Insights into the mechanism of the effects of rhizosphere microorganisms on the quality of authentic <i>Angelica sinensis</i> under different soil microenvironments

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Abstract

Background

Angelica sinensis (Oliv.) Diels ( A. sinensis) is a Chinese herb grown in different geographical locations. It contains numerous active components with therapeutic value. Rhizosphere microbiomes affect various aspects of plant performance, such as nutrient acquisition, growth and development and plant diseases resistance. So far, few studies have investigated how the microbiome effects level of active components of A. sinensis. This study investigated whether changes in rhizosphere microbial communities and metabolites of A. sinensis vary with the soil microenvironment. Soils from the two main A. sinensis-producing areas, Gansu and Yunnan Province, were used to conduct pot experiments. The soil samples were divided into two parts, one part was sterilized and the other was unsterilized planting with the seedling variety of Gansu danggui 90–01. All seedlings were allowed to grow for 180 days. At the end of the experiment, radix A. sinensis were collected and used to characterize growth targets and chemical compositions. Rhizosphere soils were subjected to microbial analyses.

Results

Changes in metabolic profiles and rhizosphere microbial communities of A. sinensis grown under different soil microenvironments were similar. The GN (Gansu non-sterilized), YN (Yunnan non-sterilized), GS (Gansu sterilized), and YS (Yunnan sterilized) groups were significantly separated. Notably, antagonistic bacteria such as Sphingomonas, Pseudomonas, Lysobacter, Pseudoxanthomonas, etc. were significantly ( p < 0.05) enriched in Gansu soil compared with Yunnan soil. Moreover, senkyunolide I and ligustilide dimers which were enriched in GS group were strongly positively correlated with Pseudomonas parafulva; organic acids (including chlorogenic acid, dicaffeoylquinic acid and 5-feruloylquinic acid) and their ester coniferyl ferulate which were enriched in YS Group were positively associated with Gemmatimonadetes bacterium WY71 and Mucilaginibater sp., respectively.

Conclusions

The soil microenvironment influences growth and level/type of active components in A. sinensis. Further studies should explore the functional features of quality-related bacteria, identify the key response genes and clarify the interactions between genes and soil environments. This will reveal the mechanisms that determine the quality formation of genuine A. sinensis.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12870-021-03047-w.

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Most cited references 57

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For centuries, biologists have studied patterns of plant and animal diversity at continental scales. Until recently, similar studies were impossible for microorganisms, arguably the most diverse and abundant group of organisms on Earth. Here, we present a continental-scale description of soil bacterial communities and the environmental factors influencing their biodiversity. We collected 98 soil samples from across North and South America and used a ribosomal DNA-fingerprinting method to compare bacterial community composition and diversity quantitatively across sites. Bacterial diversity was unrelated to site temperature, latitude, and other variables that typically predict plant and animal diversity, and community composition was largely independent of geographic distance. The diversity and richness of soil bacterial communities differed by ecosystem type, and these differences could largely be explained by soil pH (r(2) = 0.70 and r(2) = 0.58, respectively; P < 0.0001 in both cases). Bacterial diversity was highest in neutral soils and lower in acidic soils, with soils from the Peruvian Amazon the most acidic and least diverse in our study. Our results suggest that microbial biogeography is controlled primarily by edaphic variables and differs fundamentally from the biogeography of "macro" organisms.

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Plants depend upon beneficial interactions between roots and microbes for nutrient availability, growth promotion, and disease suppression. High-throughput sequencing approaches have provided recent insights into root microbiomes, but our current understanding is still limited relative to animal microbiomes. Here we present a detailed characterization of the root-associated microbiomes of the crop plant rice by deep sequencing, using plants grown under controlled conditions as well as field cultivation at multiple sites. The spatial resolution of the study distinguished three root-associated compartments, the endosphere (root interior), rhizoplane (root surface), and rhizosphere (soil close to the root surface), each of which was found to harbor a distinct microbiome. Under controlled greenhouse conditions, microbiome composition varied with soil source and genotype. In field conditions, geographical location and cultivation practice, namely organic vs. conventional, were factors contributing to microbiome variation. Rice cultivation is a major source of global methane emissions, and methanogenic archaea could be detected in all spatial compartments of field-grown rice. The depth and scale of this study were used to build coabundance networks that revealed potential microbial consortia, some of which were involved in methane cycling. Dynamic changes observed during microbiome acquisition, as well as steady-state compositions of spatial compartments, support a multistep model for root microbiome assembly from soil wherein the rhizoplane plays a selective gating role. Similarities in the distribution of phyla in the root microbiomes of rice and other plants suggest that conclusions derived from this study might be generally applicable to land plants.

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Author and article information

Contributors

Hui Yan: glory-yan@163.com

Jin-ao Duan: dja@njucm.edu.cn

Journal

Journal ID (nlm-ta): BMC Plant Biol

Journal ID (iso-abbrev): BMC Plant Biol

Title: BMC Plant Biology

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2229

Publication date (Electronic): 22 June 2021

Publication date PMC-release: 22 June 2021

Publication date Collection: 2021

Volume: 21

Electronic Location Identifier: 285

Affiliations

[1 ]GRID grid.410745.3, ISNI 0000 0004 1765 1045, National and Local Collaborative Engineering Center of Chinese Medicinal Resources Industrialization and Formulae Innovative Medicine, Jiangsu Collaborative Innovation Center of Chinese Medicinal Resources Industrialization, State Administration of Traditional Chinese Medicine Key Laboratory of Chinese Medicinal Resources Recycling Utilization, , Nanjing University of Chinese Medicine, ; Nanjing, China

[2 ]GRID grid.27871.3b, ISNI 0000 0000 9750 7019, State Key Laboratory of Crop Genetics and Germplasm Enhancement, , Nanjing Agricultural University, ; Nanjing, China

Article

Publisher ID: 3047

DOI: 10.1186/s12870-021-03047-w

PMC ID: 8220839

PubMed ID: 34157988

SO-VID: 16046440-674a-49a1-a48d-b7844266108d

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

History

Date received : 23 December 2020

Date accepted : 11 May 2021

Custom metadata

ScienceOpen disciplines: Plant science & Botany

Keywords: angelica sinensis,rhizosphere microorganism,metabolomics,quality,correlation

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ScienceOpen disciplines: Plant science & Botany

Keywords: angelica sinensis, rhizosphere microorganism, metabolomics, quality, correlation

Insights into the mechanism of the effects of rhizosphere microorganisms on the quality of authentic Angelica sinensis under different soil microenvironments

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Abstract

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Supplementary Information

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Irish Journal of Agricultural and Food Research

Most cited references 57

The diversity and biogeography of soil bacterial communities.

The rhizosphere microbiome and plant health.

Structure, variation, and assembly of the root-associated microbiomes of rice.

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