Taxonomic Structure of Rhizosphere Bacterial Communities and Its Association With the Accumulation of Alkaloidal Metabolites in Sophora flavescens

Plant secondary metabolites (SMs) play a crucial role in plant defense against pathogens and adaptation to environmental stresses, some of which are produced from medicinal plants and are the material basis of clinical efficacy and vital indicators for quality evaluation of corresponding medicinal m...

Full description

Bibliographic Details
Main Authors: Jie Chen, Na Li, Jiayu Chang, Kaida Ren, Jiangtao Zhou, Guan’e Yang
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-12-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.781316/full
_version_ 1819172683181457408
author Jie Chen
Na Li
Jiayu Chang
Kaida Ren
Jiangtao Zhou
Guan’e Yang
author_facet Jie Chen
Na Li
Jiayu Chang
Kaida Ren
Jiangtao Zhou
Guan’e Yang
author_sort Jie Chen
collection DOAJ
description Plant secondary metabolites (SMs) play a crucial role in plant defense against pathogens and adaptation to environmental stresses, some of which are produced from medicinal plants and are the material basis of clinical efficacy and vital indicators for quality evaluation of corresponding medicinal materials. The influence of plant microbiota on plant nutrient uptake, production, and stress tolerance has been revealed, but the associations between plant microbiota and the accumulation of SMs in medicinal plants remain largely unknown. Plant SMs can vary among individuals, which could be partly ascribed to the shift in microbial community associated with the plant host. In the present study, we sampled fine roots and rhizosphere soils of Sophora flavescens grown in four well-separated cities/counties in China and determined the taxonomic composition of rhizosphere bacterial communities using Illumina 16S amplicon sequencing. In addition, the association of the rhizosphere bacterial microbiota with the accumulation of alkaloids in the roots of S. flavescens was analyzed. The results showed that S. flavescens hosted distinct bacterial communities in the rhizosphere across geographic locations and plant ages, also indicating that geographic location was a larger source of variation than plant age. Moreover, redundancy analysis revealed that spatial, climatic (mean annual temperature and precipitation), and edaphic factors (pH and available N and P) were the key drivers that shape the rhizosphere bacterial communities. Furthermore, the results of the Mantel test demonstrated that the rhizosphere bacterial microbiota was remarkably correlated with the contents of oxymatrine, sophoridine, and matrine + oxymatrine in roots. Specific taxa belonging to Actinobacteria and Chloroflexi were identified as potential beneficial bacteria associated with the total accumulation of matrine and oxymatrine by a random forest machine learning algorithm. Finally, the structural equation modeling indicated that the Actinobacteria phylum had a direct effect on the total accumulation of matrine and oxymatrine. The present study addresses the association between the rhizosphere bacterial communities and the accumulation of alkaloids in the medicinal plant S. flavescens. Our findings may provide a basis for the quality improvement and sustainable utilization of this medicinal plant thorough rhizosphere microbiota manipulation.
first_indexed 2024-12-22T20:11:05Z
format Article
id doaj.art-33dbd900218d412da4f10af2e5a0e490
institution Directory Open Access Journal
issn 1664-302X
language English
last_indexed 2024-12-22T20:11:05Z
publishDate 2021-12-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Microbiology
spelling doaj.art-33dbd900218d412da4f10af2e5a0e4902022-12-21T18:14:02ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-12-011210.3389/fmicb.2021.781316781316Taxonomic Structure of Rhizosphere Bacterial Communities and Its Association With the Accumulation of Alkaloidal Metabolites in Sophora flavescensJie ChenNa LiJiayu ChangKaida RenJiangtao ZhouGuan’e YangPlant secondary metabolites (SMs) play a crucial role in plant defense against pathogens and adaptation to environmental stresses, some of which are produced from medicinal plants and are the material basis of clinical efficacy and vital indicators for quality evaluation of corresponding medicinal materials. The influence of plant microbiota on plant nutrient uptake, production, and stress tolerance has been revealed, but the associations between plant microbiota and the accumulation of SMs in medicinal plants remain largely unknown. Plant SMs can vary among individuals, which could be partly ascribed to the shift in microbial community associated with the plant host. In the present study, we sampled fine roots and rhizosphere soils of Sophora flavescens grown in four well-separated cities/counties in China and determined the taxonomic composition of rhizosphere bacterial communities using Illumina 16S amplicon sequencing. In addition, the association of the rhizosphere bacterial microbiota with the accumulation of alkaloids in the roots of S. flavescens was analyzed. The results showed that S. flavescens hosted distinct bacterial communities in the rhizosphere across geographic locations and plant ages, also indicating that geographic location was a larger source of variation than plant age. Moreover, redundancy analysis revealed that spatial, climatic (mean annual temperature and precipitation), and edaphic factors (pH and available N and P) were the key drivers that shape the rhizosphere bacterial communities. Furthermore, the results of the Mantel test demonstrated that the rhizosphere bacterial microbiota was remarkably correlated with the contents of oxymatrine, sophoridine, and matrine + oxymatrine in roots. Specific taxa belonging to Actinobacteria and Chloroflexi were identified as potential beneficial bacteria associated with the total accumulation of matrine and oxymatrine by a random forest machine learning algorithm. Finally, the structural equation modeling indicated that the Actinobacteria phylum had a direct effect on the total accumulation of matrine and oxymatrine. The present study addresses the association between the rhizosphere bacterial communities and the accumulation of alkaloids in the medicinal plant S. flavescens. Our findings may provide a basis for the quality improvement and sustainable utilization of this medicinal plant thorough rhizosphere microbiota manipulation.https://www.frontiersin.org/articles/10.3389/fmicb.2021.781316/fullmedicinal plantssecondary metabolitesalkaloidsplant bacterial communityrhizosphere
spellingShingle Jie Chen
Na Li
Jiayu Chang
Kaida Ren
Jiangtao Zhou
Guan’e Yang
Taxonomic Structure of Rhizosphere Bacterial Communities and Its Association With the Accumulation of Alkaloidal Metabolites in Sophora flavescens
Frontiers in Microbiology
medicinal plants
secondary metabolites
alkaloids
plant bacterial community
rhizosphere
title Taxonomic Structure of Rhizosphere Bacterial Communities and Its Association With the Accumulation of Alkaloidal Metabolites in Sophora flavescens
title_full Taxonomic Structure of Rhizosphere Bacterial Communities and Its Association With the Accumulation of Alkaloidal Metabolites in Sophora flavescens
title_fullStr Taxonomic Structure of Rhizosphere Bacterial Communities and Its Association With the Accumulation of Alkaloidal Metabolites in Sophora flavescens
title_full_unstemmed Taxonomic Structure of Rhizosphere Bacterial Communities and Its Association With the Accumulation of Alkaloidal Metabolites in Sophora flavescens
title_short Taxonomic Structure of Rhizosphere Bacterial Communities and Its Association With the Accumulation of Alkaloidal Metabolites in Sophora flavescens
title_sort taxonomic structure of rhizosphere bacterial communities and its association with the accumulation of alkaloidal metabolites in sophora flavescens
topic medicinal plants
secondary metabolites
alkaloids
plant bacterial community
rhizosphere
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.781316/full
work_keys_str_mv AT jiechen taxonomicstructureofrhizospherebacterialcommunitiesanditsassociationwiththeaccumulationofalkaloidalmetabolitesinsophoraflavescens
AT nali taxonomicstructureofrhizospherebacterialcommunitiesanditsassociationwiththeaccumulationofalkaloidalmetabolitesinsophoraflavescens
AT jiayuchang taxonomicstructureofrhizospherebacterialcommunitiesanditsassociationwiththeaccumulationofalkaloidalmetabolitesinsophoraflavescens
AT kaidaren taxonomicstructureofrhizospherebacterialcommunitiesanditsassociationwiththeaccumulationofalkaloidalmetabolitesinsophoraflavescens
AT jiangtaozhou taxonomicstructureofrhizospherebacterialcommunitiesanditsassociationwiththeaccumulationofalkaloidalmetabolitesinsophoraflavescens
AT guaneyang taxonomicstructureofrhizospherebacterialcommunitiesanditsassociationwiththeaccumulationofalkaloidalmetabolitesinsophoraflavescens