Uncovering molecular mechanisms of soybean response to 12C6+ heavy ion irradiation through integrated transcriptomic and metabolomic profiling

Ion beam mutagenesis is an advanced technique capable of inducing substantial changes in plants, resulting in noticeable alterations in their growth. However, the precise molecular mechanisms underlying the effects of radiation on soybeans remain unclear. This study investigates the impact of ionizi...

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Main Authors: Honglei Ren, Bixian Zhang, Chunlei Zhang, Xiulin Liu, Xueyang Wang, Fengyi Zhang, Kezhen Zhao, Rongqiang Yuan, Ahmed M. Abdelghany, Sobhi F. Lamlom
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Ecotoxicology and Environmental Safety
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Online Access:http://www.sciencedirect.com/science/article/pii/S0147651325000259
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author Honglei Ren
Bixian Zhang
Chunlei Zhang
Xiulin Liu
Xueyang Wang
Fengyi Zhang
Kezhen Zhao
Rongqiang Yuan
Ahmed M. Abdelghany
Sobhi F. Lamlom
author_facet Honglei Ren
Bixian Zhang
Chunlei Zhang
Xiulin Liu
Xueyang Wang
Fengyi Zhang
Kezhen Zhao
Rongqiang Yuan
Ahmed M. Abdelghany
Sobhi F. Lamlom
author_sort Honglei Ren
collection DOAJ
description Ion beam mutagenesis is an advanced technique capable of inducing substantial changes in plants, resulting in noticeable alterations in their growth. However, the precise molecular mechanisms underlying the effects of radiation on soybeans remain unclear. This study investigates the impact of ionizing radiation on soybean development through a comprehensive approach that integrates transcriptomics and metabolomics. A total of 1500 rounds of disease-free soybean seeds underwent irradiation with 270 MeV/u 12C6+ ion beams, administered at doses of 0, 120, and 150 Gy. Our results revealed that key growth-related parameters, including plant height, branch number, number of pods per plant, and number of seeds per plant, were closely monitored and exhibited significant declines with increasing radiation doses. Transcriptomic analysis identified a multitude of differentially expressed genes (DEGs), with 6013, 3588, and 340 genes significantly altered in high vs. control, low vs. control, and high vs. low-dose irradiation comparisons, respectively, while metabolomic profiling unveiled 445, 445, and 218 differentially expressed metabolites (DEMs) in analogous comparisons. This comprehensive analysis ultimately pinpointed 123 key metabolites influenced by radiation stress. Putting together transcriptomic and metabolomic data showed strong connections between genes and metabolites, which had a big effect on pathways like pyruvate metabolism, ABC transporters, and glutathione metabolism. This underscores the comprehensive reprogramming of soybean metabolism to address irradiation-induced challenges. Specifically, we observed significant up-regulation of 24 DEGs, notable down-regulation of 8 DEMs, and significant activation of 15 metabolic pathways, all of which contributed to the observed phenotypic changes. These findings elucidate soybeans' complex molecular reactions to ionizing radiation, helping us understand how radiation-induced genetic and metabolic alterations affect plant growth.
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spelling doaj-art-bfb78e7d68d64a5fb5aed41e03500a692025-01-23T05:26:07ZengElsevierEcotoxicology and Environmental Safety0147-65132025-01-01289117689Uncovering molecular mechanisms of soybean response to 12C6+ heavy ion irradiation through integrated transcriptomic and metabolomic profilingHonglei Ren0Bixian Zhang1Chunlei Zhang2Xiulin Liu3Xueyang Wang4Fengyi Zhang5Kezhen Zhao6Rongqiang Yuan7Ahmed M. Abdelghany8Sobhi F. Lamlom9Soybean Research Institute of Heilongjiang Academy of Agriculture Sciences, Harbin 150086, ChinaSoybean Research Institute of Heilongjiang Academy of Agriculture Sciences, Harbin 150086, China; Corresponding author.Soybean Research Institute of Heilongjiang Academy of Agriculture Sciences, Harbin 150086, ChinaSoybean Research Institute of Heilongjiang Academy of Agriculture Sciences, Harbin 150086, ChinaSoybean Research Institute of Heilongjiang Academy of Agriculture Sciences, Harbin 150086, ChinaSoybean Research Institute of Heilongjiang Academy of Agriculture Sciences, Harbin 150086, ChinaSoybean Research Institute of Heilongjiang Academy of Agriculture Sciences, Harbin 150086, ChinaSoybean Research Institute of Heilongjiang Academy of Agriculture Sciences, Harbin 150086, ChinaCrop Science Department, Faculty of Agriculture, Damanhour University, Damanhour 22516, EgyptPlant Production Department, Faculty of Agriculture Saba Basha, Alexandria University, Alexandria 21531, Egypt; Work Station of Science and Technique for Post-doctoral in Sugar Beet Institute Afliated to Heilongjiang University, 74 Xuefu Road, Harbin 150000, Heilongjiang, ChinaIon beam mutagenesis is an advanced technique capable of inducing substantial changes in plants, resulting in noticeable alterations in their growth. However, the precise molecular mechanisms underlying the effects of radiation on soybeans remain unclear. This study investigates the impact of ionizing radiation on soybean development through a comprehensive approach that integrates transcriptomics and metabolomics. A total of 1500 rounds of disease-free soybean seeds underwent irradiation with 270 MeV/u 12C6+ ion beams, administered at doses of 0, 120, and 150 Gy. Our results revealed that key growth-related parameters, including plant height, branch number, number of pods per plant, and number of seeds per plant, were closely monitored and exhibited significant declines with increasing radiation doses. Transcriptomic analysis identified a multitude of differentially expressed genes (DEGs), with 6013, 3588, and 340 genes significantly altered in high vs. control, low vs. control, and high vs. low-dose irradiation comparisons, respectively, while metabolomic profiling unveiled 445, 445, and 218 differentially expressed metabolites (DEMs) in analogous comparisons. This comprehensive analysis ultimately pinpointed 123 key metabolites influenced by radiation stress. Putting together transcriptomic and metabolomic data showed strong connections between genes and metabolites, which had a big effect on pathways like pyruvate metabolism, ABC transporters, and glutathione metabolism. This underscores the comprehensive reprogramming of soybean metabolism to address irradiation-induced challenges. Specifically, we observed significant up-regulation of 24 DEGs, notable down-regulation of 8 DEMs, and significant activation of 15 metabolic pathways, all of which contributed to the observed phenotypic changes. These findings elucidate soybeans' complex molecular reactions to ionizing radiation, helping us understand how radiation-induced genetic and metabolic alterations affect plant growth.http://www.sciencedirect.com/science/article/pii/S0147651325000259SoybeanIonizing radiationGrowthTranscriptomicsMetabolomicsRadiation stress
spellingShingle Honglei Ren
Bixian Zhang
Chunlei Zhang
Xiulin Liu
Xueyang Wang
Fengyi Zhang
Kezhen Zhao
Rongqiang Yuan
Ahmed M. Abdelghany
Sobhi F. Lamlom
Uncovering molecular mechanisms of soybean response to 12C6+ heavy ion irradiation through integrated transcriptomic and metabolomic profiling
Ecotoxicology and Environmental Safety
Soybean
Ionizing radiation
Growth
Transcriptomics
Metabolomics
Radiation stress
title Uncovering molecular mechanisms of soybean response to 12C6+ heavy ion irradiation through integrated transcriptomic and metabolomic profiling
title_full Uncovering molecular mechanisms of soybean response to 12C6+ heavy ion irradiation through integrated transcriptomic and metabolomic profiling
title_fullStr Uncovering molecular mechanisms of soybean response to 12C6+ heavy ion irradiation through integrated transcriptomic and metabolomic profiling
title_full_unstemmed Uncovering molecular mechanisms of soybean response to 12C6+ heavy ion irradiation through integrated transcriptomic and metabolomic profiling
title_short Uncovering molecular mechanisms of soybean response to 12C6+ heavy ion irradiation through integrated transcriptomic and metabolomic profiling
title_sort uncovering molecular mechanisms of soybean response to 12c6 heavy ion irradiation through integrated transcriptomic and metabolomic profiling
topic Soybean
Ionizing radiation
Growth
Transcriptomics
Metabolomics
Radiation stress
url http://www.sciencedirect.com/science/article/pii/S0147651325000259
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