The peanut root exudate increases the transport and metabolism of nutrients and enhances the plant growth-promoting effects of <i>burkholderia pyrrocinia</i> strain P10

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Abstract

Background

Burkholderia pyrrocinia strain P10 is a plant growth-promoting rhizobacterium (PGPR) that can substantially increase peanut growth. However, the mechanisms and pathways involved in the interaction between B. pyrrocinia P10 and peanut remain unclear. To clarify complex plant–PGPR interactions and the growth-promoting effects of PGPR strains, the B. pyrrocinia P10 transcriptome changes in response to the peanut root exudate (RE) were elucidated and the effects of RE components on biofilm formation and indole-3-acetic acid (IAA) secretion were analyzed.

Results

During the early interaction phase, the peanut RE enhanced the transport and metabolism of nutrients, including carbohydrates, amino acids, nitrogen, and sulfur. Although the expression of flagellar assembly-related genes was down-regulated, the expression levels of other genes involved in biofilm formation, quorum sensing, and Type II, III, and VI secretion systems were up-regulated, thereby enabling strain P10 to outcompete other microbes to colonize the peanut rhizosphere. The peanut RE also improved the plant growth-promoting effects of strain P10 by activating the expression of genes associated with siderophore biosynthesis, IAA production, and phosphorus solubilization. Additionally, organic acids and amino acids were identified as the dominant components in the peanut RE. Furthermore, strain P10 biofilm formation was induced by malic acid, oxalic acid, and citric acid, whereas IAA secretion was promoted by the alanine, glycine, and proline in the peanut RE.

Conclusion

The peanut RE positively affects B. pyrrocinia P10 growth, while also enhancing colonization and growth-promoting effects during the early interaction period. These findings may help to elucidate the mechanisms underlying complex plant–PGPR interactions, with potential implications for improving the applicability of PGPR strains.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12866-023-02818-9.

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Most cited references 68

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KEGG: kyoto encyclopedia of genes and genomes.

M Kanehisa (2000)

KEGG (Kyoto Encyclopedia of Genes and Genomes) is a knowledge base for systematic analysis of gene functions, linking genomic information with higher order functional information. The genomic information is stored in the GENES database, which is a collection of gene catalogs for all the completely sequenced genomes and some partial genomes with up-to-date annotation of gene functions. The higher order functional information is stored in the PATHWAY database, which contains graphical representations of cellular processes, such as metabolism, membrane transport, signal transduction and cell cycle. The PATHWAY database is supplemented by a set of ortholog group tables for the information about conserved subpathways (pathway motifs), which are often encoded by positionally coupled genes on the chromosome and which are especially useful in predicting gene functions. A third database in KEGG is LIGAND for the information about chemical compounds, enzyme molecules and enzymatic reactions. KEGG provides Java graphics tools for browsing genome maps, comparing two genome maps and manipulating expression maps, as well as computational tools for sequence comparison, graph comparison and path computation. The KEGG databases are daily updated and made freely available (http://www. genome.ad.jp/kegg/).

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Toward understanding the origin and evolution of cellular organisms

Minoru Kanehisa (2019)

In this era of high‐throughput biology, bioinformatics has become a major discipline for making sense out of large‐scale datasets. Bioinformatics is usually considered as a practical field developing databases and software tools for supporting other fields, rather than a fundamental scientific discipline for uncovering principles of biology. The KEGG resource that we have been developing is a reference knowledge base for biological interpretation of genome sequences and other high‐throughput data. It is now one of the most utilized biological databases because of its practical values. For me personally, KEGG is a step toward understanding the origin and evolution of cellular organisms.

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KEGG: integrating viruses and cellular organisms

Minoru Kanehisa, Miho Furumichi, Yoko Sato … (2020)

Abstract KEGG (https://www.kegg.jp/) is a manually curated resource integrating eighteen databases categorized into systems, genomic, chemical and health information. It also provides KEGG mapping tools, which enable understanding of cellular and organism-level functions from genome sequences and other molecular datasets. KEGG mapping is a predictive method of reconstructing molecular network systems from molecular building blocks based on the concept of functional orthologs. Since the introduction of the KEGG NETWORK database, various diseases have been associated with network variants, which are perturbed molecular networks caused by human gene variants, viruses, other pathogens and environmental factors. The network variation maps are created as aligned sets of related networks showing, for example, how different viruses inhibit or activate specific cellular signaling pathways. The KEGG pathway maps are now integrated with network variation maps in the NETWORK database, as well as with conserved functional units of KEGG modules and reaction modules in the MODULE database. The KO database for functional orthologs continues to be improved and virus KOs are being expanded for better understanding of virus-cell interactions and for enabling prediction of viral perturbations.

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Author and article information

Contributors

Lizhen Han: lzhan1@gzu.edu.cn

Hong Zhang: 1528332100@qq.com

Xue Bai: 1035376374@qq.com

Biao Jiang: 974518089@qq.com

Journal

Journal ID (nlm-ta): BMC Microbiol

Journal ID (iso-abbrev): BMC Microbiol

Title: BMC Microbiology

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2180

Publication date (Electronic): 30 March 2023

Publication date PMC-release: 30 March 2023

Publication date Collection: 2023

Volume: 23

Electronic Location Identifier: 85

Affiliations

GRID grid.443382.a, ISNI 0000 0004 1804 268X, College of Life Sciences, , Guizhou University, ; 550025 Guiyang, Guizhou China

Article

Publisher ID: 2818

DOI: 10.1186/s12866-023-02818-9

PMC ID: 10061817

PubMed ID: 36991332

SO-VID: b15de0a7-8249-41d8-9d10-68316aec78ac

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 : 12 January 2023

Date accepted : 10 March 2023

Funding

Funded by: the National Natural Science Foundation of China

Award ID: 31760030

Funded by: the Science and Technology Planning Project of Guizhou Province

Award ID: ZK[2022]009

Custom metadata

ScienceOpen disciplines: Microbiology & Virology

Keywords: burkholderia pyrrocinia,arachis hypogaea,pgpr,root exudates,growth-promoting mechanisms

Data availability:

ScienceOpen disciplines: Microbiology & Virology

Keywords: burkholderia pyrrocinia, arachis hypogaea, pgpr, root exudates, growth-promoting mechanisms

The peanut root exudate increases the transport and metabolism of nutrients and enhances the plant growth-promoting effects of burkholderia pyrrocinia strain P10

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Abstract

Background

Results

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Supplementary Information

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Role of Microbes in Soil Fertility and Human Health

Most cited references 68

KEGG: kyoto encyclopedia of genes and genomes.

Toward understanding the origin and evolution of cellular organisms

KEGG: integrating viruses and cellular organisms

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