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

• Published in: The New phytologist 2024-05, Vol.242 (4), p.1645-1660
• Main Authors: 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
• Format: Article
• Language: English
• Subjects: Carbon; Carbon content; ectomycorrhizal fungi; Ectomycorrhizas; Electromagnetic fields; Fluorescence; Fungi; Host plants; Inoculation; Iron; iron cycling; Low frequency; Metabolites; meta‐transcriptomics; Microorganisms; Molecular modelling; nuclear magnetic resonance spectroscopy; Pine trees; Pinus; Plant growth; Plant roots; Plants; Rhizosphere; Rhizosphere microorganisms; Roots; Suillus; Symbionts; Symbiosis; Transcriptomics; X‐ray micro‐fluorescence
• ISSN: 0028-646X; 1469-8137
• DOI: 10.1111/nph.19449

Summary 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.