Host phenology and potential saprotrophism of ectomycorrhizal fungi in the boreal forest

Abstract

Summary Phenology‐induced changes in carbon assimilation by trees may affect carbon stored in fine roots and as a consequence, alter carbon allocated to ectomycorrhizal fungi. Two competing models exist to explain carbon mobilization by ectomycorrhizal fungi. Under the ‘saprotrophy model’, decreased allocation of carbon may induce saprotrophic behaviour in ectomycorrhizal fungi, resulting in the decomposition of organic matter to mobilize carbon. Alternatively, under the ‘nutrient acquisition model’, decomposition may instead be driven by the acquisition of nutrients locked within soil organic matter compounds, with carbon mobilization a secondary process. We tested whether phenology‐induced shifts in carbon reserves of fine roots of aspen (Populus tremuloides) affect potential activity of four carbon‐compound degrading enzymes, β‐glucuronidase, β‐glucosidase, N‐acetylglucosaminidase and laccase, by ectomycorrhizal fungi. Ectomycorrhizal roots from mature aspen were collected across eight stands in north‐eastern Alberta, Canada, and analysed during tree dormancy, leaf flush, full leaf expansion and leaf abscission. We predicted potential extracellular enzyme activity to be highest when root carbon reserves were lowest, should host phenology induce saprotrophism. Further, we anticipated enzyme activity to be mediated by invertase, a plant‐derived enzyme which makes carbon available to fungal symbionts in the plant–fungus interface. Root carbon reserves were positively correlated with invertase, suggesting phenology may affect carbon allocation to ectomycorrhizal fungi. However, of the four enzymes, host phenology had the largest effect on β‐glucuronidase, but activity of this enzyme was not correlated with root carbon reserves or invertase. Low‐biomass ectomycorrhizas had greater potential laccase activity than high‐biomass ectomycorrhizas, highlighting discrete functional traits in fungi for litter decomposition. Our results suggest that the decomposition of organic matter may be driven by foraging by fungi for nutrients locked within organic compounds rather than for mobilizing carbon. Furthermore, the potential ability to degrade lignin was more common in low‐biomass ectomycorrhizas when compared to high‐biomass ectomycorrhizas. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.12695/suppinfo is available for this article.

Tree thinning and fire affect ectomycorrhizal fungal communities and enzyme activities

“…Laccase activity in EMF often correlates with morphology, with fungi with very little extraradical mycelium, such as many Russula species, often having the highest laccase activity (Tedersoo et al 2012, Hupperts et al 2016), a pattern corroborated here. EMF enzyme activity was also seen to be more strongly related to exploration type than fungal lineage in a tropical forest (Tedersoo et al 2012) and more strongly related to exploration type than host phenology in a boreal forest (Hupperts et al 2016). Laccaria, the principal genus represented in the Hydnangiaceae, typically have medium-or short-distance exploration types (Agerer 2001) and here had high laccase activity consistent with short-distance exploration types.…”

“…Ectomycorrhizae produce little NAGase relative to saprotrophs (Burke et al 2014), but even though their enzyme activity levels are low, their activity is important because EMF represent a direct path of N to trees (Cullings and Courty 2009). Boletaceae here had high NAGase activity but low phenol-degrading activity, consistent with Hupperts et al (2016). This family consistently produces rhizomorphs characteristic of a longdistance exploration type (Agerer 2001).…”

Quantitative losses vs. qualitative stability of ectomycorrhizal community responses to 3 years of experimental summer drought in a beech–spruce forest

“…Drought increased the extracellular cellulolytic potential per vital tip irrespective of tree species. Extracellular cellulolytic activity may be stimulated by the presence of dead fine‐root material, which accumulated during repeated drought events, to gain access to nutrients contained in these dead tissues (Hupperts, Karst, Pritsch, & Landhäusser, ; Lindahl & Tunlid, ; Pritsch & Garbaye, ). The alternative explanation of saprotrophic carbon acquisition by ECM fungi from organic matter decay rather than the internal carbon supply of the plant (Bréda et al., ; Courty, Bréda, & Garbaye, ) seems unlikely as the observed increase in long‐distance types under drought suggests that carbon was not limiting.…”

“…Drought increased the extracellular cellulolytic potential per vital tip irrespective of tree species. Extracellular cellulolytic activity may be stimulated by the presence of dead fine-root material, which accumulated during repeated drought events, to gain access to nutrients contained in these dead tissues (Hupperts, Karst, Pritsch, & Landh€ ausser, 2017;Lindahl & Tunlid, 2015;Pritsch & Garbaye, 2011…”

Non-structural carbohydrate concentrations of Fagus sylvatica and Pinus sylvestris fine roots are linked to ectomycorrhizal enzymatic activity during spring reactivation

“…Tree hosts have developed mechanisms to regulate carbohydrate flows towards the fungal partner (Nehls 2008;Nehls et al 2010) and therefore govern growth and metabolism of EM fungi (Högberg et al 2010). A recent study by Hupperts et al (2017) found a significant positive correlation between the amount of sugar in the fine roots and the activity of root invertase. This enzyme hydrolyzes sucrose into glucose and fructose in the interfacial apoplast.…”