Lipo-chitooligosaccharides as regulatory signals of fungal growth and development

Tomás Allen Rush; Virginie Puech-Pagès; Adeline Bascaules; Patricia Jargeat; Fabienne Maillet; Alexandra Haouy; Arthur Quy Manh Maës; Cristobal Carrera Carriel; Devanshi Khokhani; Michelle Keller-Pearson; Joanna Tannous; Kevin R. Cope; Kevin Garcia; Junko Maeda; Chad Johnson; Bailey Kleven; Quanita J. Choudhury; Jessy Labbé; Candice Swift; Michelle A. O’Malley; Jin Woo Bok; Sylvain Cottaz; Sébastien Fort; Verena Poinsot; Michael R. Sussman; Corinne Lefort; Jeniel Nett; Nancy P. Keller; Guillaume Bécard; Jean Michel Ané

doi:10.1038/s41467-020-17615-5

Lipo-chitooligosaccharides as regulatory signals of fungal growth and development

Tomás Allen Rush, Virginie Puech-Pagès, Adeline Bascaules, Patricia Jargeat, Fabienne Maillet, Alexandra Haouy, Arthur Quy Manh Maës, Cristobal Carrera Carriel, Devanshi Khokhani, Michelle Keller-Pearson, Joanna Tannous, Kevin R. Cope, Kevin Garcia, Junko Maeda, Chad Johnson, Bailey Kleven, Quanita J. Choudhury, Jessy Labbé, Candice Swift, Michelle A. O’MalleyJin Woo Bok, Sylvain Cottaz, Sébastien Fort, Verena Poinsot, Michael R. Sussman, Corinne Lefort, Jeniel Nett, Nancy P. Keller, Guillaume Bécard, Jean Michel Ané

Research output: Contribution to journal › Article › peer-review

60 Scopus citations

Abstract

Lipo-chitooligosaccharides (LCOs) are signaling molecules produced by rhizobial bacteria that trigger the nodulation process in legumes, and by some fungi that also establish symbiotic relationships with plants, notably the arbuscular and ecto mycorrhizal fungi. Here, we show that many other fungi also produce LCOs. We tested 59 species representing most fungal phyla, and found that 53 species produce LCOs that can be detected by functional assays and/or by mass spectroscopy. LCO treatment affects spore germination, branching of hyphae, pseudohyphal growth, and transcription in non-symbiotic fungi from the Ascomycete and Basidiomycete phyla. Our findings suggest that LCO production is common among fungi, and LCOs may function as signals regulating fungal growth and development.

Original language	English
Article number	3897
Journal	Nature Communications
Volume	11
Issue number	1
DOIs	https://doi.org/10.1038/s41467-020-17615-5
State	Published - Dec 1 2020

Funding

We thank Dr. Hugues Driguez for providing some synthetic lipochitin standards for mass spectrometry. RNA-Seq data were based upon work supported by the National Science Foundation under Award Numbers DBI-0735191, DBI-1265383, and DBI-1743442 (URL: http://www.cyverse.org). Support for mass spectrometry analyses was provided by the ICT-Mass spectrometry and MetaToul-MetaboHUB Facilities, and by the MetaboHUB-ANR-11-INBS-0010 network. Support for synthesis and characterization of COs and LCOs was provided by Labex Arcane and CBH-EUR-GS (ANR-17-EURE-0003), CDP Glyco@alps (ANR-15-IDEX-02), PolyNat Carnot Institut (16-CARN-0025-01), and ICMG (FR 2607) mass spectrometry platform. We thank Dr. Gregory Bonito for the cultures of Mortierella elongata, M. minutissima, and Mortierella sp. nov. strain GBAus27b; Dr. Tony Goldberg, Dr. Jeffrey Lorch, and Karen Vanderwolf for cultures of Aureobasidium pullulans, Protomyces inouye, R. mucilaginosa, and Taphrina virginica; Dr. Chris Hittinger for a culture of S. cerevisiae; Dr. Brian Hudelson and Armila Francis for cultures of Fusarium oxysporum, Mucor circinelloides, P. ery-throseptica, P. ultimum, and Trichoderma harizanum; Dr. Paul Koch for cultures of Clarireedia homoeocarpa, Fusarium fujikuroi, and Typhula incarnata; Drs. Timothy James and Rabern Simmons for cultures of Entophlyctis luteolus, Paraphysoderma sedebokerensis, and Powellomyces hirtus; Dr. Thierry Rouxel for a culture of L. maculans; Drs. Francis Martin and Annegret Kohler for their advice and for cultures of L. bicolor, C. geophilum, G. stellatum, and L. palutris; and Dr. Anne Pringle for cultures and samples of Amanita muscaria and A. thiersii. We also thank Marie Rodriguez, Juliette Teyssandier, Clément Bertrand, and Sandrine Paute for technical assistance, and Drs. Jacob Golan and Katie Morey Gold for statistical advice. This work was supported by the French Agence Nationale de la Recherche under contract ANR-14-CE18-0008-01, the research project Engineering Nitrogen Symbiosis for Africa (ENSA), which is funded through a grant to the University of Cambridge by the Bill & Melinda Gates Foundation (OPP11772165), the Laboratoire d’Excellence entitled TULIP (ANR-10-LABX-41), the Plant-Microbe Interfaces Scientific Focus Area in the Genomic Science Program, the Office of Biological and Environmental Research in the US Department of Energy (DOE) Office of Science (Oak Ridge National Laboratory is managed by UT-Battelle, LLC, the DOE (contract DE-AC05-00OR22725), the United States Department of Agriculture (WIS01695), and by the National Science Foundation (DGE-1256259, PGRP −1546742, and IOS-1331098). We thank the University of Wisconsin-Madison Advanced Opportunity Fellowship, Science, and Medicine Graduate Research Scholars program and the Ford Foundation Pre-Doctoral Scholarship for their support and funding of T.A. Rush.

Funders	Funder number
Engineering Nitrogen Symbiosis for Africa
Office of Biological and Environmental Research in the US Department of Energy
National Science Foundation	DBI-1265383, PGRP-1546742, DBI-0735191, DBI-1743442
Ford Foundation
U.S. Department of Energy
U.S. Department of Agriculture	1331098, 1256259, PGRP −1546742, WIS01695
Bill and Melinda Gates Foundation	OPP11772165, ANR-10-LABX-41
State of Connecticut Department of Agriculture
Oak Ridge National Laboratory	DE-AC05-00OR22725
University of Cambridge
Agence Nationale de la Recherche	ANR-14-CE18-0008-01

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10.1038/s41467-020-17615-5

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Rush, T. A., Puech-Pagès, V., Bascaules, A., Jargeat, P., Maillet, F., Haouy, A., Maës, A. Q. M., Carriel, C. C., Khokhani, D., Keller-Pearson, M., Tannous, J., Cope, K. R., Garcia, K., Maeda, J., Johnson, C., Kleven, B., Choudhury, Q. J., Labbé, J., Swift, C., ... Ané, J. M. (2020). Lipo-chitooligosaccharides as regulatory signals of fungal growth and development. Nature Communications, 11(1), Article 3897. https://doi.org/10.1038/s41467-020-17615-5

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title = "Lipo-chitooligosaccharides as regulatory signals of fungal growth and development",

abstract = "Lipo-chitooligosaccharides (LCOs) are signaling molecules produced by rhizobial bacteria that trigger the nodulation process in legumes, and by some fungi that also establish symbiotic relationships with plants, notably the arbuscular and ecto mycorrhizal fungi. Here, we show that many other fungi also produce LCOs. We tested 59 species representing most fungal phyla, and found that 53 species produce LCOs that can be detected by functional assays and/or by mass spectroscopy. LCO treatment affects spore germination, branching of hyphae, pseudohyphal growth, and transcription in non-symbiotic fungi from the Ascomycete and Basidiomycete phyla. Our findings suggest that LCO production is common among fungi, and LCOs may function as signals regulating fungal growth and development.",

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Rush, TA, Puech-Pagès, V, Bascaules, A, Jargeat, P, Maillet, F, Haouy, A, Maës, AQM, Carriel, CC, Khokhani, D, Keller-Pearson, M, Tannous, J, Cope, KR, Garcia, K, Maeda, J, Johnson, C, Kleven, B, Choudhury, QJ, Labbé, J, Swift, C, O’Malley, MA, Bok, JW, Cottaz, S, Fort, S, Poinsot, V, Sussman, MR, Lefort, C, Nett, J, Keller, NP, Bécard, G & Ané, JM 2020, 'Lipo-chitooligosaccharides as regulatory signals of fungal growth and development', Nature Communications, vol. 11, no. 1, 3897. https://doi.org/10.1038/s41467-020-17615-5

TY - JOUR

T1 - Lipo-chitooligosaccharides as regulatory signals of fungal growth and development

AU - Rush, Tomás Allen

AU - Puech-Pagès, Virginie

AU - Bascaules, Adeline

AU - Jargeat, Patricia

AU - Maillet, Fabienne

AU - Haouy, Alexandra

AU - Maës, Arthur Quy Manh

AU - Carriel, Cristobal Carrera

AU - Khokhani, Devanshi

AU - Keller-Pearson, Michelle

AU - Tannous, Joanna

AU - Cope, Kevin R.

AU - Garcia, Kevin

AU - Maeda, Junko

AU - Johnson, Chad

AU - Kleven, Bailey

AU - Choudhury, Quanita J.

AU - Labbé, Jessy

AU - Swift, Candice

AU - O’Malley, Michelle A.

AU - Bok, Jin Woo

AU - Cottaz, Sylvain

AU - Fort, Sébastien

AU - Poinsot, Verena

AU - Sussman, Michael R.

AU - Lefort, Corinne

AU - Nett, Jeniel

AU - Keller, Nancy P.

AU - Bécard, Guillaume

AU - Ané, Jean Michel

PY - 2020/12/1

Y1 - 2020/12/1

N2 - Lipo-chitooligosaccharides (LCOs) are signaling molecules produced by rhizobial bacteria that trigger the nodulation process in legumes, and by some fungi that also establish symbiotic relationships with plants, notably the arbuscular and ecto mycorrhizal fungi. Here, we show that many other fungi also produce LCOs. We tested 59 species representing most fungal phyla, and found that 53 species produce LCOs that can be detected by functional assays and/or by mass spectroscopy. LCO treatment affects spore germination, branching of hyphae, pseudohyphal growth, and transcription in non-symbiotic fungi from the Ascomycete and Basidiomycete phyla. Our findings suggest that LCO production is common among fungi, and LCOs may function as signals regulating fungal growth and development.

AB - Lipo-chitooligosaccharides (LCOs) are signaling molecules produced by rhizobial bacteria that trigger the nodulation process in legumes, and by some fungi that also establish symbiotic relationships with plants, notably the arbuscular and ecto mycorrhizal fungi. Here, we show that many other fungi also produce LCOs. We tested 59 species representing most fungal phyla, and found that 53 species produce LCOs that can be detected by functional assays and/or by mass spectroscopy. LCO treatment affects spore germination, branching of hyphae, pseudohyphal growth, and transcription in non-symbiotic fungi from the Ascomycete and Basidiomycete phyla. Our findings suggest that LCO production is common among fungi, and LCOs may function as signals regulating fungal growth and development.

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DO - 10.1038/s41467-020-17615-5

M3 - Article

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AN - SCOPUS:85089068679

SN - 2041-1723

VL - 11

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 3897

ER -

Lipo-chitooligosaccharides as regulatory signals of fungal growth and development

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