Phosphate availability and ectomycorrhizal symbiosis with Pinus sylvestris have independent effects on the Paxillus invo
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ORIGINAL ARTICLE
Phosphate availability and ectomycorrhizal symbiosis with Pinus sylvestris have independent effects on the Paxillus involutus transcriptome Christina Paparokidou 1 & Jonathan R. Leake 1 & David J. Beerling 1 & Stephen A. Rolfe 1 Received: 16 June 2020 / Accepted: 29 October 2020 # The Author(s) 2020
Abstract Many plant species form symbioses with ectomycorrhizal fungi, which help them forage for limiting nutrients in the soil such as inorganic phosphate (Pi). The transcriptional responses to symbiosis and nutrient-limiting conditions in ectomycorrhizal fungal hyphae, however, are largely unknown. An artificial system was developed to study ectomycorrhizal basidiomycete Paxillus involutus growth in symbiosis with its host tree Pinus sylvestris at different Pi concentrations. RNA-seq analysis was performed on P. involutus hyphae growing under Pi-limiting conditions, either in symbiosis or alone. We show that Pi starvation and ectomycorrhizal symbiosis have an independent effect on the P. involutus transcriptome. Notably, low Pi availability induces expression of newly identified putative high-affinity Pi transporter genes, while reducing the expression of putative organic acid transporters. Additionally, low Pi availability induces a close transcriptional interplay between P and N metabolism. GTP-related signalling was found to have a positive effect in the maintenance of ectomycorrhizal symbiosis, whereas multiple putative cytochrome P450 genes were found to be downregulated, unlike arbuscular mycorrhizal fungi. We provide the first evidence of global transcriptional changes induced by low Pi availability and ectomycorrhizal symbiosis in the hyphae of P. involutus, revealing both similarities and differences with better-characterized arbuscular mycorrhizal fungi. Keywords Paxillus involutus . Pinus sylvestris . Ectomycorrhizal symbiosis . Pi-starvation . Pi transporters . RNA-seq
Introduction The vast majority of plants, including forest trees, form symbioses with mycorrhizal fungi where over 90% of plant roots are primarily connected with the mycelia of ectomycorrhizal (EM) or arbuscular mycorrhizal (AM) fungi (Bonfante and Genre 2010). In the case of EM symbioses, the extensive extraradical mycelium that proliferates through the soil enables forest trees to forage efficiently and acquire nutrients, particularly N and P (Leake et al. 2004). In natural soils, P concentrations in the form of inorganic phosphate (Pi) are often low ranging from 1 to 10 μM (Bieleski 1973). P can be present as organic and inorganic forms, many of which are not directly accessible to plant roots (Costa et al. 2016). The EM fungal mycelium has specialized functions to mobilize, * Stephen A. Rolfe [email protected] 1
Department of Animal and Plant Sciences, University of Sheffield, Sheffield, UK
acquire, metabolize, store and transport P from these diverse sources (Nehls and Plassard 2018). EM fungi contain specialized high-affinity Pi transporters, belonging to the PHT1 family of Pi transporters, that enable the
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