Role of plant–fungal nutrient trading and host control in determining the competitive success of ectomycorrhizal fungi

Abstract

Multiple ectomycorrhizal fungi (EMF) compete to colonise the roots of a host plant, but it is not known whether their success is under plant or fungal control, or a combination of both. We assessed whether plants control EMF colonisation by preferentially allocating more carbon to more beneficial partners in terms of nitrogen supply or if other factors drive competitive success. We combined stable isotope labelling and RNA-sequencing approaches to characterise nutrient exchange between the plant host Eucalyptus grandis and three Pisolithus isolates when growing alone and when competing either indirectly (with a physical barrier) or directly. Overall, we found that nitrogen provision to the plant does not explain the amount of carbon that an isolate receives nor the number of roots that it colonises. Differences in nutrient exchange among isolates were related to differences in expression of key fungal and plant nitrogen and carbon transporter genes. When given a choice of partners, the plant was able to limit colonisation by the least cooperative isolate. This was not explained by a reduction in allocated carbon. Instead, our results suggest that partner choice in EMF could operate through the upregulation of defence-related genes against those fungi providing fewer nutrients.

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

“…Thus, in a similar manner, the effects of N availability on root colonization may be influenced not only by the transcriptomic response of the plant to its nutrient rich environment, but also by the individual fungal susceptibility to that response. In another study involving the interaction of E. grandis with the closely related P. microcarpus, E. grandis was shown to reduce the number of root tips colonized by a less cooperative symbiont (delivering less N for C than its competitor) when a more cooperative competitor was present (Hortal et al, 2017). Transcriptomic analysis showed that plant defence genes were upregulated only in roots in contact with the less cooperative symbiont.…”

“…There is some evidence from another lineage of mycorrhizal fungi, the arbuscular mycorrhizal (AM) fungi, that exchange of nutrients is based on a reciprocal rewards system, where fungal delivery of nutrients to the plant host is tied to, or 'rewarded' with, increased C supply (Kiers et al, 2011;Fellbaum et al, 2012;Fellbaum et al, 2014), although this may be context-dependent (Stonor et al, 2014;Walder & van der Heijden, 2015). Little correlation between N transferred by the fungus and C returns from the host has been shown in ECM fungal associations (Corrêa et al, 2008;Albarrac ın et al, 2013;Valtanen et al, 2014;Hortal et al, 2017), yet soil N concentrations, particularly the availability of inorganic N, can alter C/N trading dynamics (Treseder;2004;Albarrac ın et al, 2013;N€ asholm et al, 2013;Hasselquist & H€ ogberg, 2014). This may disrupt the stability of the mutualism and lead to the observed ecological outcomes.…”

Mycorrhizal types differ in ecophysiology and alter plant nutrition and soil processes

“…In AM fungi, invertase is not known and therefore, C transfer may be more under plant control (Casieri et al, 2013). Reciprocal rewarding and sanctioning mechanisms for nutrient to carbon exchange have evolved in AM and EcM systems (Kiers et al, 2011;Hortal et al, 2017), but these remain to be addressed in ErM associations.…”

Does genotypic and species diversity of mycorrhizal plants and fungi affect ecosystem function?

“…A complementary approach to using functional traits is the identification of functional genes, and the quantification of their expression levels under specific circumstances. Combining transcriptomics with ecophysiology experiments is a powerful approach to illuminate mycorrhizal fungal functions, whilst providing a genetic explanation for the functional variation observed between fungi, such as in soil organic matter decomposition (Shah et al, 2016) and nutrient exchange between symbiotic partners (Hortal et al, 2017). Such knowledge should be implemented for the development of biomarkers for the assessment of functional diversity.…”