and Modulating Antioxidant Defense, Phytohormones and Polyamines Biosynthesis

Global warming is impacting the growth and development of economically important but sensitive crops, such as soybean (Glycine max L.). Using pleiotropic signaling molecules, melatonin can relieve the negative effects of high temperature by enhancing plant growth and development as well as modulatin...

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Main Authors: Muhammad Imran, Muhammad Aaqil Khan, Raheem Shahzad, Saqib Bilal, Murtaza Khan, Byung-Wook Yun, Abdul Latif Khan, In-Jung Lee
Format: Article
Language:English
Published: MDPI AG 2021-08-01
Series:Molecules
Subjects:
Online Access:https://www.mdpi.com/1420-3049/26/17/5116
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author Muhammad Imran
Muhammad Aaqil Khan
Raheem Shahzad
Saqib Bilal
Murtaza Khan
Byung-Wook Yun
Abdul Latif Khan
In-Jung Lee
author_facet Muhammad Imran
Muhammad Aaqil Khan
Raheem Shahzad
Saqib Bilal
Murtaza Khan
Byung-Wook Yun
Abdul Latif Khan
In-Jung Lee
author_sort Muhammad Imran
collection DOAJ
description Global warming is impacting the growth and development of economically important but sensitive crops, such as soybean (Glycine max L.). Using pleiotropic signaling molecules, melatonin can relieve the negative effects of high temperature by enhancing plant growth and development as well as modulating the defense system against abiotic stresses. However, less is known about how melatonin regulates the phytohormones and polyamines during heat stress. Our results showed that high temperature significantly increased ROS and decreased photosynthesis efficiency in soybean plants. Conversely, pretreatment with melatonin increased plant growth and photosynthetic pigments (chl a and chl b) and reduced oxidative stress via scavenging hydrogen peroxide and superoxide and reducing the MDA and electrolyte leakage contents. The inherent stress defense responses were further strengthened by the enhanced activities of antioxidants and upregulation of the expression of ascorbate–glutathione cycle genes. Melatonin mitigates heat stress by increasing several biochemicals (phenolics, flavonoids, and proline), as well as the endogenous melatonin and polyamines (spermine, spermidine, and putrescine). Furthermore, the positive effects of melatonin treatment also correlated with a reduced abscisic acid content, down-regulation of the gmNCED3, and up-regulation of catabolic genes (CYP707A1 and CYP707A2) during heat stress. Contrarily, an increase in salicylic acid and up-regulated expression of the defense-related gene PAL2 were revealed. In addition, melatonin induced the expression of heat shock protein 90 (gmHsp90) and heat shock transcription factor (gmHsfA2), suggesting promotion of ROS detoxification via the hydrogen peroxide-mediated signaling pathway. In conclusion, exogenous melatonin improves the thermotolerance of soybean plants and enhances plant growth and development by activating antioxidant defense mechanisms, interacting with plant hormones, and reprogramming the biochemical metabolism.
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spelling doaj.art-9e924f8618554851a4b5a8801849e7f02023-11-22T10:59:18ZengMDPI AGMolecules1420-30492021-08-012617511610.3390/molecules26175116Melatonin Ameliorates Thermotolerance in Soybean Seedling through Balancing Redox Homeostasis and Modulating Antioxidant Defense, Phytohormones and Polyamines BiosynthesisMuhammad Imran0Muhammad Aaqil Khan1Raheem Shahzad2Saqib Bilal3Murtaza Khan4Byung-Wook Yun5Abdul Latif Khan6In-Jung Lee7School of Applied Biosciences, Kyungpook National University, Daegu 41566, KoreaSchool of Applied Biosciences, Kyungpook National University, Daegu 41566, KoreaDepartment of Horticulture, University of Haripur, Haripur 22620, PakistanNatural and Medical Sciences Research Center, University of Nizwa, Nizwa 616, OmanSchool of Applied Biosciences, Kyungpook National University, Daegu 41566, KoreaSchool of Applied Biosciences, Kyungpook National University, Daegu 41566, KoreaDepartment of Engineering Technology, College of Technology, University of Houston, TX 77479, USASchool of Applied Biosciences, Kyungpook National University, Daegu 41566, KoreaGlobal warming is impacting the growth and development of economically important but sensitive crops, such as soybean (Glycine max L.). Using pleiotropic signaling molecules, melatonin can relieve the negative effects of high temperature by enhancing plant growth and development as well as modulating the defense system against abiotic stresses. However, less is known about how melatonin regulates the phytohormones and polyamines during heat stress. Our results showed that high temperature significantly increased ROS and decreased photosynthesis efficiency in soybean plants. Conversely, pretreatment with melatonin increased plant growth and photosynthetic pigments (chl a and chl b) and reduced oxidative stress via scavenging hydrogen peroxide and superoxide and reducing the MDA and electrolyte leakage contents. The inherent stress defense responses were further strengthened by the enhanced activities of antioxidants and upregulation of the expression of ascorbate–glutathione cycle genes. Melatonin mitigates heat stress by increasing several biochemicals (phenolics, flavonoids, and proline), as well as the endogenous melatonin and polyamines (spermine, spermidine, and putrescine). Furthermore, the positive effects of melatonin treatment also correlated with a reduced abscisic acid content, down-regulation of the gmNCED3, and up-regulation of catabolic genes (CYP707A1 and CYP707A2) during heat stress. Contrarily, an increase in salicylic acid and up-regulated expression of the defense-related gene PAL2 were revealed. In addition, melatonin induced the expression of heat shock protein 90 (gmHsp90) and heat shock transcription factor (gmHsfA2), suggesting promotion of ROS detoxification via the hydrogen peroxide-mediated signaling pathway. In conclusion, exogenous melatonin improves the thermotolerance of soybean plants and enhances plant growth and development by activating antioxidant defense mechanisms, interacting with plant hormones, and reprogramming the biochemical metabolism.https://www.mdpi.com/1420-3049/26/17/5116melatoninpolyamineantioxidantabscisic acidsalicylic acidsoybean
spellingShingle Muhammad Imran
Muhammad Aaqil Khan
Raheem Shahzad
Saqib Bilal
Murtaza Khan
Byung-Wook Yun
Abdul Latif Khan
In-Jung Lee
Melatonin Ameliorates Thermotolerance in Soybean Seedling through Balancing Redox Homeostasis and Modulating Antioxidant Defense, Phytohormones and Polyamines Biosynthesis
Molecules
melatonin
polyamine
antioxidant
abscisic acid
salicylic acid
soybean
title Melatonin Ameliorates Thermotolerance in Soybean Seedling through Balancing Redox Homeostasis and Modulating Antioxidant Defense, Phytohormones and Polyamines Biosynthesis
title_full Melatonin Ameliorates Thermotolerance in Soybean Seedling through Balancing Redox Homeostasis and Modulating Antioxidant Defense, Phytohormones and Polyamines Biosynthesis
title_fullStr Melatonin Ameliorates Thermotolerance in Soybean Seedling through Balancing Redox Homeostasis and Modulating Antioxidant Defense, Phytohormones and Polyamines Biosynthesis
title_full_unstemmed Melatonin Ameliorates Thermotolerance in Soybean Seedling through Balancing Redox Homeostasis and Modulating Antioxidant Defense, Phytohormones and Polyamines Biosynthesis
title_short Melatonin Ameliorates Thermotolerance in Soybean Seedling through Balancing Redox Homeostasis and Modulating Antioxidant Defense, Phytohormones and Polyamines Biosynthesis
title_sort melatonin ameliorates thermotolerance in soybean seedling through balancing redox homeostasis and modulating antioxidant defense phytohormones and polyamines biosynthesis
topic melatonin
polyamine
antioxidant
abscisic acid
salicylic acid
soybean
url https://www.mdpi.com/1420-3049/26/17/5116
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