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Title: Regulatory networks underlying mycorrhizal development delineated by genome-wide expression profiling and functional analysis of the transcription factor repertoire of the plant symbiotic fungus Laccaria bicolor

Journal Article · · BMC Genomics
 [1];  [2];  [1];  [1];  [1];  [1];  [2];  [2];  [1];  [1];  [1]
  1. Univ. de Lorraine, Champenoux (France). Interactions Arbres/ Microorganismes, Laboratoire d’Excellence ARBRE; Univ. de Lorraine, Nancy (France). Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE
  2. Univ. degli Studi di Parma (Italy). Dipartimento di Scienze Chimiche, della Vita e della Sostenibilità Ambientale

Background: Ectomycorrhizal (ECM) fungi develop a mutualistic symbiotic interaction with the roots of their host plants. During this process, they undergo a series of developmental transitions from the running hyphae in the rhizosphere to the coenocytic hyphae forming finger-like structures within the root apoplastic space. These transitions, which involve profound, symbiosis-associated metabolic changes, also entail a substantial transcriptome reprogramming with coordinated waves of differentially expressed genes. To date, little is known about the key transcriptional regulators driving these changes, and the aim of the present study was to delineate and functionally characterize the transcription factor (TF) repertoire of the model ECM fungus Laccaria bicolor. Results: We curated the L. bicolor gene models coding for transcription factors and assessed their expression and regulation in Poplar and Douglas fir ectomycorrhizae. We identified 285 TFs, 191 of which share a significant similarity with known transcriptional regulators. Expression profiling of the corresponding transcripts identified TF-encoding fungal genes differentially expressed in the ECM root tips of both host plants. The L. bicolor core set of differentially expressed TFs consists of 12 and 22 genes that are, respectively, upregulated and downregulated in symbiotic tissues. These TFs resemble known fungal regulators involved in the control of fungal invasive growth, fungal cell wall integrity, carbon and nitrogen metabolism, invasive stress response and fruiting-body development. However, this core set of mycorrhiza-regulated TFs seems to be characteristic of L. bicolor and our data suggest that each mycorrhizal fungus has evolved its own set of ECM development regulators. A subset of the above TFs was functionally validated with the use of a heterologous, transcription activation assay in yeast, which also allowed the identification of previously unknown, transcriptionally active yet secreted polypeptides designated as Secreted Transcriptional Activator Proteins (STAPs). Conclusions: Transcriptional regulators required for ECM symbiosis development in L. bicolor have been uncovered and classified through genome-wide analysis. This study also identifies the STAPs as a new class of potential ECM effectors, highly expressed in mycorrhizae, which may be involved in the control of the symbiotic root transcriptome.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Organization:
USDOE Office of Science (SC)
Grant/Contract Number:
AC05-00OR22725
OSTI ID:
1626809
Journal Information:
BMC Genomics, Vol. 18, Issue 1; ISSN 1471-2164
Publisher:
SpringerCopyright Statement
Country of Publication:
United States
Language:
English

References (69)

The Mutualist Laccaria bicolor Expresses a Core Gene Regulon During the Colonization of Diverse Host Plants and a Variable Regulon to Counteract Host-Specific Defenses journal March 2015
The Ectomycorrhizal Infection zone and its Relation to acid Polysaccharides of Cortical cell Walls journal May 1987
Transcription factor genes of Schizophyllum commune involved in regulation of mushroom formation: Regulation of mushroom formation journal August 2011
The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis journal March 2008
Yeast RLM1 encodes a serum response factor-like protein that may function downstream of the Mpk1 (Slt2) mitogen-activated protein kinase pathway. journal October 1995
Insights into evolution of multicellular fungi from the assembled chromosomes of the mushroom Coprinopsis cinerea (Coprinus cinereus) journal June 2010
Profiling the Human Protein-DNA Interactome Reveals ERK2 as a Transcriptional Repressor of Interferon Signaling journal October 2009
Transcriptional activators in yeast journal February 2006
The acetate regulatory gene facB of Aspergillus nidulans encodes a Zn(II)2Cys6 transcriptional activator journal May 1997
H2O2 sensing through oxidation of the Yap1 transcription factor journal October 2000
Genome-wide search and functional identification of transcription factors in the mycorrhizal fungus Tuber melanosporum journal November 2010
Metabolic enzymes and coenzymes in transcription – a direct link between metabolism and transcription? journal September 2004
MADS-Box Transcription Factor Mig1 Is Required for Infectious Growth in Magnaporthe grisea journal March 2008
Mycorrhizal ecology and evolution: the past, the present, and the future journal February 2015
Phylogenetic, genomic organization and expression analysis of hydrophobin genes in the ectomycorrhizal basidiomycete Laccaria bicolor journal March 2012
The Aspergillus nidulans abaA gene encodes a transcriptional activator that acts as a genetic switch to control development. journal April 1994
Dry and wet approaches for genome-wide functional annotation of conventional and unconventional transcriptional activators journal January 2016
Moonlighting transcriptional activation function of a fungal sulfur metabolism enzyme journal April 2016
Ontogeny of Alnus rubraAlpova diplophloeus ectomycorrhizae. I. Light microscopy and scanning electron microscopy journal January 1989
A Secreted Effector Protein of Laccaria bicolor Is Required for Symbiosis Development journal July 2011
Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis journal March 2010
Prevalence of transcription factors in ascomycete and basidiomycete fungi journal January 2014
Tapping Genomics to Unravel Ectomycorrhizal Symbiosis book January 2011
Ectomycorrhizal ecology is imprinted in the genome of the dominant symbiotic fungus Cenococcum geophilum journal September 2016
Coevolution of roots and mycorrhizas of land plants journal May 2002
The pheromone response factor coordinates filamentous growth and pathogenicity in Ustilago maydis. journal April 1996
CreA influences the metabolic fluxes of Aspergillus nidulans during growth on glucose and xylose journal July 2005
MpkA-Dependent and -Independent Cell Wall Integrity Signaling in Aspergillus nidulans journal June 2007
Regulation of the yeast Rlm1 transcription factor by the Mpk1 cell wall integrity MAP kinase: Reporters for cell wall integrity signalling journal October 2002
A new mathematical model for relative quantification in real-time RT-PCR journal May 2001
FAR1 and FAR2 Regulate the Expression of Genes Associated with Lipid Metabolism in the Rice Blast Fungus Magnaporthe oryzae journal June 2014
Lateral root stimulation in the early interaction between Arabidopsis thaliana and the ectomycorrhizal fungus Laccaria bicolor : Is fungal auxin the trigger? journal July 2010
A regulator gene for acetate utilisation from Neurospora crassa journal June 2002
The Ectomycorrhizal Symbiosis: a Marriage of Convenience book January 2009
Spatial patterns of gene expression in the extramatrical mycelium and mycorrhizal root tips formed by the ectomycorrhizal fungus Paxillus involutus in association with birch (Betula pendula) seedlings in soil microcosms journal April 2005
Pseudohyphal Regulation by the Transcription Factor Rfg1p in Candida albicans journal July 2010
Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes journal May 2014
Modification of the Host-Fungus Interface in Mycorrhizas Synthesized Between Suillus Bovjnus (Fr.) o. Kuntz and Pinus Sylvestris l. journal April 1984
Comparative genomics and expression levels of hydrophobins from eight mycorrhizal genomes journal January 2017
The major pathways of carbohydrate metabolism in the ectomycorrhizal basidiomycete Laccaria bicolor S238N journal October 2008
Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists journal February 2015
Genomic and transcriptomic analysis of Laccaria bicolor CAZome reveals insights into polysaccharides remodelling during symbiosis establishment journal November 2014
Regulatory roles for the homeodomain and C2H2 zinc finger regions of Cryptococcus neoformans Ste12αp: Roles of the homeodomain and C2H2 zinc fingers of Ste12απ journal August 2004
The Ectomycorrhizal Fungus Laccaria bicolor Stimulates Lateral Root Formation in Poplar and Arabidopsis through Auxin Transport and Signaling journal October 2009
Transcriptional Responses of Paxillus involutus and Betula pendula During Formation of Ectomycorrhizal Root Tissue journal February 2004
Gcn4 co-ordinates morphogenetic and metabolic responses to amino acid starvation in Candida albicans journal October 2002
Global Patterns of Gene Regulation Associated with the Development of Ectomycorrhiza Between Birch ( Betula pendula Roth.) and Paxillus involutus (Batsch) Fr. journal July 2005
Variation in mycorrhizal development and growth stimulation by 20 Pisolithus isolates inoculated on to Eucalyptus grandis W. Hill ex Maiden journal August 1994
Transcript patterns associated with ectomycorrhiza development in Eucalyptus globulus and Pisolithus microcarpus journal November 2004
Mycorrhizas and nutrient cycling in ecosystems - a journey towards relevance? journal March 2003
NAC transcription factors: structurally distinct, functionally diverse journal February 2005
Development of the Poplar -Laccaria bicolor Ectomycorrhiza Modifies Root Auxin Metabolism, Signaling, and Response journal June 2015
Moc3, a novel Zn finger type protein involved in sexual development, ascus formation, and stress response of Schizosaccharomyces pombe journal November 2005
Structure and ontogeny of Betula alleghaniensisPisolithus tinctorius ectomycorrhizae journal March 1990
Ontogeny of Eucalyptus pilularisPisolithus tinctorius ectomycorrhizae. I. Light microscopy and scanning electron microscopy journal September 1987
The MADS-Box transcription factor Bcmads1 is required for growth, sclerotia production and pathogenicity of Botrytis cinerea journal September 2016
Ontogeny of Eucalyptus pilularisPisolithus tinctorius ectomycorrhizae. II. Transmission electron microscopy journal September 1987
The ectomycorrhizal basidiomycete Hebeloma cylindrosporum undergoes early waves of transcriptional reprogramming prior to symbiotic structures differentiation: Hebeloma cylindrosporum pre-infectious transcriptome journal February 2017
Using next generation transcriptome sequencing to predict an ectomycorrhizal metabolome journal January 2011
Regulation of Gene Expression by a Metabolic Enzyme journal October 2004
Structure and ontogeny of Alnus crispaAlpova diplophloeus ectomycorrhizae journal January 1986
The R2R3-MYB gene family in Arabidopsis thaliana journal October 2001
Ste12 and Ste12-Like Proteins, Fungal Transcription Factors Regulating Development and Pathogenicity journal February 2010
Proteomic analyses reveal the key roles of BrlA and AbaA in biogenesis of gliotoxin in Aspergillus fumigatus journal July 2015
Laser Capture Microdissection of Uredinia Formed by Melampsora larici-populina Revealed a Transcriptional Switch Between Biotrophy and Sporulation journal October 2010
Unearthing the roots of ectomycorrhizal symbioses journal October 2016
The Ectomycorrhizal Infection zone and its Relation to acid Polysaccharides of Cortical cell Walls journal July 1987
Integrated analyses of the transcriptome and small RNA of the hemiparasitic plant Monochasma savatieri before and after establishment of parasite-host association journal February 2021
The Aspergillus nidulans abaA gene encodes a transcriptional activator that acts as a genetic switch to control development journal April 1994