Soil fertility controls ectomycorrhizal mycelial traits in alpine forests receiving nitrogen deposition
Introduction
Symbiotic ectomycorrhizal (ECM) associations are prevalent in most boreal and temperate forests, as ECM fungi help plants to access growth-limiting nutrients such as nitrogen (N) in return for carbon (C) from the plant (Smith and Read, 2010). Importantly, dense extraradical mycelia (hereafter mycelia) emanating from ECM root tips can efficiently explore the surrounding soil to forage for nutrients beyond the nutrition-depleted root zone (Meier et al., 2015; Zhang et al., 2020). In addition, the production and turnover of mycelia represent significant processes for soil C input and storage (Baskaran et al., 2017), and the mycelia of ECM fungi have been highlighted as a critical moderator of C and nutrient dynamics in forest soils (Ekblad et al., 2013, Zhang et al., 2018). Therefore, unraveling how mycelial traits respond to realistic environmental conditions is crucial to predict how ECM fungi will contribute to biogeochemical processes in the context of ongoing global change.
Atmospheric N deposition has increased dramatically at a global scale, leading to gradually increased soil N availability (Stevens et al., 2018). As resource availability most likely determines the amount of C allocated from host plants to their symbiotic partners (Smith and Read, 2010; Verlinden et al., 2018), N deposition-induced changes in soil N availability would largely regulate ECM fungal-host plant interactions and influence the production of ECM root tips and mycelia (Treseder, 2004; Lilleskov et al., 2019). It has been suggested that ECM fungi can adjust their C costs by regulating mycelial production based on soil N availability and the amount of plant C allocation to balance the C costs in N exploration and the C benefits obtained from host plants (Sterkenburg et al., 2015; Plett et al., 2019). ECM biomass and production are expected to be suppressed by increased N deposition, as the relative proportion of plant C allocated to ECM fungi is generally thought to decrease as N availability increases (Verlinden et al., 2018). In addition, altered N availability would affect the dominance of ECM fungal taxa with different mycelium exploration types. Short-distance, contact and smooth exploration types (without cords) have been reported to dominate at high N availability, whereas long-distance exploration types (with thickened mycelial cords and thus higher C demand) dominate at N-limited conditions (Sterkenburg et al., 2015).
Despite the generally assumed inhibition of mycelial production and the shift of mycelial functional traits towards limited exploration ability under increased N deposition, positive effects on ECM biomass and production resulting from improved N availability have also been reported. For example, Hendricks et al. (2016) revealed an increase in ECM biomass after N fertilization. Similarly, Kalliokoski et al. (2010) found higher mycelium production in fertile sites. One reason for these discrepant findings could be the difference in direct N limitation of ECM fungi influenced by native soil nutrient availability, which might affect the magnitude and direction of the N-deposition effects on mycelial dynamics (Treseder, 2004; Lilleskov et al., 2019). In addition, numerous studies have found that external N inputs into N-limited ecosystems can increase the phosphorus (P) demand of plant host and symbiotic fungi, thus could gradually shift the nutrient status of these ecosystems to P limitation (Akselsson et al., 2008; Tarvainen et al., 2016). This change of nutrient limitation status may also stimulate C allocation to ECM mycelia and would favor the fungi with lower N-mobilizing but higher P-mobilizing capacity (Lilleskov et al., 2019). Similar to N scavenging, medium fringe- and long-distance explorers are more effective at P exploration, compared to contact- and short-distance explorers (Plassard et al., 2011). However, whether and how native soil nutrient availability modulates the effects of N deposition on the growth and functional traits of mycelia remains less explored, which may largely hinder our understanding of mycelia-mediated nutrient cycling in forest ecosystems under changing N deposition.
Here, we performed a simulated atmospheric N deposition experiment through N fertilization in two ECM-dominated alpine coniferous plantations (Picea asperata Mast. and Pinus armandii Franch.) on the eastern Tibetan Plateau, China, to examine the effects of N deposition on the growth and functional traits of ECM mycelia. Compared with the P. asperata stand, the P. armandii stand is characterized by relatively lower inorganic N pool but higher soil P availability. We took advantage of the distinct soil fertility between the two plantations to assess the influence of native soil nutrient availability on the response of mycelial dynamics to N deposition. As host plants and ECM fungi exhibit different sensitivities to N limitation (Treseder, 2004; Zhang et al., 2019), we hypothesized that the effects of N deposition on the traits of ECM mycelia would be regulated by the soil native nutrient availability. More specifically, (i) if N deposition is imposed to forest stands with relatively high native soil N availability, then the mycelial growth should be depressed, because less than N limitation of plants will decrease belowground C allocation to ECM fungi; if N is deposited to forests with relatively low native soil N availability, then the mycelial growth will be stimulated, because a slight increase in soil N availability will relieve direct N limitation of ECM fungi rather than host plants; (ii) if N deposition increases soil N availability, then the nutrient exploiting distance of mycelia explorers will be shorter, because host plants with enhanced N supply should benefit more when associating with ‘Contact-Short’ and ‘Contact-Medium’ explorers than C-demanding ‘Medium-Long’ explorers.
Section snippets
Site description
We conducted this study in two typical alpine coniferous plantations located in the Maoxian Ecosystem Research Station of the Chinese Academy of Sciences on the eastern Tibetan Plateau in Sichuan, China (31° 42′N, 103° 54′E, and 2200m a.s.l.). One is a P. armandi plantation with relatively lower soil N availability and higher P availability, compared to the other stand (P. asperata plantation) (Table 1). Both forest stands are ~40 years old. Trees were planted after the clear-cutting of shrubs
Response of mycelial growth traits to N addition
Over the 180-d growing season, N fertilization decreased the mycelial production by 35% (from 1.6 to 1.0 kg ha−1d−1) in the P. asperata stand (P < 0.001) but increased it by 78% (from 1.2 to 2.1 kg ha−1d−1) in the P. armandii stand (P = 0.007) (Fig. 2a). Nitrogen addition induced a 33% decrease (P = 0.003) but a 39% increase (P = 0.006) in the mycelial biomass in the P. asperata stand and the P. armandii stand, respectively (Fig. 2b). The mycelial density showed a similar trend in response to N
Native soil nutrient availability impacts N-deposition effect on mycelial growth traits
Consistent with our first hypothesis, N addition induced contrasting effects on mycelial growth traits in the P. asperata stand and the P. armandii stand with different native soil nutrient availability (Fig. 2; Fig. 6). In the P. asperata stand with relatively high N availability, the mycelial biomass and production showed negative responses to N addition (Fig. 6). Generally, when soil N availability is limited, plants will deliver a large amount of C to ECM fungi by boosting their abilities
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This study was supported jointly by the Second Tibetan Plateau Scientific Expedition and Research program (2019QZKK0301), the National Natural Science Foundation of China (No. 31872700 and 31901131), the Major Science Technology Project of Sichuan Province (2018SZDZX0035), and the Science and Technology Plan Projects of Sichuan Province (2021YJ0283). We are very grateful to the staff in the Maoxian Ecological Positioning Research Station of the Chinese Academy of Sciences for their field work
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