TY - JOUR

T1 - Tripartite symbioses regulate plant-soil feedback in alder

AU - Ardanuy, Agnes

AU - Walker, Jennifer K. M.

AU - Kritzler, Ully

AU - Taylor, Andy F. S.

AU - Johnson, David

N1 - Funding Information: We thank the National Trust for Scotland for access to the Crathes Estate. This work was funded by the Natural Environment Research Council (ref NE/M015653/1) and a Ramon Areces Fellowship to A.A. D.J. receives partial funding from the N8 AgriFood programme. We thank Filipa Cox for a critical read of the manuscript. Publisher Copyright: © 2021 British Ecological Society

PY - 2021/6/30

Y1 - 2021/6/30

N2 - Plant–soil feedbacks regulate plant productivity and diversity, but potential mechanisms underpinning such feedbacks, such as the allocation of recent plant assimilate, remain largely untested especially for plants forming tripartite symbioses. We tested how soils from under alder Alnus glutinosa and beneath other species of the same and different families affected alder growth and nutrition, and colonization of roots by nitrogen-fixing Frankia bacteria and ectomycorrhizal fungi. We also measured how the soil environment affected carbon capture and allocation by pulse labelling seedlings with 13CO 2. We then tested for linkages between foliar nutrient stoichiometry and carbon capture and allocation and soil origin using statistical modelling approaches. Performance of alder and nitrogen nutrition were best on home and birch Betula pendula soils (both Betulaceae), whereas performance on Douglas fir Pseudotsuga menziesii (Pinaceae) soil was poor. Plants growing in P. menziesii soil were virtually devoid of Frankia and ectomycorrhizas, and the natural abundance 15N signatures of leaves were more enriched indicating distinct nitrogen acquisition pathways. Seedlings in these soils also had smaller 13C fixation and root allocation rates, leading to smaller 13C respiration rates by microbes. Statistical models showed that the best predictors of foliar N concentration were 13C allocation rates to fine roots and net CO 2 exchange from the mesocosms. The best predictors for foliar phosphorus concentration were net CO 2 exchange from the mesocosms and soil origin; seedlings in home soils tended to have greater foliar phosphorus compared to birch soils while seedlings from Douglas fir soils were no different from the other treatments. Foliar phosphorus concentration was not correlated with plant available or total soil phosphorus for any of the soils. Home soils also resulted in distinct ectomycorrhizal communities on seedlings roots, which could be responsible for greater foliar phosphorus concentration. Our findings show how the association of alder with nitrogen-fixing Frankia relieved nitrogen limitation in the seedling triggering a performance feedback loop. We propose that relief of nitrogen limitation likely increases plant phosphorus demand, which may promote the formation of ectomycorrhizas in nutrient-deficient soils. The formation of tripartite symbioses therefore generates positive plant–soil feedbacks, which enables plants to acquire mineral nutrients otherwise inaccessible in trade for carbon. A free Plain Language Summary can be found within the Supporting Information of this article.

AB - Plant–soil feedbacks regulate plant productivity and diversity, but potential mechanisms underpinning such feedbacks, such as the allocation of recent plant assimilate, remain largely untested especially for plants forming tripartite symbioses. We tested how soils from under alder Alnus glutinosa and beneath other species of the same and different families affected alder growth and nutrition, and colonization of roots by nitrogen-fixing Frankia bacteria and ectomycorrhizal fungi. We also measured how the soil environment affected carbon capture and allocation by pulse labelling seedlings with 13CO 2. We then tested for linkages between foliar nutrient stoichiometry and carbon capture and allocation and soil origin using statistical modelling approaches. Performance of alder and nitrogen nutrition were best on home and birch Betula pendula soils (both Betulaceae), whereas performance on Douglas fir Pseudotsuga menziesii (Pinaceae) soil was poor. Plants growing in P. menziesii soil were virtually devoid of Frankia and ectomycorrhizas, and the natural abundance 15N signatures of leaves were more enriched indicating distinct nitrogen acquisition pathways. Seedlings in these soils also had smaller 13C fixation and root allocation rates, leading to smaller 13C respiration rates by microbes. Statistical models showed that the best predictors of foliar N concentration were 13C allocation rates to fine roots and net CO 2 exchange from the mesocosms. The best predictors for foliar phosphorus concentration were net CO 2 exchange from the mesocosms and soil origin; seedlings in home soils tended to have greater foliar phosphorus compared to birch soils while seedlings from Douglas fir soils were no different from the other treatments. Foliar phosphorus concentration was not correlated with plant available or total soil phosphorus for any of the soils. Home soils also resulted in distinct ectomycorrhizal communities on seedlings roots, which could be responsible for greater foliar phosphorus concentration. Our findings show how the association of alder with nitrogen-fixing Frankia relieved nitrogen limitation in the seedling triggering a performance feedback loop. We propose that relief of nitrogen limitation likely increases plant phosphorus demand, which may promote the formation of ectomycorrhizas in nutrient-deficient soils. The formation of tripartite symbioses therefore generates positive plant–soil feedbacks, which enables plants to acquire mineral nutrients otherwise inaccessible in trade for carbon. A free Plain Language Summary can be found within the Supporting Information of this article.

KW - Alnus glutinosa

KW - Frankia

KW - carbon allocation

KW - carbon-13

KW - ectomycorrhiza

KW - nitrogen

KW - phosphorus

U2 - 10.1111/1365-2435.13799

DO - 10.1111/1365-2435.13799

M3 - Journal article

VL - 35

SP - 1353

EP - 1365

JO - Functional Ecology

JF - Functional Ecology

SN - 0269-8463

IS - 6

ER -