The fungal root endophyte Serendipita vermifera displays inter-kingdom synergistic beneficial effects with the microbiota in Arabidopsis thaliana and barley

Lisa K. Mahdi; Shingo Miyauchi; Charles Uhlmann; Ruben Garrido-Oter; Gregor Langen; Stephan Wawra; Yulong Niu; Rui Guan; Senga Robertson-Albertyn; Davide Bulgarelli; Jane E. Parker; Alga Zuccaro

doi:10.1038/s41396-021-01138-y

The fungal root endophyte Serendipita vermifera displays inter-kingdom synergistic beneficial effects with the microbiota in Arabidopsis thaliana and barley

Lisa K. Mahdi, Shingo Miyauchi, Charles Uhlmann, Ruben Garrido-Oter, Gregor Langen, Stephan Wawra, Yulong Niu, Rui Guan, Senga Robertson-Albertyn, Davide Bulgarelli, Jane E. Parker, Alga Zuccaro (Lead / Corresponding author)

Plant Sciences

Research output: Contribution to journal › Article › peer-review

30 Citations (Scopus)

140 Downloads (Pure)

Abstract

Plant root-associated bacteria can confer protection against pathogen infection. By contrast, the beneficial effects of root endophytic fungi and their synergistic interactions with bacteria remain poorly defined. We demonstrate that the combined action of a fungal root endophyte from a widespread taxon with core bacterial microbiota members provides synergistic protection against an aggressive soil-borne pathogen in Arabidopsis thaliana and barley. We additionally reveal early inter-kingdom growth promotion benefits which are host and microbiota composition dependent. Using RNA-sequencing, we show that these beneficial activities are not associated with extensive host transcriptional reprogramming but rather with the modulation of expression of microbial effectors and carbohydrate-active enzymes.

Original language	English
Pages (from-to)	876-889
Number of pages	14
Journal	ISME Journal
Volume	16
Early online date	22 Oct 2021
DOIs	https://doi.org/10.1038/s41396-021-01138-y
Publication status	Published - Mar 2022

Keywords

Plant sciences
Symbiosis

ASJC Scopus subject areas

Microbiology
Ecology, Evolution, Behavior and Systematics

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10.1038/s41396-021-01138-y

Final Published VersionFinal published version, 3.71 MBLicence: CC BY

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Mahdi, L. K., Miyauchi, S., Uhlmann, C., Garrido-Oter, R., Langen, G., Wawra, S., Niu, Y., Guan, R., Robertson-Albertyn, S., Bulgarelli, D., Parker, J. E., & Zuccaro, A. (2022). The fungal root endophyte Serendipita vermifera displays inter-kingdom synergistic beneficial effects with the microbiota in Arabidopsis thaliana and barley. ISME Journal, 16, 876-889. https://doi.org/10.1038/s41396-021-01138-y

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title = "The fungal root endophyte Serendipita vermifera displays inter-kingdom synergistic beneficial effects with the microbiota in Arabidopsis thaliana and barley",

abstract = "Plant root-associated bacteria can confer protection against pathogen infection. By contrast, the beneficial effects of root endophytic fungi and their synergistic interactions with bacteria remain poorly defined. We demonstrate that the combined action of a fungal root endophyte from a widespread taxon with core bacterial microbiota members provides synergistic protection against an aggressive soil-borne pathogen in Arabidopsis thaliana and barley. We additionally reveal early inter-kingdom growth promotion benefits which are host and microbiota composition dependent. Using RNA-sequencing, we show that these beneficial activities are not associated with extensive host transcriptional reprogramming but rather with the modulation of expression of microbial effectors and carbohydrate-active enzymes.",

keywords = "Plant sciences, Symbiosis",

author = "Mahdi, {Lisa K.} and Shingo Miyauchi and Charles Uhlmann and Ruben Garrido-Oter and Gregor Langen and Stephan Wawra and Yulong Niu and Rui Guan and Senga Robertson-Albertyn and Davide Bulgarelli and Parker, {Jane E.} and Alga Zuccaro",

note = "Funding Information: We thank Paul Schulze-Lefert and the DECRyPT community (SPP 2125) for providing the bacterial strains used in this study. LM was supported by the Max-Planck-Gesellschaft through the International Max Planck Research School (IMPRS) on {\textquoteleft}Understanding Complex Plant Traits using Computational and Evolutionary Approaches{\textquoteright} and the University of Cologne. AZ and JEP acknowledge support from the Cluster of Excellence on Plant Sciences (CEPLAS) funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany{\textquoteright}s Excellence Strategy—EXC 2048/1—Project ID: 390686111 and projects ZU 263/11-1 and PA 917/8-1 (SPP DECRyPT). JEP and CU acknowledge The Max Planck Society for additional support. Graphical illustrations were designed with the BioRender online tool. We thank Francis Martin for allowing us to use the secretome prediction and visual omics workflow on the computing cluster at INRAE Nancy, France. Publisher Copyright: {\textcopyright} 2021, The Author(s).",

year = "2022",

month = mar,

doi = "10.1038/s41396-021-01138-y",

language = "English",

volume = "16",

pages = "876--889",

journal = "ISME Journal",

issn = "1751-7362",

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Mahdi, LK, Miyauchi, S, Uhlmann, C, Garrido-Oter, R, Langen, G, Wawra, S, Niu, Y, Guan, R, Robertson-Albertyn, S, Bulgarelli, D, Parker, JE & Zuccaro, A 2022, 'The fungal root endophyte Serendipita vermifera displays inter-kingdom synergistic beneficial effects with the microbiota in Arabidopsis thaliana and barley', ISME Journal, vol. 16, pp. 876-889. https://doi.org/10.1038/s41396-021-01138-y

TY - JOUR

T1 - The fungal root endophyte Serendipita vermifera displays inter-kingdom synergistic beneficial effects with the microbiota in Arabidopsis thaliana and barley

AU - Mahdi, Lisa K.

AU - Miyauchi, Shingo

AU - Uhlmann, Charles

AU - Garrido-Oter, Ruben

AU - Langen, Gregor

AU - Wawra, Stephan

AU - Niu, Yulong

AU - Guan, Rui

AU - Robertson-Albertyn, Senga

AU - Bulgarelli, Davide

AU - Parker, Jane E.

AU - Zuccaro, Alga

N1 - Funding Information: We thank Paul Schulze-Lefert and the DECRyPT community (SPP 2125) for providing the bacterial strains used in this study. LM was supported by the Max-Planck-Gesellschaft through the International Max Planck Research School (IMPRS) on ‘Understanding Complex Plant Traits using Computational and Evolutionary Approaches’ and the University of Cologne. AZ and JEP acknowledge support from the Cluster of Excellence on Plant Sciences (CEPLAS) funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany’s Excellence Strategy—EXC 2048/1—Project ID: 390686111 and projects ZU 263/11-1 and PA 917/8-1 (SPP DECRyPT). JEP and CU acknowledge The Max Planck Society for additional support. Graphical illustrations were designed with the BioRender online tool. We thank Francis Martin for allowing us to use the secretome prediction and visual omics workflow on the computing cluster at INRAE Nancy, France. Publisher Copyright: © 2021, The Author(s).

PY - 2022/3

Y1 - 2022/3

N2 - Plant root-associated bacteria can confer protection against pathogen infection. By contrast, the beneficial effects of root endophytic fungi and their synergistic interactions with bacteria remain poorly defined. We demonstrate that the combined action of a fungal root endophyte from a widespread taxon with core bacterial microbiota members provides synergistic protection against an aggressive soil-borne pathogen in Arabidopsis thaliana and barley. We additionally reveal early inter-kingdom growth promotion benefits which are host and microbiota composition dependent. Using RNA-sequencing, we show that these beneficial activities are not associated with extensive host transcriptional reprogramming but rather with the modulation of expression of microbial effectors and carbohydrate-active enzymes.

AB - Plant root-associated bacteria can confer protection against pathogen infection. By contrast, the beneficial effects of root endophytic fungi and their synergistic interactions with bacteria remain poorly defined. We demonstrate that the combined action of a fungal root endophyte from a widespread taxon with core bacterial microbiota members provides synergistic protection against an aggressive soil-borne pathogen in Arabidopsis thaliana and barley. We additionally reveal early inter-kingdom growth promotion benefits which are host and microbiota composition dependent. Using RNA-sequencing, we show that these beneficial activities are not associated with extensive host transcriptional reprogramming but rather with the modulation of expression of microbial effectors and carbohydrate-active enzymes.

KW - Plant sciences

KW - Symbiosis

UR - http://www.scopus.com/inward/record.url?scp=85117575095&partnerID=8YFLogxK

U2 - 10.1038/s41396-021-01138-y

DO - 10.1038/s41396-021-01138-y

M3 - Article

C2 - 34686763

AN - SCOPUS:85117575095

SN - 1751-7362

VL - 16

SP - 876

EP - 889

JO - ISME Journal

JF - ISME Journal

ER -

The fungal root endophyte Serendipita vermifera displays inter-kingdom synergistic beneficial effects with the microbiota in Arabidopsis thaliana and barley

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Keywords

ASJC Scopus subject areas

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The fungal root endophyte Serendipita vermifera displays inter-kingdom synergistic beneficial effects with the microbiota in Arabidopsis thaliana and barley

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