Inorganic nitrogen availability alters Eucalyptus grandis receptivity to the ectomycorrhizal fungus Pisolithus albus but not symbiotic nitrogen transfer

Abstract

Summary Forest trees are able to thrive in nutrient‐poor soils in part because they obtain growth‐limiting nutrients, especially nitrogen (N), through mutualistic symbiosis with ectomycorrhizal (ECM) fungi. Addition of inorganic N into these soils is known to disrupt this mutualism and reduce the diversity of ECM fungi. Despite its ecological impact, the mechanisms governing the observed effects of elevated inorganic N on mycorrhizal communities remain unknown. We address this by using a compartmentalized in vitro system to independently alter nutrients to each symbiont. Using stable isotopes, we traced the nutrient flux under different nutrient regimes between Eucalyptus grandis and its ectomycorrhizal symbiont, Pisolithus albus. We demonstrate that giving E. grandis independent access to N causes a significant reduction in root colonization by P. albus. Transcriptional analysis suggests that the observed reduction in colonization may be caused, in part, by altered transcription of microbe perception genes and defence genes. We show that delivery of N to host leaves is not increased by host nutrient deficiency but by fungal nutrient availability instead. Overall, this advances our understanding of the effects of N fertilization on ECM fungi and the factors governing nutrient transfer in the E. grandis–P. microcarpus interaction.

Does resource exchange in ectomycorrhizal symbiosis vary with competitive context and nitrogen addition?

“…In an earlier study on ectomycorrhizal seedlings, we found that photosynthate allocation corresponded well to root N concentrations, suggesting that C and N may be similarly linked in this symbiosis (Bogar et al, 2019). Several other studies, however, have found no correspondence (Näsholm et al, 2013;Hortal et al, 2017;Plett et al, 2020) or a negative relationship (Hasselquist et al, 2016) between fungus-derived N in leaves and plant C allocation to those fungi, similar to our finding with S. pungens. Correspondence between Suillus pungens received more plant C per unit N in the mycorrhizas under high N than did Tt, and more under high N than under low N, but the two fungi did not receive different exchange rates under low N. In all plots, boxes illustrate the median value (midline) and first and third quartiles (box edges), with whiskers spanning the range of the data to 1.5 times the interquartile range.…”

“…Much of this context-dependency may be explained by source-sink dynamics (Fellbaum et al, 2014) and competition between roots and fungi (Püschel et al, 2016). Mirroring this complexity, ectomycorrhizal symbiosis has so far demonstrated neutral or negative relationships between plant C investment and fungal N provisioning (Näsholm et al, 2013;Hortal et al, 2017;Plett et al, 2020), while fungal C sink strength often predicts plant C movement (Bidartondo et al, 2001;Nickel et al, 2017). Our goal with this study was to clarify the forces affecting resource exchange in ectomycorrhizal symbiosis by investigating the influence of resource availability and competition on C and N movement.…”

“…Ectomycorrhizal fungi produce less aboveground and belowground biomass in N-polluted forests (Ekblad et al, 2016;Lilleskov et al, 2019), likely because plants reduce their investment in fungi and belowground tissues when N is plentiful (Miller & Cramer, 2005;Högberg et al, 2011;Li et al, 2015;Lilleskov et al, 2019). Intriguingly, despite these shifts in C investment incentives, plants do not exhibit reduced ectomycorrhizal colonization under high-N field conditions (Taylor et al, 2000;Peter et al, 2001;Treseder, 2004;Cudlin et al, 2007;Lucas & Casper, 2008;Corrales et al, 2017), and increased plant C transfer to fungi does not always enhance N transfer to the host (Näsholm et al, 2013;Hasselquist et al, 2016;Plett et al, 2020). The movement of plant C and fungal N appears to be governed by complex factors.…”

Intra‐species genetic variability drives carbon metabolism and symbiotic host interactions in the ectomycorrhizal fungus Pisolithus microcarpus

“…While reduced glucose generally resulted in fewer mycorrhizal root tips formed across the isolates tested, R4 was an exception. In another study considering the effect of glucose availability on the colonization of E. grandis by the closely related P. albus , reduced glucose availability resulted in more mycorrhizal root tips formed, similar to R4 (Plett et al ., 2020a). Similarly, the depth of the Hartig net in individual root tips was significantly affected by the interaction between glucose availability and isolate.…”

Does fungal competitive ability explain host specificity or rarity in ectomycorrhizal symbioses?

“…Moving forward, more detailed studies using isotopic tracers to track carbon and nitrogen exchange ([e.g. 44 ]) will be key to determining whether S . subaureus has different physiological interactions with its host relative to other species.…”