Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome

Víctor J. Carrión, Juan Perez-Jaramillo, Viviane Cordovez, Vittorio Tracanna, Mattias De Hollander, Daniel Ruiz-Buck, Lucas W. Mendes, Wilfred F.J. van Ijcken, Ruth Gomez-Exposito, Somayah S. Elsayed, Prarthana Mohanraju, Adini Arifah, John van der Oost, Joseph N. Paulson, Rodrigo Mendes, Gilles P. van Wezel, Marnix H. Medema*, Jos M. Raaijmakers

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

5 Citations (Scopus)

Abstract

Microorganisms living inside plants can promote plant growth and health, but their genomic and functional diversity remain largely elusive. Here, metagenomics and network inference show that fungal infection of plant roots enriched for Chitinophagaceae and Flavobacteriaceae in the root endosphere and for chitinase genes and various unknown biosynthetic gene clusters encoding the production of nonribosomal peptide synthetases (NRPSs) and polyketide synthases (PKSs). After strain-level genome reconstruction, a consortium of Chitinophaga and Flavobacterium was designed that consistently suppressed fungal root disease. Site-directed mutagenesis then revealed that a previously unidentified NRPS-PKS gene cluster from Flavobacterium was essential for disease suppression by the endophytic consortium. Our results highlight that endophytic root microbiomes harbor a wealth of as yet unknown functional traits that, in concert, can protect the plant inside out.

Original languageEnglish
Pages (from-to)606-612
Number of pages7
JournalScience
Volume366
Issue number6465
DOIs
Publication statusPublished - 1 Nov 2019

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Microbiota
Peptide Synthases
Polyketide Synthases
Flavobacterium
Mycoses
Multigene Family
Flavobacteriaceae
Metagenomics
Chitinases
Plant Roots
Site-Directed Mutagenesis
Genome
Health
Growth
Genes

Cite this

Carrión, V. J., Perez-Jaramillo, J., Cordovez, V., Tracanna, V., De Hollander, M., Ruiz-Buck, D., ... Raaijmakers, J. M. (2019). Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome. Science, 366(6465), 606-612. https://doi.org/10.1126/science.aaw9285
Carrión, Víctor J. ; Perez-Jaramillo, Juan ; Cordovez, Viviane ; Tracanna, Vittorio ; De Hollander, Mattias ; Ruiz-Buck, Daniel ; Mendes, Lucas W. ; van Ijcken, Wilfred F.J. ; Gomez-Exposito, Ruth ; Elsayed, Somayah S. ; Mohanraju, Prarthana ; Arifah, Adini ; van der Oost, John ; Paulson, Joseph N. ; Mendes, Rodrigo ; van Wezel, Gilles P. ; Medema, Marnix H. ; Raaijmakers, Jos M. / Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome. In: Science. 2019 ; Vol. 366, No. 6465. pp. 606-612.
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abstract = "Microorganisms living inside plants can promote plant growth and health, but their genomic and functional diversity remain largely elusive. Here, metagenomics and network inference show that fungal infection of plant roots enriched for Chitinophagaceae and Flavobacteriaceae in the root endosphere and for chitinase genes and various unknown biosynthetic gene clusters encoding the production of nonribosomal peptide synthetases (NRPSs) and polyketide synthases (PKSs). After strain-level genome reconstruction, a consortium of Chitinophaga and Flavobacterium was designed that consistently suppressed fungal root disease. Site-directed mutagenesis then revealed that a previously unidentified NRPS-PKS gene cluster from Flavobacterium was essential for disease suppression by the endophytic consortium. Our results highlight that endophytic root microbiomes harbor a wealth of as yet unknown functional traits that, in concert, can protect the plant inside out.",
author = "Carri{\'o}n, {V{\'i}ctor J.} and Juan Perez-Jaramillo and Viviane Cordovez and Vittorio Tracanna and {De Hollander}, Mattias and Daniel Ruiz-Buck and Mendes, {Lucas W.} and {van Ijcken}, {Wilfred F.J.} and Ruth Gomez-Exposito and Elsayed, {Somayah S.} and Prarthana Mohanraju and Adini Arifah and {van der Oost}, John and Paulson, {Joseph N.} and Rodrigo Mendes and {van Wezel}, {Gilles P.} and Medema, {Marnix H.} and Raaijmakers, {Jos M.}",
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Carrión, VJ, Perez-Jaramillo, J, Cordovez, V, Tracanna, V, De Hollander, M, Ruiz-Buck, D, Mendes, LW, van Ijcken, WFJ, Gomez-Exposito, R, Elsayed, SS, Mohanraju, P, Arifah, A, van der Oost, J, Paulson, JN, Mendes, R, van Wezel, GP, Medema, MH & Raaijmakers, JM 2019, 'Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome', Science, vol. 366, no. 6465, pp. 606-612. https://doi.org/10.1126/science.aaw9285

Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome. / Carrión, Víctor J.; Perez-Jaramillo, Juan; Cordovez, Viviane; Tracanna, Vittorio; De Hollander, Mattias; Ruiz-Buck, Daniel; Mendes, Lucas W.; van Ijcken, Wilfred F.J.; Gomez-Exposito, Ruth; Elsayed, Somayah S.; Mohanraju, Prarthana; Arifah, Adini; van der Oost, John; Paulson, Joseph N.; Mendes, Rodrigo; van Wezel, Gilles P.; Medema, Marnix H.; Raaijmakers, Jos M.

In: Science, Vol. 366, No. 6465, 01.11.2019, p. 606-612.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome

AU - Carrión, Víctor J.

AU - Perez-Jaramillo, Juan

AU - Cordovez, Viviane

AU - Tracanna, Vittorio

AU - De Hollander, Mattias

AU - Ruiz-Buck, Daniel

AU - Mendes, Lucas W.

AU - van Ijcken, Wilfred F.J.

AU - Gomez-Exposito, Ruth

AU - Elsayed, Somayah S.

AU - Mohanraju, Prarthana

AU - Arifah, Adini

AU - van der Oost, John

AU - Paulson, Joseph N.

AU - Mendes, Rodrigo

AU - van Wezel, Gilles P.

AU - Medema, Marnix H.

AU - Raaijmakers, Jos M.

PY - 2019/11/1

Y1 - 2019/11/1

N2 - Microorganisms living inside plants can promote plant growth and health, but their genomic and functional diversity remain largely elusive. Here, metagenomics and network inference show that fungal infection of plant roots enriched for Chitinophagaceae and Flavobacteriaceae in the root endosphere and for chitinase genes and various unknown biosynthetic gene clusters encoding the production of nonribosomal peptide synthetases (NRPSs) and polyketide synthases (PKSs). After strain-level genome reconstruction, a consortium of Chitinophaga and Flavobacterium was designed that consistently suppressed fungal root disease. Site-directed mutagenesis then revealed that a previously unidentified NRPS-PKS gene cluster from Flavobacterium was essential for disease suppression by the endophytic consortium. Our results highlight that endophytic root microbiomes harbor a wealth of as yet unknown functional traits that, in concert, can protect the plant inside out.

AB - Microorganisms living inside plants can promote plant growth and health, but their genomic and functional diversity remain largely elusive. Here, metagenomics and network inference show that fungal infection of plant roots enriched for Chitinophagaceae and Flavobacteriaceae in the root endosphere and for chitinase genes and various unknown biosynthetic gene clusters encoding the production of nonribosomal peptide synthetases (NRPSs) and polyketide synthases (PKSs). After strain-level genome reconstruction, a consortium of Chitinophaga and Flavobacterium was designed that consistently suppressed fungal root disease. Site-directed mutagenesis then revealed that a previously unidentified NRPS-PKS gene cluster from Flavobacterium was essential for disease suppression by the endophytic consortium. Our results highlight that endophytic root microbiomes harbor a wealth of as yet unknown functional traits that, in concert, can protect the plant inside out.

U2 - 10.1126/science.aaw9285

DO - 10.1126/science.aaw9285

M3 - Article

VL - 366

SP - 606

EP - 612

JO - Science

JF - Science

SN - 0036-8075

IS - 6465

ER -

Carrión VJ, Perez-Jaramillo J, Cordovez V, Tracanna V, De Hollander M, Ruiz-Buck D et al. Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome. Science. 2019 Nov 1;366(6465):606-612. https://doi.org/10.1126/science.aaw9285