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

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 an...

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Published in	Science (American Association for the Advancement of Science) Vol. 366; no. 6465; pp. 606 - 612
Main Authors	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
Format	Journal Article
Language	English
Published	United States The American Association for the Advancement of Science 01.11.2019
Subjects	Antifungal activity Bacteria - classification Bacterial Physiological Phenomena Bacteroidetes - physiology Beta vulgaris - microbiology Biodiversity Cell walls Chitinase Chitinases - genetics Chitinophagaceae Consortia Disease Resistance Endophytes Endophytes - physiology Flavobacterium Flavobacterium - physiology Fungal diseases Fungi Fungicides Gene clusters Genes, Bacterial Genome, Bacterial Genomes Metabolites Metagenome Microbiomes Microbiota Microorganisms Mutagenesis, Site-Directed Pathogens Peptide Synthases - genetics Phenotypes Plant diseases Plant Diseases - microbiology Plant growth Plant protection Plant roots Plant Roots - microbiology Polyketide Synthases - genetics Polyketides Rhizoctonia - pathogenicity Rhizoctonia solani Roots Secondary metabolites Siderophores Site-directed mutagenesis Soil Microbiology Sugar beets Transcription Wilt
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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 and was designed that consistently suppressed fungal root disease. Site-directed mutagenesis then revealed that a previously unidentified NRPS-PKS gene cluster from 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.
AbstractList	Some soils show a remarkable ability to suppress disease caused by plant pathogens, an ability that is attributed to plant-associated microbiota. Carrión et al. investigated the role of endophytes, the intimate microbial community found within roots, in fungal disease suppression (see the Perspective by Tringe). The wilt fungus Rhizoctonia solani infects sugar beets, whereupon transcriptional analysis shows that several bacterial endophyte species activate biosynthetic gene clusters to cause disease suppression. These organisms produce antifungal effectors, including enzymes that can digest fungal cell walls, and secondary metabolites, including phenazines, polyketides, and siderophores, which may contribute to the antifungal phenotype. Science , this issue p. 606 ; see also p. 568 Bacteria living between and within the roots of plants exposed to a fungal pathogen can help generate a disease-suppressing phenotype. 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. Protecting plants from the inside outSome soils show a remarkable ability to suppress disease caused by plant pathogens, an ability that is attributed to plant-associated microbiota. Carrión et al. investigated the role of endophytes, the intimate microbial community found within roots, in fungal disease suppression (see the Perspective by Tringe). The wilt fungus Rhizoctonia solani infects sugar beets, whereupon transcriptional analysis shows that several bacterial endophyte species activate biosynthetic gene clusters to cause disease suppression. These organisms produce antifungal effectors, including enzymes that can digest fungal cell walls, and secondary metabolites, including phenazines, polyketides, and siderophores, which may contribute to the antifungal phenotype.Science, this issue p. 606; see also p. 568Microorganisms 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. 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 and was designed that consistently suppressed fungal root disease. Site-directed mutagenesis then revealed that a previously unidentified NRPS-PKS gene cluster from 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	Mendes, Lucas W Mohanraju, Prarthana Mendes, Rodrigo Paulson, Joseph N Perez-Jaramillo, Juan Ruiz-Buck, Daniel Raaijmakers, Jos M van Ijcken, Wilfred F J van der Oost, John Tracanna, Vittorio Elsayed, Somayah S Arifah, Adini Cordovez, Viviane van Wezel, Gilles P Medema, Marnix H de Hollander, Mattias Gomez-Exposito, Ruth Carrión, Víctor J
Author_xml	– sequence: 1 givenname: Víctor J orcidid: 0000-0002-4093-0355 surname: Carrión fullname: Carrión, Víctor J organization: Institute of Biology, Leiden University, Sylviusweg 72, 2333 BE Leiden, Netherlands – sequence: 2 givenname: Juan orcidid: 0000-0002-0479-7227 surname: Perez-Jaramillo fullname: Perez-Jaramillo, Juan organization: PECET, University of Antioquia, Medellín, Antioquia 050010, Colombia – sequence: 3 givenname: Viviane orcidid: 0000-0002-3669-7298 surname: Cordovez fullname: Cordovez, Viviane organization: Institute of Biology, Leiden University, Sylviusweg 72, 2333 BE Leiden, Netherlands – sequence: 4 givenname: Vittorio surname: Tracanna fullname: Tracanna, Vittorio organization: Bioinformatics Group, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, Netherlands – sequence: 5 givenname: Mattias surname: de Hollander fullname: de Hollander, Mattias organization: Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Droevendaalsesteeg 10, 6708 PB Wageningen, Netherlands – sequence: 6 givenname: Daniel surname: Ruiz-Buck fullname: Ruiz-Buck, Daniel organization: Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Droevendaalsesteeg 10, 6708 PB Wageningen, Netherlands – sequence: 7 givenname: Lucas W orcidid: 0000-0003-0980-7006 surname: Mendes fullname: Mendes, Lucas W organization: Cell and Molecular Biology Laboratory, Center for Nuclear Energy in Agriculture (CENA), University of Sao Paulo (USP), Piracicaba, Brazil – sequence: 8 givenname: Wilfred F J orcidid: 0000-0002-0421-8301 surname: van Ijcken fullname: van Ijcken, Wilfred F J organization: Erasmus MC, University Medical Center Rotterdam, Department of Cell Biology, Center for Biomics, 3025 CN Rotterdam, Netherlands – sequence: 9 givenname: Ruth surname: Gomez-Exposito fullname: Gomez-Exposito, Ruth organization: Laboratory of Microbiology, Wageningen University and Research, Stippeneng 4, 6708 WE Wageningen, Netherlands – sequence: 10 givenname: Somayah S orcidid: 0000-0003-3837-6137 surname: Elsayed fullname: Elsayed, Somayah S organization: Institute of Biology, Leiden University, Sylviusweg 72, 2333 BE Leiden, Netherlands – sequence: 11 givenname: Prarthana orcidid: 0000-0002-4766-8660 surname: Mohanraju fullname: Mohanraju, Prarthana organization: Laboratory of Microbiology, Wageningen University and Research, Stippeneng 4, 6708 WE Wageningen, Netherlands – sequence: 12 givenname: Adini orcidid: 0000-0002-9283-9713 surname: Arifah fullname: Arifah, Adini organization: Laboratory of Microbiology, Wageningen University and Research, Stippeneng 4, 6708 WE Wageningen, Netherlands – sequence: 13 givenname: John orcidid: 0000-0001-5024-1871 surname: van der Oost fullname: van der Oost, John organization: Laboratory of Microbiology, Wageningen University and Research, Stippeneng 4, 6708 WE Wageningen, Netherlands – sequence: 14 givenname: Joseph N orcidid: 0000-0001-8221-7139 surname: Paulson fullname: Paulson, Joseph N organization: Department of Biostatistics, Product Development, Genentech Inc., South San Francisco, CA 94080, USA – sequence: 15 givenname: Rodrigo orcidid: 0000-0002-9817-4118 surname: Mendes fullname: Mendes, Rodrigo organization: Laboratory of Environmental Microbiology, Brazilian Agricultural Research Corporation, Embrapa Environment, Rodovia SP 340, Km 127.5, 13820-000 Jaguariúna, Brazil – sequence: 16 givenname: Gilles P orcidid: 0000-0003-0341-1561 surname: van Wezel fullname: van Wezel, Gilles P organization: Institute of Biology, Leiden University, Sylviusweg 72, 2333 BE Leiden, Netherlands – sequence: 17 givenname: Marnix H orcidid: 0000-0002-2191-2821 surname: Medema fullname: Medema, Marnix H email: j.raaijmakers@nioo.knaw.nl, marnix.medema@wur.nl organization: Bioinformatics Group, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, Netherlands. j.raaijmakers@nioo.knaw.nl marnix.medema@wur.nl – sequence: 18 givenname: Jos M orcidid: 0000-0003-1608-6614 surname: Raaijmakers fullname: Raaijmakers, Jos M email: j.raaijmakers@nioo.knaw.nl, marnix.medema@wur.nl organization: Institute of Biology, Leiden University, Sylviusweg 72, 2333 BE Leiden, Netherlands
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Copyright	Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works
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Snippet	Microorganisms living inside plants can promote plant growth and health, but their genomic and functional diversity remain largely elusive. Here, metagenomics... Some soils show a remarkable ability to suppress disease caused by plant pathogens, an ability that is attributed to plant-associated microbiota. Carrión et... Protecting plants from the inside outSome soils show a remarkable ability to suppress disease caused by plant pathogens, an ability that is attributed to...
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SubjectTerms	Antifungal activity Bacteria - classification Bacterial Physiological Phenomena Bacteroidetes - physiology Beta vulgaris - microbiology Biodiversity Cell walls Chitinase Chitinases - genetics Chitinophagaceae Consortia Disease Resistance Endophytes Endophytes - physiology Flavobacterium Flavobacterium - physiology Fungal diseases Fungi Fungicides Gene clusters Genes, Bacterial Genome, Bacterial Genomes Metabolites Metagenome Microbiomes Microbiota Microorganisms Mutagenesis, Site-Directed Pathogens Peptide Synthases - genetics Phenotypes Plant diseases Plant Diseases - microbiology Plant growth Plant protection Plant roots Plant Roots - microbiology Polyketide Synthases - genetics Polyketides Rhizoctonia - pathogenicity Rhizoctonia solani Roots Secondary metabolites Siderophores Site-directed mutagenesis Soil Microbiology Sugar beets Transcription Wilt
Title	Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome
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