Inoculation with Micromonospora sp. enhances carbohydrate and amino acid production, strengthening antioxidant metabolism to mitigate heat stress in wheat cultivars

IntroductionHeat stress caused by global warming adversely affects wheat yield through declining most nutritional quality attributes in grains, excluding grain protein content.MethodsThis research investigated the biochemical, physiological, and antioxidant responses of wheat plants under heat stres...

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Main Authors: Abdelrahim H. A. Hassan, Enas Shaban Ahmed, Mohamed S. Sheteiwy, Yousef Alhaj Hamoud, Mohammad K. Okla, Amal Mohamed AlGarawi, Maria Gabriela Maridueña-Zavala, Ibrahim A. Alaraidh, Ahmed M. Reyad, Hamada Abdelgawad
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-12-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2024.1500894/full
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author Abdelrahim H. A. Hassan
Abdelrahim H. A. Hassan
Enas Shaban Ahmed
Mohamed S. Sheteiwy
Mohamed S. Sheteiwy
Yousef Alhaj Hamoud
Mohammad K. Okla
Amal Mohamed AlGarawi
Maria Gabriela Maridueña-Zavala
Ibrahim A. Alaraidh
Ahmed M. Reyad
Hamada Abdelgawad
author_facet Abdelrahim H. A. Hassan
Abdelrahim H. A. Hassan
Enas Shaban Ahmed
Mohamed S. Sheteiwy
Mohamed S. Sheteiwy
Yousef Alhaj Hamoud
Mohammad K. Okla
Amal Mohamed AlGarawi
Maria Gabriela Maridueña-Zavala
Ibrahim A. Alaraidh
Ahmed M. Reyad
Hamada Abdelgawad
author_sort Abdelrahim H. A. Hassan
collection DOAJ
description IntroductionHeat stress caused by global warming adversely affects wheat yield through declining most nutritional quality attributes in grains, excluding grain protein content.MethodsThis research investigated the biochemical, physiological, and antioxidant responses of wheat plants under heat stress, focusing on the role of plant growth-promoting bacteria (Micromonospora sp.). Two wheat genotypes were studied: one heat-sensitive and one heat-tolerant, examining their responses to heat stress with and without bacterial inoculation.ResultsUnder heat stress, the sensitive cultivar experienced significant reductions in photosynthesis rate, chlorophyll content, and RuBisCO activity (57-61%), while the tolerant cultivar had milder reductions (24-28%). Micromonospora sp. treatment notably improved these parameters in the sensitive cultivar (+48-78%), resulting in a substantial increase in biomass production (+43-53%), which was not seen in the tolerant cultivar. Additionally, oxidative stress markers (H2O2 and MDA) were elevated more in the sensitive cultivar (82% and 90% higher) compared to the tolerant one. Micromonospora sp. treatment effectively reduced these markers in the sensitive cultivar (-28% and -27%). Enhanced activity of antioxidant enzymes and ASC-GSH pathway enzymes was particularly evident in Micromonospora sp.-treated sensitive plants. Carbohydrate metabolism shifted, with increased soluble sugars and significant rises in sucrose content in Micromonospora sp.-treated plants under stress.DiscussionThe higher soluble sugar levels facilitated amino acid synthesis, contributing to biosynthesis of secondary metabolites, including flavonoids, polyphenols, and anthocyanins. This was reflected in increased activity of phenylalanine ammonia-lyase, cinnamate (CA) 4-hydroxylase, and chalcone synthase enzymes, indicating the activation of phenylpropanoid pathways. Overall, the findings suggest that Micromonospora sp. can mitigate heat stress effects by enhancing photosynthetic efficiency, antioxidant defense, and metabolic adaptations in heat-sensitive wheat cultivars.
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spelling doaj-art-58fa6d04bcca4c34ba553ca8698472d12025-08-20T01:58:08ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2024-12-011510.3389/fpls.2024.15008941500894Inoculation with Micromonospora sp. enhances carbohydrate and amino acid production, strengthening antioxidant metabolism to mitigate heat stress in wheat cultivarsAbdelrahim H. A. Hassan0Abdelrahim H. A. Hassan1Enas Shaban Ahmed2Mohamed S. Sheteiwy3Mohamed S. Sheteiwy4Yousef Alhaj Hamoud5Mohammad K. Okla6Amal Mohamed AlGarawi7Maria Gabriela Maridueña-Zavala8Ibrahim A. Alaraidh9Ahmed M. Reyad10Hamada Abdelgawad11School of Biotechnology, Nile University, Giza, EgyptDepartment of Food Safety and Technology, Faculty of Veterinary Medicine, Beni-Suef University, Beni-Suef, EgyptBotany and Microbiology Department, Faculty of Science, Beni-Suef University, Beni-Suef, EgyptDepartment of Integrative Agriculture, College of Agriculture and Veterinary Medicine, United Arab Emirates University, Abu Dhabi, United Arab EmiratesDepartment of Agronomy, Faculty of Agriculture, Mansoura University, Mansoura, EgyptThe National Key Laboratory of Water Disaster Prevention, College of Hydrology and Water Resources, Hohai University, Nanjing, ChinaBotany and Microbiology Department, College of Science, King Saud University, Riyadh, Saudi ArabiaBotany and Microbiology Department, College of Science, King Saud University, Riyadh, Saudi ArabiaCentro de Investigaciones Biotecnológicas del Ecuador (CIBE), Escuela Superior Politécnica del Litoral, ESPOL, Guayaquil, EcuadorBotany and Microbiology Department, College of Science, King Saud University, Riyadh, Saudi ArabiaBotany and Microbiology Department, Faculty of Science, Beni-Suef University, Beni-Suef, EgyptBotany and Microbiology Department, Faculty of Science, Beni-Suef University, Beni-Suef, EgyptIntroductionHeat stress caused by global warming adversely affects wheat yield through declining most nutritional quality attributes in grains, excluding grain protein content.MethodsThis research investigated the biochemical, physiological, and antioxidant responses of wheat plants under heat stress, focusing on the role of plant growth-promoting bacteria (Micromonospora sp.). Two wheat genotypes were studied: one heat-sensitive and one heat-tolerant, examining their responses to heat stress with and without bacterial inoculation.ResultsUnder heat stress, the sensitive cultivar experienced significant reductions in photosynthesis rate, chlorophyll content, and RuBisCO activity (57-61%), while the tolerant cultivar had milder reductions (24-28%). Micromonospora sp. treatment notably improved these parameters in the sensitive cultivar (+48-78%), resulting in a substantial increase in biomass production (+43-53%), which was not seen in the tolerant cultivar. Additionally, oxidative stress markers (H2O2 and MDA) were elevated more in the sensitive cultivar (82% and 90% higher) compared to the tolerant one. Micromonospora sp. treatment effectively reduced these markers in the sensitive cultivar (-28% and -27%). Enhanced activity of antioxidant enzymes and ASC-GSH pathway enzymes was particularly evident in Micromonospora sp.-treated sensitive plants. Carbohydrate metabolism shifted, with increased soluble sugars and significant rises in sucrose content in Micromonospora sp.-treated plants under stress.DiscussionThe higher soluble sugar levels facilitated amino acid synthesis, contributing to biosynthesis of secondary metabolites, including flavonoids, polyphenols, and anthocyanins. This was reflected in increased activity of phenylalanine ammonia-lyase, cinnamate (CA) 4-hydroxylase, and chalcone synthase enzymes, indicating the activation of phenylpropanoid pathways. Overall, the findings suggest that Micromonospora sp. can mitigate heat stress effects by enhancing photosynthetic efficiency, antioxidant defense, and metabolic adaptations in heat-sensitive wheat cultivars.https://www.frontiersin.org/articles/10.3389/fpls.2024.1500894/fullwheat cultivarsheat stresssugarsanthocyanin metabolismphenylpropanoid pathwaysASC/GSH cycle 2
spellingShingle Abdelrahim H. A. Hassan
Abdelrahim H. A. Hassan
Enas Shaban Ahmed
Mohamed S. Sheteiwy
Mohamed S. Sheteiwy
Yousef Alhaj Hamoud
Mohammad K. Okla
Amal Mohamed AlGarawi
Maria Gabriela Maridueña-Zavala
Ibrahim A. Alaraidh
Ahmed M. Reyad
Hamada Abdelgawad
Inoculation with Micromonospora sp. enhances carbohydrate and amino acid production, strengthening antioxidant metabolism to mitigate heat stress in wheat cultivars
Frontiers in Plant Science
wheat cultivars
heat stress
sugars
anthocyanin metabolism
phenylpropanoid pathways
ASC/GSH cycle 2
title Inoculation with Micromonospora sp. enhances carbohydrate and amino acid production, strengthening antioxidant metabolism to mitigate heat stress in wheat cultivars
title_full Inoculation with Micromonospora sp. enhances carbohydrate and amino acid production, strengthening antioxidant metabolism to mitigate heat stress in wheat cultivars
title_fullStr Inoculation with Micromonospora sp. enhances carbohydrate and amino acid production, strengthening antioxidant metabolism to mitigate heat stress in wheat cultivars
title_full_unstemmed Inoculation with Micromonospora sp. enhances carbohydrate and amino acid production, strengthening antioxidant metabolism to mitigate heat stress in wheat cultivars
title_short Inoculation with Micromonospora sp. enhances carbohydrate and amino acid production, strengthening antioxidant metabolism to mitigate heat stress in wheat cultivars
title_sort inoculation with micromonospora sp enhances carbohydrate and amino acid production strengthening antioxidant metabolism to mitigate heat stress in wheat cultivars
topic wheat cultivars
heat stress
sugars
anthocyanin metabolism
phenylpropanoid pathways
ASC/GSH cycle 2
url https://www.frontiersin.org/articles/10.3389/fpls.2024.1500894/full
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