Interspecific plant interaction structures the microbiomes of poplar-soil interface to alter nutrient cycling and utilization

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ABSTRACT

Terrestrial plants can influence the growth and health of adjacent plants through interspecific interaction. Here, the mechanisms of interspecific plant interaction on microbial function and nutrient utilization in the plant-soil interface (non-rhizosphere soil, rhizosphere soil, and root) were studied by soybean- and potato-poplar intercropping. First, metagenomics showed that soybean- and potato-poplar intercropping influenced the composition and co-occurrence networks of microbial communities in different ecological niches, with higher stability of the microbial community in soybean intercropping. Second, the gene abundance related to carbon metabolism, nitrogen cycling, phosphorus cycling, and sulfur cycling was increased at the poplar-soil interface in soybean intercropping. Moreover, soybean intercropping increased soil nutrient content and enzymatic activity. It showed higher metabolic potential in nutrient metabolism and transportation. Third, functional microorganisms that influenced nutrient cycling and transportation in different intercropping have been identified, namely Acidobacteria, Sphingomonas, Gemmatimonadaceae, Alphaproteobacteria, and Bradyrhizobium. Therefore, intercropping can construct microbial communities to alter metabolic functions and improve nutrient cycling and absorption. Interspecific plant interactions to influence the microbiome were revealed, opening up a new way for the precise regulation of plant microbiome.

IMPORTANCE

Poplar has the characteristics of wide distribution, strong adaptability, and fast growth, which is an ideal tree species for timber forest. In this study, metagenomics and elemental analysis were used to comprehensively reveal the effects of interspecific plant interactions on microbial communities and functions in different ecological niches. It can provide a theoretical basis for the development and application of the precise management model in poplar.

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The rhizosphere microbiome and plant health.

Roeland L. Berendsen, Corné Pieterse, Peter A.H.M. Bakker (2012)

The diversity of microbes associated with plant roots is enormous, in the order of tens of thousands of species. This complex plant-associated microbial community, also referred to as the second genome of the plant, is crucial for plant health. Recent advances in plant-microbe interactions research revealed that plants are able to shape their rhizosphere microbiome, as evidenced by the fact that different plant species host specific microbial communities when grown on the same soil. In this review, we discuss evidence that upon pathogen or insect attack, plants are able to recruit protective microorganisms, and enhance microbial activity to suppress pathogens in the rhizosphere. A comprehensive understanding of the mechanisms that govern selection and activity of microbial communities by plant roots will provide new opportunities to increase crop production. Copyright © 2012 Elsevier Ltd. All rights reserved.

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Structure and functions of the bacterial microbiota of plants.

Davide Bulgarelli, Klaus Schlaeppi, Stijn Spaepen … (2013)

Plants host distinct bacterial communities on and inside various plant organs, of which those associated with roots and the leaf surface are best characterized. The phylogenetic composition of these communities is defined by relatively few bacterial phyla, including Actinobacteria, Bacteroidetes, Firmicutes, and Proteobacteria. A synthesis of available data suggests a two-step selection process by which the bacterial microbiota of roots is differentiated from the surrounding soil biome. Rhizodeposition appears to fuel an initial substrate-driven community shift in the rhizosphere, which converges with host genotype-dependent fine-tuning of microbiota profiles in the selection of root endophyte assemblages. Substrate-driven selection also underlies the establishment of phyllosphere communities but takes place solely at the immediate leaf surface. Both the leaf and root microbiota contain bacteria that provide indirect pathogen protection, but root microbiota members appear to serve additional host functions through the acquisition of nutrients from soil for plant growth. Thus, the plant microbiota emerges as a fundamental trait that includes mutualism enabled through diverse biochemical mechanisms, as revealed by studies on plant growth-promoting and plant health-promoting bacteria.

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Soil bacterial networks are less stable under drought than fungal networks

Franciska T. de Vries, Rob I. Griffiths, Mark Bailey … (2018)

Soil microbial communities play a crucial role in ecosystem functioning, but it is unknown how co-occurrence networks within these communities respond to disturbances such as climate extremes. This represents an important knowledge gap because changes in microbial networks could have implications for their functioning and vulnerability to future disturbances. Here, we show in grassland mesocosms that drought promotes destabilising properties in soil bacterial, but not fungal, co-occurrence networks, and that changes in bacterial communities link more strongly to soil functioning during recovery than do changes in fungal communities. Moreover, we reveal that drought has a prolonged effect on bacterial communities and their co-occurrence networks via changes in vegetation composition and resultant reductions in soil moisture. Our results provide new insight in the mechanisms through which drought alters soil microbial communities with potential long-term consequences, including future plant community composition and the ability of aboveground and belowground communities to withstand future disturbances.

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Author and article information

Contributors

Yimin You:

ORCID: https://orcid.org/0009-0008-8399-7438

Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review and editing

Liran Wang: Role: ConceptualizationRole: Data curationRole: Formal analysisRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review and editing

Xiaoting Liu: Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: Supervision

Xuelai Wang: Role: Investigation

Luping Jiang: Role: Investigation

Changjun Ding: Role: Investigation

Weina Wang: Role: Investigation

Dawei Zhang: Role: Investigation

Xiyang Zhao: Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: Supervision

Adriana Lopes dos Santos: Role: Editor

Journal

Journal ID (nlm-ta): Microbiol Spectr

Journal ID (iso-abbrev): Microbiol Spectr

Journal ID (publisher-id): spectrum

Title: Microbiology Spectrum

Publisher: American Society for Microbiology (1752 N St., N.W., Washington, DC )

ISSN (Electronic): 2165-0497

Publication date (Electronic, collection): February 2024

Publication date (Electronic, pub): 10 January 2024

Publication date PMC-release: 10 January 2024

Volume: 12

Issue: 2

Electronic Location Identifier: e03368-23

Affiliations

[1 ]Jilin Provincial Key Laboratory of Tree and Grass Genetics and Breeding, College of Forestry and Grassland Science, Jilin Agricultural University; , Changchun, China

[2 ]National Key Laboratory of Forest Genetics and Breeding, Northeast Forestry University; , Harbin, China

[3 ]Chinese Academy of Forestry; , Beijing City, China

[4 ]Heilongjiang Provincial Forestry Technology Service Center; , Heilongjiang Province, China

[5 ]Fuyu Forest Farm; , Qiqihar City, China

Universitetet i Oslo; , Oslo, Norway

Author notes

Address correspondence to Yimin You, strivingmin@ 123456163.com

Address correspondence to Xiyang Zhao, zhaoxyphd@ 123456163.com

Yimin You and Liran Wang contributed equally to this article. Author order was determined by drawing straws.

The authors declare no conflict of interest.

Author information

Yimin You https://orcid.org/0009-0008-8399-7438

Article

Publisher ID: 03368-23 Publisher ID: spectrum.03368-23

DOI: 10.1128/spectrum.03368-23

PMC ID: 10846221

PubMed ID: 38197657

SO-VID: 55e364b9-38b7-4b72-98fc-57ef73c68886

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

History

Date received : 14 September 2023

Date accepted : 12 December 2023

Page count

supplementary-material: 1, authors: 9, Figures: 7, Tables: 1, References: 65, Pages: 17, Words: 8987

Funding

Funded by: MOST | National Key Research and Development Program of China (NKPs);

Award ID: 2021YFD2201204

Award Recipient : Xiyang Zhao

Custom metadata

cover-date February 2024

Keywords: intercropping,microbiome,co-occurrence networks,metabolism,rhizosphere

Data availability:

Keywords: intercropping, microbiome, co-occurrence networks, metabolism, rhizosphere

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Interspecific plant interaction structures the microbiomes of poplar-soil interface to alter nutrient cycling and utilization

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ABSTRACT

IMPORTANCE

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Most cited references 65

The rhizosphere microbiome and plant health.

Structure and functions of the bacterial microbiota of plants.

Soil bacterial networks are less stable under drought than fungal networks

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