Decoding submergence tolerance in Prunus persica: Integrated transcriptomic and metabolomic acclimations of antioxidant system, cell wall dynamics, and hormonal signaling

Abstract Low oxygen stress (hypoxia) induced by submergence significantly impairs respiration in fruit trees, leading to reduced yield and, in extreme cases, tree mortality. While extensive research has focused on the root responses of peach trees to waterlogging, the mechanisms underlying leaf resp...

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Main Authors: Muhammad Ateeq, Dongmei Zhang, Jinping Xiao, Huiqin Zhang, Xingyi Shen, Jian Meng, Jinzhi Yang, Shariq Mahmood Alam, Muhammad Mohsin Kaleem, Muhammad Abbas Khan, Kaijie Zhu, Guohuai Li, Junwei Liu
Format: Article
Language:English
Published: Springer 2025-02-01
Series:Horticulture Advances
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Online Access:https://doi.org/10.1007/s44281-024-00058-z
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author Muhammad Ateeq
Dongmei Zhang
Jinping Xiao
Huiqin Zhang
Xingyi Shen
Jian Meng
Jinzhi Yang
Shariq Mahmood Alam
Muhammad Mohsin Kaleem
Muhammad Abbas Khan
Kaijie Zhu
Guohuai Li
Junwei Liu
author_facet Muhammad Ateeq
Dongmei Zhang
Jinping Xiao
Huiqin Zhang
Xingyi Shen
Jian Meng
Jinzhi Yang
Shariq Mahmood Alam
Muhammad Mohsin Kaleem
Muhammad Abbas Khan
Kaijie Zhu
Guohuai Li
Junwei Liu
author_sort Muhammad Ateeq
collection DOAJ
description Abstract Low oxygen stress (hypoxia) induced by submergence significantly impairs respiration in fruit trees, leading to reduced yield and, in extreme cases, tree mortality. While extensive research has focused on the root responses of peach trees to waterlogging, the mechanisms underlying leaf responses to complete submergence remain poorly understood. In this study, both transcriptomic and metabolic approaches were employed to explore the differential submergence tolerance between two peach cultivars: 'Dongxi Xiaoxian' (DX), which exhibits tolerance, and 'Hujing Milu' (HM), which is sensitive. Compared to HM, DX leaves experienced less decline in leaf verdancy, chlorophyll, and carotenoid content under submergence. DX leaves also showed enhanced antioxidant activities of ROS scavengers and reduced levels of H2O2 and MDA, correlating with improved tolerance. Transcriptomic analysis revealed significant alterations in the expression of genes involved in photosynthesis, glycan biosynthesis, and α-linolenic acid metabolism between the two cultivars. Key metabolites, including sugars (sorbitol and sucrose), amino acids (phenylalanine and L-norvaline), cell wall polysaccharides (lignin and pectin), and plant hormones (jasmonic acid and salicylic acid), were identified as critical for DX's superior submergence tolerance. These findings elucidate the mechanisms of peach leaf tolerance to submergence, providing insights into potential strategies for genetic improvement aimed at enhancing hypoxia resistance in fruit trees.
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spelling doaj-art-b959689d063c481ebb3be954ef7fbb722025-08-20T02:12:58ZengSpringerHorticulture Advances2948-11042025-02-013112110.1007/s44281-024-00058-zDecoding submergence tolerance in Prunus persica: Integrated transcriptomic and metabolomic acclimations of antioxidant system, cell wall dynamics, and hormonal signalingMuhammad Ateeq0Dongmei Zhang1Jinping Xiao2Huiqin Zhang3Xingyi Shen4Jian Meng5Jinzhi Yang6Shariq Mahmood Alam7Muhammad Mohsin Kaleem8Muhammad Abbas Khan9Kaijie Zhu10Guohuai Li11Junwei Liu12National Key Laboratory for Germplasm Innovation and Utilization of Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityNational Key Laboratory for Germplasm Innovation and Utilization of Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityZhejiang Academy of Agricultural Sciences, Yangdu Scientific Research and Innovation BaseZhejiang Academy of Agricultural Sciences, Yangdu Scientific Research and Innovation BaseNational Key Laboratory for Germplasm Innovation and Utilization of Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityNational Key Laboratory for Germplasm Innovation and Utilization of Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityNational Key Laboratory for Germplasm Innovation and Utilization of Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityNational Key Laboratory for Germplasm Innovation and Utilization of Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityNational Key Laboratory for Germplasm Innovation and Utilization of Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityNational Key Laboratory for Germplasm Innovation and Utilization of Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityNational Key Laboratory for Germplasm Innovation and Utilization of Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityNational Key Laboratory for Germplasm Innovation and Utilization of Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityNational Key Laboratory for Germplasm Innovation and Utilization of Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityAbstract Low oxygen stress (hypoxia) induced by submergence significantly impairs respiration in fruit trees, leading to reduced yield and, in extreme cases, tree mortality. While extensive research has focused on the root responses of peach trees to waterlogging, the mechanisms underlying leaf responses to complete submergence remain poorly understood. In this study, both transcriptomic and metabolic approaches were employed to explore the differential submergence tolerance between two peach cultivars: 'Dongxi Xiaoxian' (DX), which exhibits tolerance, and 'Hujing Milu' (HM), which is sensitive. Compared to HM, DX leaves experienced less decline in leaf verdancy, chlorophyll, and carotenoid content under submergence. DX leaves also showed enhanced antioxidant activities of ROS scavengers and reduced levels of H2O2 and MDA, correlating with improved tolerance. Transcriptomic analysis revealed significant alterations in the expression of genes involved in photosynthesis, glycan biosynthesis, and α-linolenic acid metabolism between the two cultivars. Key metabolites, including sugars (sorbitol and sucrose), amino acids (phenylalanine and L-norvaline), cell wall polysaccharides (lignin and pectin), and plant hormones (jasmonic acid and salicylic acid), were identified as critical for DX's superior submergence tolerance. These findings elucidate the mechanisms of peach leaf tolerance to submergence, providing insights into potential strategies for genetic improvement aimed at enhancing hypoxia resistance in fruit trees.https://doi.org/10.1007/s44281-024-00058-zAntioxidant defenseCell wall metabolismPhytohormoneHypoxiaPeach cultivarsPhotosynthesis
spellingShingle Muhammad Ateeq
Dongmei Zhang
Jinping Xiao
Huiqin Zhang
Xingyi Shen
Jian Meng
Jinzhi Yang
Shariq Mahmood Alam
Muhammad Mohsin Kaleem
Muhammad Abbas Khan
Kaijie Zhu
Guohuai Li
Junwei Liu
Decoding submergence tolerance in Prunus persica: Integrated transcriptomic and metabolomic acclimations of antioxidant system, cell wall dynamics, and hormonal signaling
Horticulture Advances
Antioxidant defense
Cell wall metabolism
Phytohormone
Hypoxia
Peach cultivars
Photosynthesis
title Decoding submergence tolerance in Prunus persica: Integrated transcriptomic and metabolomic acclimations of antioxidant system, cell wall dynamics, and hormonal signaling
title_full Decoding submergence tolerance in Prunus persica: Integrated transcriptomic and metabolomic acclimations of antioxidant system, cell wall dynamics, and hormonal signaling
title_fullStr Decoding submergence tolerance in Prunus persica: Integrated transcriptomic and metabolomic acclimations of antioxidant system, cell wall dynamics, and hormonal signaling
title_full_unstemmed Decoding submergence tolerance in Prunus persica: Integrated transcriptomic and metabolomic acclimations of antioxidant system, cell wall dynamics, and hormonal signaling
title_short Decoding submergence tolerance in Prunus persica: Integrated transcriptomic and metabolomic acclimations of antioxidant system, cell wall dynamics, and hormonal signaling
title_sort decoding submergence tolerance in prunus persica integrated transcriptomic and metabolomic acclimations of antioxidant system cell wall dynamics and hormonal signaling
topic Antioxidant defense
Cell wall metabolism
Phytohormone
Hypoxia
Peach cultivars
Photosynthesis
url https://doi.org/10.1007/s44281-024-00058-z
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