Dauphin Benjamin, de Freitas Pereira Maíra, Croll Daniel, Cardoso Anastácio Thalita, Fauchery Laure, Guinet Frédéric, Dutra Costa Maurício, Martin Francis, Peter Martina, Kohler Annegret
Swiss Federal Research Institute WSL, Zuercherstrasse 111, Birmensdorf, 8903, Switzerland.
Université de Lorraine, Institut national de recherche pour l'agriculture, l'alimentation et l'environnement, UMR Interactions Arbres/Microorganismes, Centre INRAE Grand Est-Nancy, 54280, Champenoux, France.
New Phytol. 2025 Oct;248(1):157-177. doi: 10.1111/nph.70395. Epub 2025 Aug 7.
Forest trees rely on ectomycorrhizal (ECM) fungi for acquiring scarce resources such as water and nutrients. However, the molecular mechanisms governing ECM traits remain inadequately understood, particularly the role of intraspecific fungal variation in root-tip colonisation and trophic interactions. This study examined six ECM traits using Pisolithus microcarpus, an ECM fungus capable of forming ECM rootlets in poplar. A collection of 40 sibling monokaryons and their parental dikaryon was analysed through genome and transcriptome sequencing to examine quantitative trait loci, gene expression and mating-type loci. These findings revealed a pronounced phenotypic continuum in poplar root colonisation by sibling monokaryons, ranging from incompatible to fully compatible strains. Genetic recombination among monokaryons was demonstrated, and genomic regions potentially involved in ECM fungal traits were identified. Transcriptomic analysis revealed greater differentiation in transcriptomic profiles between fungal strains than between fungal tissues, and uncovered tissue-specific functional responses for ECM and free-living mycelia. Poplar exhibited distinct transcriptomic responses when interacting with different sibling monokaryons and the parental dikaryon. Allele sorting at 11 mating-type loci confirmed the species' heterothallic tetrapolar system. This study advances understanding of the genetic and transcriptomic mechanisms underlying ECM symbioses, highlighting intraspecific fungal diversity's role in forest ecosystem functioning.
林木依靠外生菌根（ECM）真菌获取水和养分等稀缺资源。然而，调控ECM性状的分子机制仍未得到充分理解，尤其是种内真菌变异在根尖定殖和营养相互作用中的作用。本研究使用微小皮伞（一种能够在杨树中形成ECM根状菌索的ECM真菌）检测了六个ECM性状。通过基因组和转录组测序分析了40个同胞单核体及其亲本双核体的集合，以检测数量性状位点、基因表达和交配型位点。这些发现揭示了同胞单核体在杨树根部定殖过程中存在明显的表型连续体，范围从不相容菌株到完全相容菌株。证明了单核体之间的基因重组，并鉴定了可能参与ECM真菌性状的基因组区域。转录组分析显示，真菌菌株之间的转录组图谱差异大于真菌组织之间的差异，并揭示了ECM和自由生活菌丝体的组织特异性功能反应。杨树在与不同的同胞单核体和亲本双核体相互作用时表现出不同的转录组反应。11个交配型位点的等位基因分类证实了该物种的异宗配合四极性系统。本研究推进了对ECM共生遗传和转录组机制的理解，突出了种内真菌多样性在森林生态系统功能中的作用。
