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.
Highlights
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)
We explored the role of EM symbiosis and its effect on transcriptional changes in P. involutus hyphae under Pi-limiting conditions
The dry mass of the mycelium increased with increasing Pi supply in both NS and S conditions and the mycelial mass was greater in the NS condition compared to the S condition (ANCOVA, p = 0.006) but there was no significant interaction between Pi supply and symbiotic status (p = 0.833) (Fig. 2a)
Summary
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). EM fungi contain specialized high-affinity Pi transporters, belonging to the PHT1 family of Pi transporters, that enable the acquisition of Pi present at low concentrations in the soil (Casieri et al 2013). In the Basidiomycete EM fungus Tricholoma spp., Kothe et al (2002) identified two genes with homology to high-affinity Pi transporters, whose expression was induced under Pi starvation. Tatry et al (2009) identified and functionally characterized two plasma membrane Pi transporter genes, HcPT1 and HcPT2, from Hebeloma cylindrosporum, an EM-forming Basidiomycete. Both transporters were proposed to function as high-affinity Pi transporters coupled with H+ symporter activity and were expressed during EM symbiosis. Under Pi-limiting conditions, only the expression of HcPT1 was induced, suggesting a specific role of HcPT1 in response to Pi deprivation, with HcPT2 having a role in Pi-sufficient conditions (Tatry et al 2009)
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