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Ectomycorrhizal fungi enhance pine growth by stimulating iron‐dependent mechanisms with trade‐offs in symbiotic performance

Published in:

New Phytologist ( 2023)

Author(s):

Zhang, Kaile, Wang, Haihua, Tappero, Ryan, Bhatnagar, Jennifer M., Vilgalys, Rytas, Barry, Kerrie, Keymanesh, Keykhosrow, Tejomurthula, Sravanthi, Grigoriev, Igor V., Kew, William R., Eder, Elizabeth K., Nicora, Carrie D., Liao, Hui‐Ling

DOI:

10.1111/nph.19449

Abstract:

Iron (Fe) is crucial for metabolic functions of living organisms. Plants access occluded Fe through interactions with rhizosphere microorganisms and symbionts. Yet, the interplay between Fe addition and plant-mycorrhizal interactions, especially the molecular mechanisms underlying mycorrhiza-assisted Fe processing in plants, remains largely unexplored. We conducted mesocosms in Pinus plants inoculated with different ectomycorrhizal fungi (EMF) Suillus species under conditions with and without Fe coatings. Meta-transcriptomic, biogeochemical, and X-ray fluorescence imaging analyses were applied to investigate early-stage mycorrhizal roots. While Fe addition promoted Pinus growth, it concurrently reduced mycorrhiza formation rate, symbiosis-related metabolites in plant roots, and aboveground plant carbon and macronutrient content. This suggested potential trade-offs between Fe-enhanced plant growth and symbiotic performance. However, the extent of this trade-off may depend on interactions between host plants and EMF species. Interestingly, dual EMF species were more effective at facilitating plant Fe uptake by inducing diverse Fe-related functions than single-EMF species. This subsequently triggered various Fe-dependent physiological and biochemical processes in Pinus roots, significantly contributing to Pinus growth. However, this resulted in a greater carbon allocation to roots, relatively reducing the aboveground plant carbon content. Our study offers critical insights into how EMF communities rebalance benefits of Fe-induced effects on symbiotic partners.

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