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Title: Expanding the Biological Role of Lipo-Chitooligosaccharides and Chitooligosaccharides in Laccaria bicolor Growth and Development

Journal Article · · Frontiers in Fungal Biology

The role of lipo-chitooligosaccharides (LCOs) as signaling molecules that mediate the establishment of symbiotic relationships between fungi and plants is being redefined. New evidence suggests that the production of these molecular signals may be more of a common trait in fungi than what was previously thought. LCOs affect different aspects of growth and development in fungi. For the ectomycorrhizal forming fungi, Laccaria bicolor, the production and effects of LCOs have always been studied with a symbiotic plant partner; however, there is still no scientific evidence describing the effects that these molecules have on this organism. Here, we explored the physiological, molecular, and metabolomic changes in L. bicolor when grown in the presence of exogenous sulfated and non-sulfated LCOs, as well as the chitooligomers, chitotetraose (CO4), and chitooctaose (CO8). Physiological data from 21 days post-induction showed reduced fungal growth in response to CO and LCO treatments compared to solvent controls. The underlying molecular changes were interrogated by proteomics, which revealed substantial alterations to biological processes related to growth and development. Moreover, metabolite data showed that LCOs and COs caused a downregulation of organic acids, sugars, and fatty acids. At the same time, exposure to LCOs resulted in the overproduction of lactic acid in L. bicolor. Altogether, these results suggest that these signals might be fungistatic compounds and contribute to current research efforts investigating the emerging impacts of these molecules on fungal growth and development.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Organization:
National Science Foundation (NSF); USDA; USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC05-00OR22725
OSTI ID:
1845783
Journal Information:
Frontiers in Fungal Biology, Journal Name: Frontiers in Fungal Biology Journal Issue: 1 Vol. 3; ISSN 2673-6128
Publisher:
Frontiers Media S.A.Copyright Statement
Country of Publication:
United States
Language:
English

References (92)

Organic acids in root exudates from Picea abies seedlings influenced by mycorrhiza and aluminum journal October 2007
Autophagy-related gene ATG7 participates in the asexual development, stress response and virulence of filamentous insect pathogenic fungus Beauveria bassiana journal March 2019
The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility journal January 2003
Effect of l-lactic acid from whey wastes on enzyme activities and bacterial diversity of soil journal February 2017
A ras homologue of Neurospora crassa regulates morphology journal April 1997
A Ras protein from a phytopathogenic fungus causes defects in hyphal growth polarity, and induces tumors in mice journal August 1999
Multiple roles of a putative vacuolar protein sorting associated protein 74, FgVPS74, in the cereal pathogen Fusarium graminearum journal April 2015
Quo vadis: signaling molecules and small secreted proteins from mycorrhizal fungi at the early stage of mycorrhiza formation journal July 2021
Kinesin and dynein mutants provide novel insights into the roles of vesicle traffic during cell morphogenesis in Neurospora journal August 1999
The effects of ropy-1 mutation on cytoplasmic organization and intracellular motility in mature hyphae of Neurospora crassa journal November 2002
Cell cycle control of yeast filamentous growth journal December 2001
Development by Self-Digestion journal April 2004
New insights into Nod factor biosynthesis: Analyses of chitooligomers and lipo-chitooligomers of Rhizobium sp. IRBG74 mutants journal November 2016
Understanding the Arbuscule at the Heart of Endomycorrhizal Symbioses in Plants journal September 2017
Regulation of low-molecular weight organic acid production in fungi journal February 2009
Nuclear migration and positioning in filamentous fungi journal April 2004
Autophagy in filamentous fungi journal January 2009
Eliminating a global regulator of carbon catabolite repression enhances the conversion of aromatic lignin monomers to muconate in Pseudomonas putida KT2440 journal December 2017
Nod factors stimulate seed germination and promote growth and nodulation of pea and vetch under competitive conditions journal March 2012
Quantitative analysis of exudates from soil-living basidiomycetes in pure culture as a response to lead, cadmium and arsenic stress journal September 2008
Crystal Structures of Fungal Tectonin in Complex with O-Methylated Glycans Suggest Key Role in Innate Immune Defense journal March 2018
Fungal behaviour: a new frontier in behavioural ecology journal September 2021
Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal journal April 1990
The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis journal March 2008
Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza journal January 2011
Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis journal July 2010
The Perseus computational platform for comprehensive analysis of (prote)omics data journal June 2016
Semi-supervised learning for peptide identification from shotgun proteomics datasets journal October 2007
Transcript, protein and metabolite temporal dynamics in the CAM plant Agave journal November 2016
Autophagy: from phenomenology to molecular understanding in less than a decade journal November 2007
A combination of chitooligosaccharide and lipochitooligosaccharide recognition promotes arbuscular mycorrhizal associations in Medicago truncatula journal November 2019
Lipo-chitooligosaccharides as regulatory signals of fungal growth and development journal August 2020
SignalP 5.0 improves signal peptide predictions using deep neural networks journal February 2019
Terpene Synthase Genes Originated from Bacteria through Horizontal Gene Transfer Contribute to Terpenoid Diversity in Fungi journal June 2019
The mutualism effector MiSSP7 of Laccaria bicolor alters the interactions between the poplar JAZ6 protein and its associated proteins journal November 2020
Molecular basis of lipo-chitooligosaccharide recognition by the lysin motif receptor-like kinase LYR3 in legumes journal May 2016
Lipids in roots of Pinus sylvestris seedlings and in mycelia of Pisolithus tinctorius during ectomycorrhiza formation: changes in fatty acid and sterol composition journal January 2004
Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes journal May 2014
Methylated glycans as conserved targets of animal and fungal innate defense journal May 2014
The Autolysis of Industrial Filamentous Fungi journal January 2002
Perception of lipo-chitooligosaccharides by the bioenergy crop Populus journal April 2021
Regulation of small GTPase activity by G1 cyclins journal January 2017
DAnTE: a statistical tool for quantitative analysis of -omics data journal May 2008
ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks journal February 2009
Nod factor structures, responses, and perception during initiation of nodule development journal June 2002
Effect of lipo-chitooligosaccharide on early growth of C 4 grass seedlings journal June 2015
Transient Cytoplasmic pH Change and Ion Fluxes through the Plasma Memberan in Suspension-Cultured Rice Cells Triggered by N-Acetylchitooligosaccharide Elicitor journal January 1997
Germinating Spore Exudates from Arbuscular Mycorrhizal Fungi: Molecular and Developmental Responses in Plants and Their Regulation by Ethylene journal February 2011
Populus trichocarpa and Populus deltoides Exhibit Different Metabolomic Responses to Colonization by the Symbiotic Fungus Laccaria bicolor journal June 2014
Characterizing the Effect of Foliar Lipo-chitooligosaccharide Application on Sudden Death Syndrome and Sclerotinia Stem Rot in Soybean journal January 2018
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks journal November 2003
Control of Yeast Filamentous-Form Growth by Modules in an Integrated Molecular Network journal March 2004
Activation of Symbiosis Signaling by Arbuscular Mycorrhizal Fungi in Legumes and Rice journal February 2015
Plant Signaling and Metabolic Pathways Enabling Arbuscular Mycorrhizal Symbiosis journal August 2017
The Ectomycorrhizal Fungus Laccaria bicolor Produces Lipochitooligosaccharides and Uses the Common Symbiosis Pathway to Colonize Populus Roots journal August 2019
Laccaria bicolor MiSSP8 is a small‐secreted protein decisive for the establishment of the ectomycorrhizal symbiosis journal July 2019
The small secreted effector protein MiSSP7.6 of Laccaria bicolor is required for the establishment of ectomycorrhizal symbiosis journal April 2020
Surveying purine biosynthesis across the domains of life unveils promising drug targets in pathogens journal September 2020
Polarized growth in fungi – interplay between the cytoskeleton, positional markers and membrane domains journal May 2008
The Laccaria genome: a symbiont blueprint decoded journal October 2008
Fatty acid metabolism in the ectomycorrhizal fungus Laccaria bicolor journal March 2009
Arbuscular mycorrhizal hyphopodia and germinated spore exudates trigger Ca2+ spiking in the legume and nonlegume root epidermis journal September 2010
Metal-chelating compounds produced by ectomycorrhizal fungi collected from pine plantations journal January 2007
Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca 2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone journal February 2013
The LysM receptor-like kinase SlLYK10 regulates the arbuscular mycorrhizal symbiosis in tomato journal November 2015
Biology and evolution of arbuscular mycorrhizal symbiosis in the light of genomics journal October 2016
An endophytic Fusarium –legume association is partially dependent on the common symbiotic signalling pathway journal March 2020
Know your enemy, embrace your friend: using omics to understand how plants respond differently to pathogenic and mutualistic microorganisms journal January 2018
How mycorrhizal associations drive plant population and community biology journal February 2020
Control of Saccharomyces cerevisiae Filamentous Growth by Cyclin-Dependent Kinase Cdc28 journal February 1999
A G 1 Cyclin Is Necessary for Maintenance of Filamentous Growth in Candida albicans journal June 1999
Crk1, a Novel Cdc2-Related Protein Kinase, Is Required for Hyphal Development and Virulence in Candida albicans journal December 2000
Central Roles of Small GTPases in the Development of Cell Polarity in Yeast and Beyond journal March 2007
Cdc42: An Essential Rho-Type GTPase Controlling Eukaryotic Cell Polarity journal March 1999
Organic acid exudation by Laccaria bicolor and Pisolithus tinctorius exposed to aluminum in vitro journal April 2001
The Structure, Distribution, and Biomass of the World's Forests journal November 2013
Deciphering the Chitin Code in Plant Symbiosis, Defense, and Microbial Networks journal October 2021
Mechanisms Underlying Establishment of Arbuscular Mycorrhizal Symbioses journal August 2018
Rhizobium Lipo-Chitooligosaccharide Nodulation Factors: Signaling Molecules Mediating Recognition and Morphogenesis journal June 1996
Plants, Mycorrhizal Fungi, and Bacteria: A Network of Interactions journal October 2009
Exploring fungal biodiversity: organic acid production by 66 strains of filamentous fungi journal November 2014
Cytoplasmic dynein in fungi: insights from nuclear migration journal November 2003
Comparative Genome Analysis of Filamentous Fungi Reveals Gene Family Expansions Associated with Fungal Pathogenesis journal June 2008
Systems Approaches to Predict the Functions of Glycoside Hydrolases during the Life Cycle of Aspergillus niger Using Developmental Mutants ∆brlA and ∆flbA journal January 2015
Nudix Effectors: A Common Weapon in the Arsenal of Plant Pathogens journal August 2016
tRNAs as regulators of biological processes journal June 2014
DiVenn: An Interactive and Integrated Web-Based Visualization Tool for Comparing Gene Lists journal May 2019
Newly identified helper bacteria stimulate ectomycorrhizal formation in Populus journal October 2014
Chitin Oligosaccharide and Chitosan Oligosaccharide: Two Similar but Different Plant Elicitors journal April 2016
LysM Receptor-Like Kinase and LysM Receptor-Like Protein Families: An Update on Phylogeny and Functional Characterization journal October 2018
Rhizospheric Organic Acids as Biostimulants: Monitoring Feedbacks on Soil Microorganisms and Biochemical Properties journal May 2020
Symbiotic Activity of Pea (Pisum sativum) after Application of Nod Factors under Field Conditions journal April 2014