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

Publication ,  Journal Article
Zhang, K; Wang, H; Tappero, R; Bhatnagar, JM; Vilgalys, R; Barry, K; Keymanesh, K; Tejomurthula, S; Grigoriev, IV; Kew, WR; Eder, EK ...
Published in: The New phytologist
May 2024

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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Published In

The New phytologist

DOI

EISSN

1469-8137

ISSN

1469-8137

Publication Date

May 2024

Volume

242

Issue

4

Start / End Page

1645 / 1660

Related Subject Headings

  • Symbiosis
  • Plant Roots
  • Plant Biology & Botany
  • Pinus
  • Mycorrhizae
  • Iron
  • 4102 Ecological applications
  • 4101 Climate change impacts and adaptation
  • 3108 Plant biology
  • 07 Agricultural and Veterinary Sciences
 

Citation

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Zhang, K., Wang, H., Tappero, R., Bhatnagar, J. M., Vilgalys, R., Barry, K., … Liao, H.-L. (2024). Ectomycorrhizal fungi enhance pine growth by stimulating iron-dependent mechanisms with trade-offs in symbiotic performance. The New Phytologist, 242(4), 1645–1660. https://doi.org/10.1111/nph.19449
Zhang, Kaile, Haihua Wang, Ryan Tappero, Jennifer M. Bhatnagar, Rytas Vilgalys, Kerrie Barry, Keykhosrow Keymanesh, et al. “Ectomycorrhizal fungi enhance pine growth by stimulating iron-dependent mechanisms with trade-offs in symbiotic performance.The New Phytologist 242, no. 4 (May 2024): 1645–60. https://doi.org/10.1111/nph.19449.
Zhang K, Wang H, Tappero R, Bhatnagar JM, Vilgalys R, Barry K, et al. Ectomycorrhizal fungi enhance pine growth by stimulating iron-dependent mechanisms with trade-offs in symbiotic performance. The New phytologist. 2024 May;242(4):1645–60.
Zhang, Kaile, et al. “Ectomycorrhizal fungi enhance pine growth by stimulating iron-dependent mechanisms with trade-offs in symbiotic performance.The New Phytologist, vol. 242, no. 4, May 2024, pp. 1645–60. Epmc, doi:10.1111/nph.19449.
Zhang K, Wang H, Tappero R, Bhatnagar JM, Vilgalys R, Barry K, Keymanesh K, Tejomurthula S, Grigoriev IV, Kew WR, Eder EK, Nicora CD, Liao H-L. Ectomycorrhizal fungi enhance pine growth by stimulating iron-dependent mechanisms with trade-offs in symbiotic performance. The New phytologist. 2024 May;242(4):1645–1660.
Journal cover image

Published In

The New phytologist

DOI

EISSN

1469-8137

ISSN

1469-8137

Publication Date

May 2024

Volume

242

Issue

4

Start / End Page

1645 / 1660

Related Subject Headings

  • Symbiosis
  • Plant Roots
  • Plant Biology & Botany
  • Pinus
  • Mycorrhizae
  • Iron
  • 4102 Ecological applications
  • 4101 Climate change impacts and adaptation
  • 3108 Plant biology
  • 07 Agricultural and Veterinary Sciences