The small secreted effector protein MiSSP7.6 of Laccaria bicolor is required for the establishment of ectomycorrhizal symbiosis
Abstract
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 secretedmore »
- Authors:
-
- 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
- College of Plant Science and Technology, Huazhong Agricultural University Wuhan 430070 China
- 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
- University of Lorraine, Institut National de la Recherche Agronomique, UMR Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, Centre INRA‐Grand Est Champenoux France
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1602327
- Resource Type:
- Publisher's Accepted Manuscript
- Journal Name:
- Environmental Microbiology
- Additional Journal Information:
- Journal Name: Environmental Microbiology Journal Volume: 22 Journal Issue: 4; Journal ID: ISSN 1462-2912
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
Kang, Heng, Chen, Xin, Kemppainen, Minna, Pardo, Alejandro G., Veneault‐Fourrey, Claire, Kohler, Annegret, and Martin, Francis M. The small secreted effector protein MiSSP7.6 of Laccaria bicolor is required for the establishment of ectomycorrhizal symbiosis. United Kingdom: N. p., 2020.
Web. doi:10.1111/1462-2920.14959.
Kang, Heng, Chen, Xin, Kemppainen, Minna, Pardo, Alejandro G., Veneault‐Fourrey, Claire, Kohler, Annegret, & Martin, Francis M. The small secreted effector protein MiSSP7.6 of Laccaria bicolor is required for the establishment of ectomycorrhizal symbiosis. United Kingdom. https://doi.org/10.1111/1462-2920.14959
Kang, Heng, Chen, Xin, Kemppainen, Minna, Pardo, Alejandro G., Veneault‐Fourrey, Claire, Kohler, Annegret, and Martin, Francis M. Mon .
"The small secreted effector protein MiSSP7.6 of Laccaria bicolor is required for the establishment of ectomycorrhizal symbiosis". United Kingdom. https://doi.org/10.1111/1462-2920.14959.
@article{osti_1602327,
title = {The small secreted effector protein MiSSP7.6 of Laccaria bicolor is required for the establishment of ectomycorrhizal symbiosis},
author = {Kang, Heng and Chen, Xin and Kemppainen, Minna and Pardo, Alejandro G. and Veneault‐Fourrey, Claire and Kohler, Annegret and Martin, Francis M.},
abstractNote = {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.},
doi = {10.1111/1462-2920.14959},
journal = {Environmental Microbiology},
number = 4,
volume = 22,
place = {United Kingdom},
year = {Mon Mar 02 00:00:00 EST 2020},
month = {Mon Mar 02 00:00:00 EST 2020}
}
https://doi.org/10.1111/1462-2920.14959
Web of Science
Works referenced in this record:
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
- Plett, Jonathan M.; Tisserant, Emilie; Brun, Annick
- Molecular Plant-Microbe Interactions, Vol. 28, Issue 3
Lineages of ectomycorrhizal fungi revisited: Foraging strategies and novel lineages revealed by sequences from belowground
journal, December 2013
- Tedersoo, Leho; Smith, Matthew E.
- Fungal Biology Reviews, Vol. 27, Issue 3-4
New GATEWAY vectors for High Throughput Analyses of Protein–Protein Interactions by Bimolecular Fluorescence Complementation
journal, September 2009
- Gehl, Christian; Waadt, Rainer; Kudla, Jörg
- Molecular Plant, Vol. 2, Issue 5
Comparative genomics reveals unique wood‐decay strategies and fruiting body development in the Schizophyllaceae
journal, June 2019
- Almási, Éva; Sahu, Neha; Krizsán, Krisztina
- New Phytologist, Vol. 224, Issue 2
Improved vectors for Agrobacterium mediated genetic manipulation of Hypholoma spp. and other homobasidiomycetes
journal, November 2017
- Al-Salihi, Suhad A. A.; Scott, Thomas A.; Bailey, Andy M.
- Journal of Microbiological Methods, Vol. 142
pHg/pSILBAγ vector system for efficient gene silencing in homobasidiomycetes: optimization of ihpRNA - triggering in the mycorrhizal fungus Laccaria bicolor
journal, March 2010
- Kemppainen, Minna J.; Pardo, Alejandro G.
- Microbial Biotechnology, Vol. 3, Issue 2
Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes
journal, May 2014
- Plett, J. M.; Daguerre, Y.; Wittulsky, S.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 22
Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants
journal, March 2013
- Oldroyd, Giles E. D.
- Nature Reviews Microbiology, Vol. 11, Issue 4
New Phytologist ? an evolving host for mycorrhizal research
journal, April 2007
- Martin, Francis; Slater, Holly
- New Phytologist, Vol. 174, Issue 2
Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists
journal, February 2015
- Kohler, Annegret; Kuo, Alan; Nagy, Laszlo G.
- Nature Genetics, Vol. 47, Issue 4
Arabidopsis Transcription Factors: Genome-Wide Comparative Analysis Among Eukaryotes
journal, December 2000
- Riechmann, J. L.; Heard, J.; Martin, G.
- Science, Vol. 290, Issue 5499
Mycorrhizal ecology and evolution: the past, the present, and the future
journal, February 2015
- van der Heijden, Marcel G. A.; Martin, Francis M.; Selosse, Marc-André
- New Phytologist, Vol. 205, Issue 4
A MYB coiled-coil transcription factor interacts with NSP2 and is involved in nodulation in Lotus japonicus
journal, November 2013
- Kang, Heng; Chu, Xiaojie; Wang, Chao
- New Phytologist, Vol. 201, Issue 3
Agrobacterium-mediated transformation of the ectomycorrhizal symbiont Laccaria bicolor S238N
journal, August 2005
- Kemppainen, Minna; Circosta, Ariana; Tagu, Denis
- Mycorrhiza, Vol. 16, Issue 1
Predicting coiled coils from protein sequences
journal, May 1991
- Lupas, A.; Van Dyke, M.; Stock, J.
- Science, Vol. 252, Issue 5009, p. 1162-1164
The Ectomycorrhizal Fungus Laccaria bicolor Stimulates Lateral Root Formation in Poplar and Arabidopsis through Auxin Transport and Signaling
journal, October 2009
- Felten, Judith; Kohler, Annegret; Morin, Emmanuelle
- Plant Physiology, Vol. 151, Issue 4
High-Throughput Yeast Two-Hybrid Assays for Large-Scale Protein Interaction Mapping
journal, July 2001
- Walhout, Albertha J. M.; Vidal, Marc
- Methods, Vol. 24, Issue 3
A Secreted Effector Protein of Laccaria bicolor Is Required for Symbiosis Development
journal, July 2011
- Plett, Jonathan M.; Kemppainen, Minna; Kale, Shiv D.
- Current Biology, Vol. 21, Issue 14
Phosphorylation of Trihelix Transcriptional Repressor ASR3 by MAP KINASE4 Negatively Regulates Arabidopsis Immunity
journal, March 2015
- Li, Bo; Jiang, Shan; Yu, Xiao
- The Plant Cell, Vol. 27, Issue 3
Laccaria bicolor MiSSP8 is a small‐secreted protein decisive for the establishment of the ectomycorrhizal symbiosis
journal, July 2019
- Pellegrin, Clément; Daguerre, Yohann; Ruytinx, Joske
- Environmental Microbiology, Vol. 21, Issue 10
Recent Insights on Biological and Ecological Aspects of Ectomycorrhizal Fungi and Their Interactions
journal, February 2018
- Mello, Antonietta; Balestrini, Raffaella
- Frontiers in Microbiology, Vol. 9
The ectomycorrhizal basidiomycete Laccaria bicolor releases a secreted β-1,4 endoglucanase that plays a key role in symbiosis development
journal, April 2018
- Zhang, Feng; Anasontzis, George E.; Labourel, Aurore
- New Phytologist, Vol. 220, Issue 4
Development of the Poplar -Laccaria bicolor Ectomycorrhiza Modifies Root Auxin Metabolism, Signaling, and Response
journal, June 2015
- Vayssières, Alice; Pěnčík, Ales; Felten, Judith
- Plant Physiology, Vol. 169, Issue 1
The ectomycorrhizal basidiomycete Hebeloma cylindrosporum undergoes early waves of transcriptional reprogramming prior to symbiotic structures differentiation: Hebeloma cylindrosporum pre-infectious transcriptome
journal, February 2017
- Doré, Jeanne; Kohler, Annegret; Dubost, Audrey
- Environmental Microbiology, Vol. 19, Issue 3
Poplar root exudates contain compounds that induce the expression of MiSSP7 in Laccaria bicolor
journal, January 2012
- Plett, Jonathan M.; Martin, Francis
- Plant Signaling & Behavior, Vol. 7, Issue 1
NIH Image to ImageJ: 25 years of image analysis
journal, June 2012
- Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W.
- Nature Methods, Vol. 9, Issue 7
A new mathematical model for relative quantification in real-time RT-PCR
journal, May 2001
- Pfaffl, M. W.
- Nucleic Acids Research, Vol. 29, Issue 9
High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method
journal, January 2007
- Gietz, R. Daniel; Schiestl, Robert H.
- Nature Protocols, Vol. 2, Issue 1
Unearthing the roots of ectomycorrhizal symbioses
journal, October 2016
- Martin, Francis; Kohler, Annegret; Murat, Claude
- Nature Reviews Microbiology, Vol. 14, Issue 12