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

• Published in: Plant, cell and environment cell and environment, 2020-04, Vol.43 (4), p.1047-1068
• Main Authors: 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
• Format: Article
• Language: English
• Subjects: Architecture; cell wall remodelling; Cell walls; Colonization; Crosstalk; Cyclopentanes - metabolism; defense; ectomycorrhizae; Ectomycorrhizas; Environmental Sciences; Ethylene; Ethylenes - metabolism; Extracellular matrix; Forest Science; Fungi; Gene expression; Gene Expression Profiling; Gene sequencing; Gibberellins; Gibberellins - metabolism; Hartig net; jasmonate; Jasmonic acid; Laccaria bicolor; Life Sciences; Liquid chromatography; Mass spectrometry; Mass spectroscopy; MiSSP; Morphology; Mycorrhizae - metabolism; Oxylipins - metabolism; phytohormones; Plant Growth Regulators - metabolism; Plant hormones; Plant Roots - metabolism; Plant Roots - microbiology; Plant Roots - physiology; Plant Shoots - metabolism; Poplar; Populus tremula x alba; Ribonucleic acid; RNA; Root development; Roots; Salicylates - metabolism; Salicylic acid; Skogsvetenskap; Symbiosis; Transcriptome
• ISSN: 0140-7791; 1365-3040; 1365-3040
• DOI: 10.1111/pce.13702

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. Here, 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. The ectomycorrhizal fungus Laccaria bicolor affects sensitivity to jasmonate in roots of Populus tremula x alba, while promoting responses to salicylate, gibberellin, and ethylene. Adjusted accumulation and perception of these phytohormones is necessary for the development of ectomycorrhizae.