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Transcriptomics reveal a mechanism of niche defense: two beneficial root endophytes deploy an antimicrobial GH18-CBM5 chitinase to protect their hosts

Journal Article · · New Phytologist
DOI:https://doi.org/10.1111/nph.20080· OSTI ID:2477365
 [1];  [2];  [1];  [1];  [2];  [3];  [4];  [4];  [5];  [5];  [5];  [5];  [5];  [6];  [2];  [4];  [1]
  1. Univ. of Cologne (Germany); Cluster of Excellence on Plant Sciences (CEPLAS), Cologne (Germany)
  2. Univ. of Cologne (Germany)
  3. Univ. of Cologne (Germany); Okinawa Institute of Science and Technology Graduate University (Japan)
  4. University of Münster (Germany)
  5. USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
  6. USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
Effector secretion is crucial for root endophytes to establish and protect their ecological niche. We used time-resolved transcriptomics to monitor effector gene expression dynamics in two closely related Sebacinales, Serendipita indica and Serendipita vermifera, during symbiosis with three plant species, competition with the phytopathogenic fungus Bipolaris sorokiniana, and cooperation with root-associated bacteria. We observed increased effector gene expression in response to biotic interactions, particularly with plants, indicating their importance in host colonization. Some effectors responded to both plants and microbes, suggesting dual roles in intermicrobial competition and plant–microbe interactions. A subset of putative antimicrobial effectors, including a GH18-CBM5 chitinase, was induced exclusively by microbes. Functional analyses of this chitinase revealed its antimicrobial and plant-protective properties. We conclude that dynamic effector gene expression underpins the ability of Sebacinales to thrive in diverse ecological niches with a single fungal chitinase contributing substantially to niche defense.
Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
2477365
Journal Information:
New Phytologist, Journal Name: New Phytologist Journal Issue: 3 Vol. 244; ISSN 0028-646X
Publisher:
WileyCopyright Statement
Country of Publication:
United States
Language:
English

References (89)

Serendipita indica chitinase protects rice from the blast and bakanae diseases journal April 2023
A proteomics approach to study synergistic and antagonistic interactions of the fungal–bacterial consortiumFusarium oxysporumwild‐type MSA 35 journal September 2010
Pairwise Transcriptomic Analysis of the Interactions Between the Ectomycorrhizal Fungus Laccaria bicolor S238N and Three Beneficial, Neutral and Antagonistic Soil Bacteria journal August 2014
Increased antifungal and chitinase specific activities of Trichoderma harzianum CECT 2413 by addition of a cellulose binding domain journal June 2004
The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms journal February 2008
Chitinolytic enzymes from endophytic fungi journal November 2010
Glycoside hydrolase family 18 chitinases: The known and the unknown journal November 2020
Suppression of Plant Immunity by Fungal Chitinase-like Effectors journal September 2018
Carbohydrate-binding modules of ChiB and ChiC promote the chitinolytic system of Serratia marcescens BWL1001 journal January 2023
Endochitinase 1 (Tv-ECH1) from Trichoderma virens has high subsite specificities for acetylated units when acting on chitosans journal July 2018
Improved Prediction of Signal Peptides: SignalP 3.0 journal July 2004
Mutualistic interactions on a knife-edge between saprotrophy and pathogenesis journal August 2011
Broad compatibility in fungal root symbioses journal August 2014
Understanding and exploiting plant beneficial microbes journal August 2017
Determinants of endophytic and pathogenic lifestyle in root colonizing fungi journal June 2022
Quantitative Mass-Spectrometric Sequencing of Chitosan Oligomers Revealing Cleavage Sites of Chitosan Hydrolases journal February 2017
Dual transcriptional profiling of a bacterial/fungal confrontation: Collimonas fungivorans versus Aspergillus niger journal May 2011
Stability and succession of the rhizosphere microbiota depends upon plant type and soil composition journal April 2015
Functional overlap of the Arabidopsis leaf and root microbiota journal December 2015
The fungal-specific β-glucan-binding lectin FGB1 alters cell-wall composition and suppresses glucan-triggered immunity in plants journal October 2016
Trichoderma: the genomics of opportunistic success journal September 2011
The fungal root endophyte Serendipita vermifera displays inter-kingdom synergistic beneficial effects with the microbiota in Arabidopsis thaliana and barley journal October 2021
Genetic determinants of endophytism in the Arabidopsis root mycobiome journal December 2021
Remote loop evolution reveals a complex biological function for chitinase enzymes beyond the active site journal April 2024
Microbiome manipulation by a soil-borne fungal plant pathogen using effector proteins journal November 2020
Plant–microbiome interactions: from community assembly to plant health journal August 2020
SignalP 5.0 improves signal peptide predictions using deep neural networks journal February 2019
SignalP 6.0 predicts all five types of signal peptides using protein language models journal January 2022
Fungal lifestyle reflected in serine protease repertoire journal August 2017
Bipolaris sorokiniana, a cereal pathogen of global concern: cytological and molecular approaches towards better control journal July 2002
The root endophytic fungus Piriformospora indica requires host cell death for proliferation during mutualistic symbiosis with barley journal November 2006
Costs and benefits of processivity in enzymatic degradation of recalcitrant polysaccharides journal November 2006
Host-related metabolic cues affect colonization strategies of a root endophyte journal August 2013
Structural insights into the catalytic mechanism of a family 18 exo-chitinase journal July 2001
Characterization of ech-42, a Trichoderma harzianum endochitinase gene expressed during mycoparasitism. journal November 1994
A family of genes required for maintenance of cell wall integrity and for the stress response in  Saccharomyces cerevisiae journal December 1997
Identification of a Chitinase-modifying Protein from Fusarium verticillioides : TRUNCATION OF A HOST RESISTANCE PROTEIN BY A FUNGALYSIN METALLOPROTEASE journal August 2011
Comparative metabolomic profiling reveals molecular mechanisms underlying growth promotion and disease resistance in wheat conferred by Piriformospora indica in the field journal May 2023
UpSetR: an R package for the visualization of intersecting sets and their properties journal June 2017
Microbiota manipulation through the secretion of effector proteins is fundamental to the wealth of lifestyles in the fungal kingdom journal May 2022
Characterization of the Wsc1 Protein, a Putative Receptor in the Stress Response of Saccharomyces cerevisiae journal August 1999
Fungi hijack a ubiquitous plant apoplastic endoglucanase to release a ROS scavenging β-glucan decasaccharide to subvert immune responses journal April 2022
Synergistic Action of a Metalloprotease and a Serine Protease from Fusarium oxysporum f. sp. lycopersici Cleaves Chitin-Binding Tomato Chitinases, Reduces Their Antifungal Activity, and Enhances Fungal Virulence journal September 2015
EffectorP 3.0: Prediction of Apoplastic and Cytoplasmic Effectors in Fungi and Oomycetes journal February 2022
Opprimo ergo sum —Evasion and Suppression in the Root Endophytic Fungus Piriformospora indica journal June 2012
Disruption of the ech42 (Endochitinase-Encoding) Gene Affects Biocontrol Activity in Trichoderma harzianum P1 journal May 1999
Plant-beneficial effects of Trichoderma and of its genes journal January 2012
Self versus non-self: fungal cell wall degradation in Trichoderma journal January 2012
Effector Biology of Plant-Associated Organisms: Concepts and Perspectives journal January 2012
Broad-Spectrum Suppression of Innate Immunity Is Required for Colonization of Arabidopsis Roots by the Fungus Piriformospora indica journal April 2011
The Mutualistic Fungus Piriformospora indica Colonizes Arabidopsis Roots by Inducing an Endoplasmic Reticulum Stress–Triggered Caspase-Dependent Cell Death journal February 2012
The local environment determines the assembly of root endophytic fungi at a continental scale: Continental-scale distribution of root endophytes journal December 2015
Fungal effector proteins: past, present and future journal November 2009
Indole derivative production by the root endophyte Piriformospora indica is not required for growth promotion but for biotrophic colonization of barley roots journal August 2012
Addition of substrate-binding domains increases substrate-binding capacity and specific activity of a chitinase fromTrichoderma harzianum journal April 2001
Degradation of chitosans with chitinase B from Serratia marcescens journal December 2004
Plant pathogen effector proteins as manipulators of host microbiomes? journal January 2018
Improved prediction of fungal effector proteins from secretomes with EffectorP 2.0: Prediction of fungal effectors with EffectorP 2.0 journal May 2018
Mutualistic root endophytism is not associated with the reduction of saprotrophic traits and requires a noncompromised plant innate immunity journal April 2015
E ffector P: predicting fungal effector proteins from secretomes using machine learning journal December 2015
Facultative root-colonizing fungi dominate endophytic assemblages in roots of nonmycorrhizal Microthlaspi species journal November 2017
ApoplastP : prediction of effectors and plant proteins in the apoplast using machine learning journal December 2017
The origin and evolution of mycorrhizal symbioses: from palaeomycology to phylogenomics journal March 2018
FGB1 and WSC3 are in planta‐ induced β ‐glucan‐binding fungal lectins with different functions journal February 2019
The inconspicuous gatekeeper: endophytic Serendipita vermifera acts as extended plant protection barrier in the rhizosphere journal June 2019
A secreted fungal histidine‐ and alanine‐rich protein regulates metal ion homeostasis and oxidative stress journal May 2020
A highly polymorphic effector protein promotes fungal virulence through suppression of plant‐associated Actinobacteria journal November 2022
Metatranscriptomics sheds light on the links between the functional traits of fungal guilds and ecological processes in forest soil ecosystems journal December 2023
Structure and Function of a Novel LD-Carboxypeptidase A Involved in Peptidoglycan Recycling journal October 2013
Chitosan and Chitin Deacetylase Activity Are Necessary for Development and Virulence of Ustilago maydis journal April 2021
Fungal Effectors and Plant Susceptibility journal April 2015
Accurate plant pathogen effector protein classification ab initio with deepredeff: an ensemble of convolutional neural networks journal July 2021
Host-specific transcriptomic pattern of Trichoderma virens during interaction with maize or tomato roots journal January 2015
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 journal December 2014
Endophytic Life Strategies Decoded by Genome and Transcriptome Analyses of the Mutualistic Root Symbiont Piriformospora indica journal October 2011
The Ustilago maydis Effector Pep1 Suppresses Plant Immunity by Inhibition of Host Peroxidase Activity journal May 2012
Serendipita indica E5′ NT modulates extracellular nucleotide levels in the plant apoplast and affects fungal colonization journal February 2019
Co‐evolution within the plant holobiont drives host performance journal July 2023
Transcriptomic Response of Fusarium verticillioides to Variably Inhibitory Environmental Isolates of Streptomyces journal July 2022
Comparative Analysis of Secretomes from Ectomycorrhizal Fungi with an Emphasis on Small-Secreted Proteins journal November 2015
Beneficial Endophytic Bacteria-Serendipita indica Interaction for Crop Enhancement and Resistance to Phytopathogens journal December 2019
The battle in the apoplast: further insights into the roles of proteases and their inhibitors in plant–pathogen interactions journal August 2015
The Piriformospora indica effector PIIN_08944 promotes the mutualistic Sebacinalean symbiosis journal October 2015
Transcriptome Profiling Reveals Differential Gene Expression of Secreted Proteases and Highly Specific Gene Repertoires Involved in Lactarius–Pinus Symbioses journal August 2021
The Root-Colonizing Endophyte Piriformospora indica Supports Nitrogen-Starved Arabidopsis thaliana Seedlings with Nitrogen Metabolites journal October 2023
A Transcriptomic Approach Provides Insights on the Mycorrhizal Symbiosis of the Mediterranean Orchid Limodorum abortivum in Nature journal January 2021
The Magas1 Gene is Involved in Pathogenesis by Affecting Penetration in Metarhizium acridum journal July 2012
Comparative Molecular Evolution of Trichoderma Chitinases in Response to Mycoparasitic Interactions journal January 2010
Plant and fungal gene expression in mycorrhizal protocorms of the orchidSerapias vomeraceacolonized byTulasnella calospora journal November 2014

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