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

Author:

Zhang Kaile12ORCID,Wang Haihua12ORCID,Tappero Ryan3ORCID,Bhatnagar Jennifer M.4ORCID,Vilgalys Rytas5ORCID,Barry Kerrie6ORCID,Keymanesh Keykhosrow6ORCID,Tejomurthula Sravanthi6ORCID,Grigoriev Igor V.67ORCID,Kew William R.8ORCID,Eder Elizabeth K.8ORCID,Nicora Carrie D.9ORCID,Liao Hui‐Ling12ORCID

Affiliation:

1. North Florida Research and Education Center University of Florida 155 Research Road Quincy FL 32351 USA

2. Department of Soil, Water, and Ecosystem Sciences University of Florida Gainesville FL 32611 USA

3. Brookhaven National Laboratory, NSLS‐II Upton NY 11973 USA

4. Department of Biology Boston University Boston MA 02215 USA

5. Department of Biology Duke University 130 Science Drive Durham NC 27708 USA

6. U.S. Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory Berkeley CA 94720 USA

7. Department of Plant and Microbial Biology University of California Berkeley CA 94720 USA

8. Environmental Molecular Science Laboratory, Pacific Northwest National Laboratory Richland WA 99354 USA

9. Biological Sciences Division, Pacific Northwest National Laboratory Richland WA 99354 USA

Abstract

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.

Funder

Biological and Environmental Research

Division of Integrative Organismal Systems

National Institute of Food and Agriculture

Publisher

Wiley

Subject

Plant Science,Physiology

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