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Title: The small secreted effector protein MiSSP7.6 of Laccaria bicolor is required for the establishment of ectomycorrhizal symbiosis

Journal Article · · Environmental Microbiology
ORCiD logo [1];  [2];  [3];  [3]; ORCiD logo [4];  [4];  [4]
  1. College of Plant Science and Technology, Huazhong Agricultural University Wuhan 430070 China, University of Lorraine, Institut National de la Recherche Agronomique, UMR Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, Centre INRA‐Grand Est Champenoux France
  2. College of Plant Science and Technology, Huazhong Agricultural University Wuhan 430070 China
  3. Laboratorio de Micología Molecular, Instituto de Microbiología Básica y Aplicada, Departamento de Ciencia y Tecnología, Universidad Nacional de Quilmes and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) Bernal Provincia de Buenos Aires Argentina
  4. University of Lorraine, Institut National de la Recherche Agronomique, UMR Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, Centre INRA‐Grand Est Champenoux France

Summary To establish and maintain a symbiotic relationship, the ectomycorrhizal fungus Laccaria bicolor releases mycorrhiza‐induced small secreted proteins (MiSSPs) into host roots. Here, we have functionally characterized the M YCORRHIZA‐ i NDUCED S MALL S ECRETED P ROTEIN OF 7 . 6 kDa ( MiSSP7 . 6 ) from L . bicolor by assessing its induced expression in ectomycorrhizae, silencing its expression by RNAi, and tracking in planta subcellular localization of its protein product. We also carried out yeast two‐hybrid assays and bimolecular fluorescence complementation analysis to identify possible protein targets of the MiSSP7.6 effector in Populus roots. We showed that MiSSP7 . 6 expression is upregulated in ectomycorrhizal rootlets and associated extramatrical mycelium during the late stage of symbiosis development. RNAi mutants with a decreased MiSSP7 . 6 expression have a lower mycorrhization rate , suggesting a key role in the establishment of the symbiosis with plants. MiSSP7.6 is secreted, and it localizes both to the nuclei and cytoplasm in plant cells. MiSSP7.6 protein was shown to interact with two Populus Trihelix transcription factors. Furthermore, when coexpressed with one of the Trihelix transcription factors, MiSSP7.6 is localized to plant nuclei only. Our data suggest that MiSSP7.6 is a novel secreted symbiotic effector and is a potential determinant for ectomycorrhiza formation.

Sponsoring Organization:
USDOE
OSTI ID:
1602327
Journal Information:
Environmental Microbiology, Journal Name: Environmental Microbiology Journal Issue: 4 Vol. 22; ISSN 1462-2912
Publisher:
Wiley-BlackwellCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (32)

High-Throughput Yeast Two-Hybrid Assays for Large-Scale Protein Interaction Mapping journal July 2001
Agrobacterium-mediated transformation of the ectomycorrhizal symbiont Laccaria bicolor S238N journal August 2005
GATEWAY™ vectors for Agrobacterium-mediated plant transformation journal May 2002
A Secreted Effector Protein of Laccaria bicolor Is Required for Symbiosis Development journal July 2011
Lineages of ectomycorrhizal fungi revisited: Foraging strategies and novel lineages revealed by sequences from belowground journal December 2013
Improved vectors for Agrobacterium mediated genetic manipulation of Hypholoma spp. and other homobasidiomycetes journal November 2017
Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists journal February 2015
NIH Image to ImageJ: 25 years of image analysis journal June 2012
High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method journal January 2007
Unearthing the roots of ectomycorrhizal symbioses journal October 2016
Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants journal March 2013
Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes journal May 2014
New GATEWAY vectors for High Throughput Analyses of Protein–Protein Interactions by Bimolecular Fluorescence Complementation journal September 2009
A new mathematical model for relative quantification in real-time RT-PCR journal May 2001
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 Fungus Laccaria bicolor Stimulates Lateral Root Formation in Poplar and Arabidopsis through Auxin Transport and Signaling journal October 2009
Development of the Poplar -Laccaria bicolor Ectomycorrhiza Modifies Root Auxin Metabolism, Signaling, and Response journal June 2015
Phosphorylation of Trihelix Transcriptional Repressor ASR3 by MAP KINASE4 Negatively Regulates Arabidopsis Immunity journal March 2015
The ectomycorrhizal basidiomycete Hebeloma cylindrosporum undergoes early waves of transcriptional reprogramming prior to symbiotic structures differentiation: Hebeloma cylindrosporum pre-infectious transcriptome journal February 2017
Laccaria bicolor MiSSP8 is a small‐secreted protein decisive for the establishment of the ectomycorrhizal symbiosis journal July 2019
Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta journal November 2008
New Phytologist ? an evolving host for mycorrhizal research journal April 2007
pHg/pSILBAγ vector system for efficient gene silencing in homobasidiomycetes: optimization of ihpRNA - triggering in the mycorrhizal fungus Laccaria bicolor journal March 2010
A MYB coiled-coil transcription factor interacts with NSP2 and is involved in nodulation in Lotus japonicus journal November 2013
Mycorrhizal ecology and evolution: the past, the present, and the future journal February 2015
The ectomycorrhizal basidiomycete Laccaria bicolor releases a secreted β-1,4 endoglucanase that plays a key role in symbiosis development journal April 2018
Comparative genomics reveals unique wood‐decay strategies and fruiting body development in the Schizophyllaceae journal June 2019
Predicting coiled coils from protein sequences journal May 1991
Arabidopsis Transcription Factors: Genome-Wide Comparative Analysis Among Eukaryotes journal December 2000
A Fruiting Body Tissue Method for Efficient Agrobacterium-Mediated Transformation of Agaricus bisporus journal October 2000
Recent Insights on Biological and Ecological Aspects of Ectomycorrhizal Fungi and Their Interactions journal February 2018
Poplar root exudates contain compounds that induce the expression of MiSSP7 in Laccaria bicolor journal January 2012