Quality traits drive the enrichment of Massilia in the rhizosphere to improve soybean oil content

Abstract Background Soybean seeds are rich in protein and oil. The selection of varieties that produce high-quality seeds has been one of the priorities of soybean breeding programs. However, the influence of improved seed quality on the rhizosphere microbiota and whether the microbiota is involved...

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Main Authors: Qin Han, Guanghui Zhu, Hongmei Qiu, Mingbo Li, Jiaming Zhang, Xinying Wu, Renhao Xiao, Yan Zhang, Wei Yang, Bing Tian, Lanxi Xu, Jiayang Zhou, Yutong Li, Yueqiang Wang, Yang Bai, Xia Li
Format: Article
Language:English
Published: BMC 2024-10-01
Series:Microbiome
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Online Access:https://doi.org/10.1186/s40168-024-01933-7
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author Qin Han
Guanghui Zhu
Hongmei Qiu
Mingbo Li
Jiaming Zhang
Xinying Wu
Renhao Xiao
Yan Zhang
Wei Yang
Bing Tian
Lanxi Xu
Jiayang Zhou
Yutong Li
Yueqiang Wang
Yang Bai
Xia Li
author_facet Qin Han
Guanghui Zhu
Hongmei Qiu
Mingbo Li
Jiaming Zhang
Xinying Wu
Renhao Xiao
Yan Zhang
Wei Yang
Bing Tian
Lanxi Xu
Jiayang Zhou
Yutong Li
Yueqiang Wang
Yang Bai
Xia Li
author_sort Qin Han
collection DOAJ
description Abstract Background Soybean seeds are rich in protein and oil. The selection of varieties that produce high-quality seeds has been one of the priorities of soybean breeding programs. However, the influence of improved seed quality on the rhizosphere microbiota and whether the microbiota is involved in determining seed quality are still unclear. Here, we analyzed the structures of the rhizospheric bacterial communities of 100 soybean varieties, including 53 landraces and 47 modern cultivars, and evaluated the interactions between seed quality traits and rhizospheric bacteria. Results We found that rhizospheric bacterial structures differed between landraces and cultivars and that this difference was directly related to their oil content. Seven bacterial families (Sphingomonadaceae, Gemmatimonadaceae, Nocardioidaceae, Xanthobacteraceae, Chitinophagaceae, Oxalobacteraceae, and Streptomycetaceae) were obviously enriched in the rhizospheres of the high-oil cultivars. Among them, Oxalobacteraceae (Massilia) was assembled specifically by the root exudates of high-oil cultivars and was associated with the phenolic acids and flavonoids in plant phenylpropanoid biosynthetic pathways. Furthermore, we showed that Massilia affected auxin signaling or interfered with active oxygen-related metabolism. In addition, Massilia activated glycolysis pathway, thereby promoting seed oil accumulation. Conclusions These results provide a solid theoretical basis for the breeding of revolutionary soybean cultivars with desired seed quality and optimal microbiomes and the development of new cultivation strategies for increasing the oil content of seeds. Video Abstract
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institution Kabale University
issn 2049-2618
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publishDate 2024-10-01
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series Microbiome
spelling doaj-art-5fe827ddf9dd4a7eb3a8f60f98e6cadd2024-12-01T12:36:43ZengBMCMicrobiome2049-26182024-10-0112111510.1186/s40168-024-01933-7Quality traits drive the enrichment of Massilia in the rhizosphere to improve soybean oil contentQin Han0Guanghui Zhu1Hongmei Qiu2Mingbo Li3Jiaming Zhang4Xinying Wu5Renhao Xiao6Yan Zhang7Wei Yang8Bing Tian9Lanxi Xu10Jiayang Zhou11Yutong Li12Yueqiang Wang13Yang Bai14Xia Li15National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, College of Plant Science and Technology, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, College of Plant Science and Technology, Huazhong Agricultural UniversityJilin Academy of Agricultural Sciences / National Engineering Research Center for SoybeanNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, College of Plant Science and Technology, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, College of Plant Science and Technology, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, College of Plant Science and Technology, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, College of Plant Science and Technology, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, College of Plant Science and Technology, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, College of Plant Science and Technology, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, College of Plant Science and Technology, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, College of Plant Science and Technology, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, College of Plant Science and Technology, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, College of Plant Science and Technology, Huazhong Agricultural UniversityJilin Academy of Agricultural Sciences / National Engineering Research Center for SoybeanState Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of SciencesNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, College of Plant Science and Technology, Huazhong Agricultural UniversityAbstract Background Soybean seeds are rich in protein and oil. The selection of varieties that produce high-quality seeds has been one of the priorities of soybean breeding programs. However, the influence of improved seed quality on the rhizosphere microbiota and whether the microbiota is involved in determining seed quality are still unclear. Here, we analyzed the structures of the rhizospheric bacterial communities of 100 soybean varieties, including 53 landraces and 47 modern cultivars, and evaluated the interactions between seed quality traits and rhizospheric bacteria. Results We found that rhizospheric bacterial structures differed between landraces and cultivars and that this difference was directly related to their oil content. Seven bacterial families (Sphingomonadaceae, Gemmatimonadaceae, Nocardioidaceae, Xanthobacteraceae, Chitinophagaceae, Oxalobacteraceae, and Streptomycetaceae) were obviously enriched in the rhizospheres of the high-oil cultivars. Among them, Oxalobacteraceae (Massilia) was assembled specifically by the root exudates of high-oil cultivars and was associated with the phenolic acids and flavonoids in plant phenylpropanoid biosynthetic pathways. Furthermore, we showed that Massilia affected auxin signaling or interfered with active oxygen-related metabolism. In addition, Massilia activated glycolysis pathway, thereby promoting seed oil accumulation. Conclusions These results provide a solid theoretical basis for the breeding of revolutionary soybean cultivars with desired seed quality and optimal microbiomes and the development of new cultivation strategies for increasing the oil content of seeds. Video Abstracthttps://doi.org/10.1186/s40168-024-01933-7Improvements in host quality traitsOil contentRhizosphere microbiotaRoot exudatesPhenylpropanoid biosynthetic pathwaysGlycolysis pathway
spellingShingle Qin Han
Guanghui Zhu
Hongmei Qiu
Mingbo Li
Jiaming Zhang
Xinying Wu
Renhao Xiao
Yan Zhang
Wei Yang
Bing Tian
Lanxi Xu
Jiayang Zhou
Yutong Li
Yueqiang Wang
Yang Bai
Xia Li
Quality traits drive the enrichment of Massilia in the rhizosphere to improve soybean oil content
Microbiome
Improvements in host quality traits
Oil content
Rhizosphere microbiota
Root exudates
Phenylpropanoid biosynthetic pathways
Glycolysis pathway
title Quality traits drive the enrichment of Massilia in the rhizosphere to improve soybean oil content
title_full Quality traits drive the enrichment of Massilia in the rhizosphere to improve soybean oil content
title_fullStr Quality traits drive the enrichment of Massilia in the rhizosphere to improve soybean oil content
title_full_unstemmed Quality traits drive the enrichment of Massilia in the rhizosphere to improve soybean oil content
title_short Quality traits drive the enrichment of Massilia in the rhizosphere to improve soybean oil content
title_sort quality traits drive the enrichment of massilia in the rhizosphere to improve soybean oil content
topic Improvements in host quality traits
Oil content
Rhizosphere microbiota
Root exudates
Phenylpropanoid biosynthetic pathways
Glycolysis pathway
url https://doi.org/10.1186/s40168-024-01933-7
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