Kaile Zhang, Haihua Wang, Ryan Tappero, Jennifer M. Bhatnagar, Rytas Vilgalys, Kerrie Barry, Keykhosrow Keymanesh, Sravanthi Tejomurthula, Igor V. Grigoriev, William R. Kew, Elizabeth K. Eder, Carrie D. Nicora, Hui-Ling Liao
{"title":"Ectomycorrhizal fungi enhance pine growth by stimulating iron-dependent mechanisms with trade-offs in symbiotic performance","authors":"Kaile Zhang, Haihua Wang, Ryan Tappero, Jennifer M. Bhatnagar, Rytas Vilgalys, Kerrie Barry, Keykhosrow Keymanesh, Sravanthi Tejomurthula, Igor V. Grigoriev, William R. Kew, Elizabeth K. Eder, Carrie D. Nicora, Hui-Ling Liao","doi":"10.1111/nph.19449","DOIUrl":null,"url":null,"abstract":"<div>\n \n <p>\n \n </p><ul>\n \n \n <li>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.</li>\n \n \n <li>We conducted mesocosms in <i>Pinus</i> plants inoculated with different ectomycorrhizal fungi (EMF) <i>Suillus</i> 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.</li>\n \n \n <li>While Fe addition promoted <i>Pinus</i> 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 <i>Pinus</i> roots, significantly contributing to <i>Pinus</i> growth. However, this resulted in a greater carbon allocation to roots, relatively reducing the aboveground plant carbon content.</li>\n \n \n <li>Our study offers critical insights into how EMF communities rebalance benefits of Fe-induced effects on symbiotic partners.</li>\n </ul>\n \n </div>","PeriodicalId":214,"journal":{"name":"New Phytologist","volume":"242 4","pages":"1645-1660"},"PeriodicalIF":8.3000,"publicationDate":"2023-12-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"New Phytologist","FirstCategoryId":"99","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1111/nph.19449","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"PLANT SCIENCES","Score":null,"Total":0}
引用次数: 0
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.
期刊介绍:
New Phytologist is an international electronic journal published 24 times a year. It is owned by the New Phytologist Foundation, a non-profit-making charitable organization dedicated to promoting plant science. The journal publishes excellent, novel, rigorous, and timely research and scholarship in plant science and its applications. The articles cover topics in five sections: Physiology & Development, Environment, Interaction, Evolution, and Transformative Plant Biotechnology. These sections encompass intracellular processes, global environmental change, and encourage cross-disciplinary approaches. The journal recognizes the use of techniques from molecular and cell biology, functional genomics, modeling, and system-based approaches in plant science. Abstracting and Indexing Information for New Phytologist includes Academic Search, AgBiotech News & Information, Agroforestry Abstracts, Biochemistry & Biophysics Citation Index, Botanical Pesticides, CAB Abstracts®, Environment Index, Global Health, and Plant Breeding Abstracts, and others.