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Title: An ectomycorrhizal fungus alters sensitivity to jasmonate, salicylate, gibberellin, and ethylene in host roots

Abstract

The phytohormones jasmonate, gibberellin, salicylate, and ethylene regulate an interconnected reprogramming network integrating root development with plant responses against microbes. The establishment of mutualistic ectomycorrhizal symbiosis requires the suppression of plant defense responses against fungi as well as the modification of root architecture and cortical cell wall properties. In this work, we investigated the contribution of phytohormones and their crosstalk to the ontogenesis of ectomycorrhizae (ECM) between grey poplar (Populus tremula x alba) roots and the fungus Laccaria bicolor. To obtain the hormonal blueprint of developing ECM, we quantified the concentrations of jasmonates, gibberellins, and salicylate via liquid chromatography-tandem mass spectrometry. Subsequently, we assessed root architecture, mycorrhizal morphology, and gene expression levels (RNA sequencing) in phytohormone-treated poplar lateral roots in the presence or absence of L. bicolor. Salicylic acid accumulated in mid-stage ECM. Exogenous phytohormone treatment affected the fungal colonization rate and/or frequency of Hartig net formation. Colonized lateral roots displayed diminished responsiveness to jasmonate but regulated some genes, implicated in defense and cell wall remodelling, that were specifically differentially expressed after jasmonate treatment. Responses to salicylate, gibberellin, and ethylene were enhanced in ECM. The dynamics of phytohormone accumulation and response suggest that jasmonate, gibberellin, salicylate, and ethylene signalling playmore » multifaceted roles in poplar L. bicolor ectomycorrhizal development.« less

Authors:
ORCiD logo [1];  [1]; ORCiD logo [1];  [2];  [1];  [3];  [3];  [2];  [2];  [1];  [4];  [2];  [5];  [6]; ORCiD logo [1]
+ Show Author Affiliations
  1. Univ. of Lorraine, Champenoux (France)
  2. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  3. Palacký Univ., Olomouc (Czech Republic); The Czech Academy of Sciences, Olomouc (Czech Republic)
  4. Univ. of Lorraine, Champenoux (France); Umea Plant Science Centre (Sweden)
  5. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States)
  6. Univ. of Lorraine, Champenoux (France); Beijing Forestry Univ. (China)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1619170
Alternate Identifier(s):
OSTI ID: 1598050
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Plant, Cell and Environment
Additional Journal Information:
Journal Volume: 43; Journal Issue: 4; Journal ID: ISSN 0140-7791
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; cell wall remodelling; crosstalk; defense; ectomycorrhizae; jasmonate; Laccaria bicolor; MiSSP; phytohormones; Populus tremula x alba; symbiosis

Citation Formats

Basso, Veronica, Kohler, Annegret, Miyauchi, Shingo, Singan, Vasanth, Guinet, Frédéric, Šimura, Jan, Novák, Ondřej, Barry, Kerrie W., Amirebrahimi, Mojgan, Block, Jonathan, Daguerre, Yohann, Na, Hyunsoo, Grigoriev, Igor V., Martin, Francis, and Veneault‐Fourrey, Claire. An ectomycorrhizal fungus alters sensitivity to jasmonate, salicylate, gibberellin, and ethylene in host roots. United States: N. p., 2019. Web. doi:10.1111/pce.13702.
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Basso, Veronica, Kohler, Annegret, Miyauchi, Shingo, Singan, Vasanth, Guinet, Frédéric, Šimura, Jan, Novák, Ondřej, Barry, Kerrie W., Amirebrahimi, Mojgan, Block, Jonathan, Daguerre, Yohann, Na, Hyunsoo, Grigoriev, Igor V., Martin, Francis, & Veneault‐Fourrey, Claire. An ectomycorrhizal fungus alters sensitivity to jasmonate, salicylate, gibberellin, and ethylene in host roots. United States. https://doi.org/10.1111/pce.13702
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Basso, Veronica, Kohler, Annegret, Miyauchi, Shingo, Singan, Vasanth, Guinet, Frédéric, Šimura, Jan, Novák, Ondřej, Barry, Kerrie W., Amirebrahimi, Mojgan, Block, Jonathan, Daguerre, Yohann, Na, Hyunsoo, Grigoriev, Igor V., Martin, Francis, and Veneault‐Fourrey, Claire. Fri . "An ectomycorrhizal fungus alters sensitivity to jasmonate, salicylate, gibberellin, and ethylene in host roots". United States. https://doi.org/10.1111/pce.13702. https://www.osti.gov/servlets/purl/1619170.
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@article{osti_1619170,
title = {An ectomycorrhizal fungus alters sensitivity to jasmonate, salicylate, gibberellin, and ethylene in host roots},
author = {Basso, Veronica and Kohler, Annegret and Miyauchi, Shingo and Singan, Vasanth and Guinet, Frédéric and Šimura, Jan and Novák, Ondřej and Barry, Kerrie W. and Amirebrahimi, Mojgan and Block, Jonathan and Daguerre, Yohann and Na, Hyunsoo and Grigoriev, Igor V. and Martin, Francis and Veneault‐Fourrey, Claire},
abstractNote = {The phytohormones jasmonate, gibberellin, salicylate, and ethylene regulate an interconnected reprogramming network integrating root development with plant responses against microbes. The establishment of mutualistic ectomycorrhizal symbiosis requires the suppression of plant defense responses against fungi as well as the modification of root architecture and cortical cell wall properties. In this work, we investigated the contribution of phytohormones and their crosstalk to the ontogenesis of ectomycorrhizae (ECM) between grey poplar (Populus tremula x alba) roots and the fungus Laccaria bicolor. To obtain the hormonal blueprint of developing ECM, we quantified the concentrations of jasmonates, gibberellins, and salicylate via liquid chromatography-tandem mass spectrometry. Subsequently, we assessed root architecture, mycorrhizal morphology, and gene expression levels (RNA sequencing) in phytohormone-treated poplar lateral roots in the presence or absence of L. bicolor. Salicylic acid accumulated in mid-stage ECM. Exogenous phytohormone treatment affected the fungal colonization rate and/or frequency of Hartig net formation. Colonized lateral roots displayed diminished responsiveness to jasmonate but regulated some genes, implicated in defense and cell wall remodelling, that were specifically differentially expressed after jasmonate treatment. Responses to salicylate, gibberellin, and ethylene were enhanced in ECM. The dynamics of phytohormone accumulation and response suggest that jasmonate, gibberellin, salicylate, and ethylene signalling play multifaceted roles in poplar L. bicolor ectomycorrhizal development.},
doi = {10.1111/pce.13702},
journal = {Plant, Cell and Environment},
number = 4,
volume = 43,
place = {United States},
year = {Fri Dec 13 00:00:00 EST 2019},
month = {Fri Dec 13 00:00:00 EST 2019}
}
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https://doi.org/10.1111/pce.13702
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