Carbon allocation and competition maintain variation in plant root mutualisms

Christian, Natalie; Bever, James D.

doi:10.1002/ece3.4118

Cited by 17 publications

(8 citation statements)

References 59 publications

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“…Biological market perspectives emphasizing the metabolic cost of fungal resource capture 33 suggest that plants may associate with ECM mutualists that maximize N acquisition and minimize plant carbon (C) expenditure (N return on C investment) 34 , 35 . ECM taxa vary widely in their capacity to decay SOM 30 , 36 , with greater decay capacity likely carrying a greater C cost to their plant host 37 .…”

Section: Introductionmentioning

confidence: 99%

Ectomycorrhizal access to organic nitrogen mediates CO2 fertilization response in a dominant temperate tree

et al. 2021

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Plant–mycorrhizal interactions mediate plant nitrogen (N) limitation and can inform model projections of the duration and strength of the effect of increasing CO2 on plant growth. We present dendrochronological evidence of a positive, but context-dependent fertilization response of Quercus rubra L. to increasing ambient CO2 (iCO2) along a natural soil nutrient gradient in a mature temperate forest. We investigated this heterogeneous response by linking metagenomic measurements of ectomycorrhizal (ECM) fungal N-foraging traits and dendrochronological models of plant uptake of inorganic N and N bound in soil organic matter (N-SOM). N-SOM putatively enhanced tree growth under conditions of low inorganic N availability, soil conditions where ECM fungal communities possessed greater genomic potential to decay SOM and obtain N-SOM. These trees were fertilized by 38 years of iCO2. In contrast, trees occupying inorganic N rich soils hosted ECM fungal communities with reduced SOM decay capacity and exhibited neutral growth responses to iCO2. This study elucidates how the distribution of N-foraging traits among ECM fungal communities govern tree access to N-SOM and subsequent growth responses to iCO2.

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Section: Introductionmentioning

confidence: 99%

Ectomycorrhizal access to organic nitrogen mediates CO2 fertilization response in a dominant temperate tree

et al. 2021

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“…Studies at local, regional, and continental scales consistently identify soil inorganic N availability as a key determinant of ECM fungal community composition (Taylor et al, 2000;Lilleskov et al, 2002a;Peay et al, 2015;van der Linde et al, 2018). Biological market perspectives provide insight into how N availability and fungal N acquisition traits may interact to structure these communities (Koide et al, 2014;Christian & Bever, 2018). Plants may partner with fungal mutualists that maximize N (or phosphorus) acquisition, while minimizing photosynthate expenditure (Hortal et al, 2017;Bogar et al, 2019;Meeds et al, 2021).…”

Section: Introductionmentioning

confidence: 99%

Ectomycorrhizal fungal decay traits along a soil nitrogen gradient

Pellitier

Zak

2021

New Phytologist

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The extent to which ectomycorrhizal (ECM) fungi decay soil organic matter (SOM) has implications for accurately predicting forest ecosystem response to climate change. Investigating the distribution of gene traits associated with SOM decay among ectomycorrhizal fungal communities could improve understanding of SOM dynamics and plant nutrition. We hypothesized that soil inorganic nitrogen (N) availability structures the distribution of ECM fungal genes associated with SOM decay and, specifically, that ECM fungal communities occurring in inorganic N-poor soils have greater SOM decay potential.To test this hypothesis, we paired amplicon and shotgun metagenomic sequencing of 60 ECM fungal communities associating with Quercus rubra along a natural soil inorganic N gradient.Ectomycorrhizal fungal communities occurring in low inorganic N soils were enriched in gene families involved in the decay of lignin, cellulose, and chitin. Ectomycorrhizal fungal community composition was the strongest driver of shifts in metagenomic estimates of fungal decay potential. Our study simultaneously illuminates the identity of key ECM fungal taxa and gene families potentially involved in the decay of SOM, and we link rhizomorphic and medium-distance hyphal morphologies with enhanced SOM decay potential.Coupled shifts in ECM fungal community composition and community-level decay gene frequencies are consistent with outcomes of trait-mediated community assembly processes.

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“…This mechanism requires that the host favours guild members with more beneficial traits, thereby explaining the persistence of good mutualists. Such preferential allocation of resources has been documented in the AM symbiosis (Kiers et al, 2011;Hammer et al, 2011;Bever et al, 2009;Ji and Bever, 2016) and has theoretical support (Bachelot and Lee, 2018;Bever, 2015;Moeller and Neubert, 2016;Hoeksema and Kummel, 2003;Christian and Bever, 2018;Křivan and Revilla, 2019;Valdovinos et al, 2013). However, experimental studies have yielded inconsistent results (Fitter, 2006;Kiers and Van Der Heijden, 2006;Walder and van der Heijden, 2015) and no physiological basis for host discrimination has been identified.…”

Section: Introductionmentioning

confidence: 70%

Parasitism within mutualist guilds explains the maintenance of diversity in multi-species mutualisms

et al. 2020

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We consider here mutualisms where there are multiple species sharing a resource supplied by the same partner. If, as commonly assumed, there is competition between the species, then only the superior competitor should persist. Nevertheless, coexistence of multiple species sharing the same mutualistic partner is a widespread phenomenon. Regulation of nutrient exchange, where each species receives resources from the partner in proportion to the strength of the mutualism between the two, has been proposed as the main mechanism for coexistence in multi-species mutualisms involving the transfer of nutrients. Significant arguments, however, challenge the importance of partner selection processes. We present a mathematical model, applied to the arbuscular mycorrhizal symbiosis, to propose an alternative explanation for this coexistence. We show that asymmetric resource exchange between the plant and its fungal guild can lead to indirect parasitic interactions between guild members. In our model, the amount of carbon supplied by the plant to the fungi depends on both plant and fungal biomass, while the amount of phosphorus supplied by the fungi to the plant depends on both plant and fungal biomass when the plant is small, and effectively on fungal biomass only when the plant is large. As a consequence of these functional responses, more beneficial mutualists increase resource availability, and are indirectly exploited by less beneficial species that consume the resource and grow larger than they would in the absence of the better mutualists. As guild mutualists are not competing, competitive exclusion does not occur. Hence, the interaction structure can explain the maintenance of diversity within guilds in the absence of spatial structure and niche-related processes.

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Carbon allocation and competition maintain variation in plant root mutualisms

Cited by 17 publications

References 59 publications

Ectomycorrhizal access to organic nitrogen mediates CO2 fertilization response in a dominant temperate tree

Ectomycorrhizal access to organic nitrogen mediates CO2 fertilization response in a dominant temperate tree

Ectomycorrhizal fungal decay traits along a soil nitrogen gradient

Parasitism within mutualist guilds explains the maintenance of diversity in multi-species mutualisms

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