Skip to main content
OSTI.GOVU.S. Department of Energy Office of Scientific and Technical Information
U.S. Department of Energy
Office of Scientific and Technical Information
 

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

Journal Article · · New Phytologist
DOI:https://doi.org/10.1111/nph.19449· OSTI ID:2341724
 [1];  [1];  [2];  [3];  [4];  [5];  [5];  [5];  [6];  [7];  [7];  [8];  [1]
  1. University of Florida, Quincy, FL (United States); University of Florida, Gainesville, FL (United States)
  2. Brookhaven National Laboratory (BNL), Upton, NY (United States)
  3. Boston University, MA (United States)
  4. Duke University, Durham, NC (United States)
  5. USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
  6. USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); University of California, Berkeley, CA (United States)
  7. Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)
  8. Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Biological Sciences Division
+ Show Author Affiliations
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. Here, 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.
Research Organization:
Boston Univ., MA (United States); Brookhaven National Laboratory (BNL), Upton, NY (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Organization:
National Science Foundation (NSF); USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC02-05CH11231; AC05-76RL01830; SC0012704; SC0020403
OSTI ID:
2341724
Alternate ID(s):
OSTI ID: 2440566
OSTI ID: 2229832
OSTI ID: 2570208
Report Number(s):
BNL--226007-2024-JAAM; PNNL-SA--189714
Journal Information:
New Phytologist, Journal Name: New Phytologist Journal Issue: 4 Vol. 242; ISSN 0028-646X
Publisher:
WileyCopyright Statement
Country of Publication:
United States
Language:
English

References (65)

Ectomycorrhizal‐fungal colonization induces physio‐morphological changes in Quercus serrata leaves and roots journal November 2012
Structure and function of enzymes in heme biosynthesis journal May 2010
Metabolite, Protein, and Lipid Extraction (MPLEx): A Method that Simultaneously Inactivates Middle East Respiratory Syndrome Coronavirus and Allows Analysis of Multiple Host Cell Components Following Infection book December 2019
Siderophores of Symbiotic Fungi book January 2007
Absolute microbiome profiling highlights the links among microbial stability, soil health, and crop productivity under long-term sod-based rotation journal October 2022
Exploration types of ectomycorrhizae journal June 2001
Hydroxamate siderophores of the ectomycorrhizal fungi Suillus granulatus and S. luteus journal October 2010
Micro-analytical, physiological and molecular aspects of Fe acquisition in leaves of Fe-deficient tomato plants re-supplied with natural Fe-complexes in nutrient solution journal June 2009
How metal-tolerant ecotypes of ectomycorrhizal fungi protect plants from heavy metal pollution journal January 2011
Chapter 12 Role of Iron in Plant–Microbe Interactions book September 2009
Integrating perennial bahiagrass into the conventional rotation of cotton and peanut enhances interactions between microbial and nematode communities journal February 2022
Ferrochelatase activity of plant frataxin journal January 2019
Ectomycorrhizal fungi affect Scots pine photosynthesis through nitrogen and water economy, not only through increased carbon demand journal January 2015
Fe(III)-complexes of the tripodal trishydroxamate siderophore basidiochrome: Potential biological implications journal December 2011
Disentangling the role of ectomycorrhizal fungi in plant nutrient acquisition along a Zn gradient using X-ray imaging journal December 2021
Biogenesis of iron–sulfur proteins in plants journal July 2005
Iron nutrition, biomass production, and plant product quality journal January 2015
Enzymes, Manganese, or Iron? Drivers of Oxidative Organic Matter Decomposition in Soils journal October 2020
Structural Fe(II) Oxidation in Biotite by an Ectomycorrhizal Fungi Drives Mechanical Forcing journal May 2016
Iron Uptake and Transport in Plants: The Good, the Bad, and the Ionome journal October 2009
Random Forests journal January 2001
Metal toxicity and ectomycorrhizas journal June 2000
Microbial regulation of the soil carbon cycle: evidence from gene–enzyme relationships journal May 2016
Fast gapped-read alignment with Bowtie 2 journal March 2012
De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis journal July 2013
Iron-mediated organic matter decomposition in humid soils can counteract protection journal May 2020
Oxalate secretion by ectomycorrhizal Paxillus involutus is mineral-specific and controls calcium weathering from minerals journal July 2015
Iron homeostasis in plants – a brief overview journal January 2017
Three rice nicotianamine synthase genes, OsNAS1, OsNAS2, and OsNAS3 are expressed in cells involved in long-distance transport of iron and differentially regulated by iron journal November 2003
Carbohydrate metabolism in ectomycorrhizas: gene expression, monosaccharide transport and metabolic control journal June 2001
A zinc-adapted fungus protects pines from zinc stress journal February 2004
Evolution of Iron Acquisition in Higher Plants journal July 2006
An underground tale: contribution of microbial activity to plant iron acquisition via ecological processes journal November 2013
SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data journal October 2012
InterProScan 5: genome-scale protein function classification journal January 2014
eggNOG-mapper v2: Functional Annotation, Orthology Assignments, and Domain Prediction at the Metagenomic Scale journal October 2021
Iron: Nutritious, Noxious, and Not Readily Available journal March 1994
The Analysis of Arabidopsis Nicotianamine Synthase Mutants Reveals Functions for Nicotianamine in Seed Iron Loading and Iron Deficiency Responses journal March 2009
Evidence for a Specific Uptake System for Iron Phytosiderophores in Roots of Grasses journal January 1986
Metatranscriptomic analysis of ectomycorrhizal roots reveals genes associated with P iloderma- P inus symbiosis: improved methodologies for assessing gene expression in situ : Metatranscriptomic analysis of ectomycorrhizae journal October 2014
Ectomycorrhizal fungal response to warming is linked to poor host performance at the boreal‐temperate ecotone journal September 2016
Patterns of structural and defense investments in fine roots of Scots pine ( Pinus sylvestris L.) across a strong temperature and latitudinal gradient in Europe journal October 2016
Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems journal November 2009
Sucrose Utilization of the Ectomycorrhizal Fungi Amanita muscaria and Hebeloma crustuliniforme Depends on the Cell Wall‐bound Invertase Activity of their Host Picea abies journal December 1991
A strong species?area relationship for eukaryotic soil microbes: island size matters for ectomycorrhizal fungi journal June 2007
Priority effects determine the outcome of ectomycorrhizal competition between two Rhizopogon species colonizing Pinus muricata seedlings journal February 2005
Ectomycorrhizal fungi and interspecific competition: species interactions, community structure, coexistence mechanisms, and future research directions: Tansley review journal July 2010
Continental-level population differentiation and environmental adaptation in the mushroom Suillus brevipes journal November 2016
Determining place and process: functional traits of ectomycorrhizal fungi that affect both community structure and ecosystem function journal October 2013
Exploring the role of ectomycorrhizal fungi in soil carbon dynamics journal February 2019
Comparative genomics reveals dynamic genome evolution in host specialist ectomycorrhizal fungi journal February 2021
The fungal collaboration gradient dominates the root economics space in plants journal July 2020
Involutin Is an Fe 3+ Reductant Secreted by the Ectomycorrhizal Fungus Paxillus involutus during Fenton-Based Decomposition of Organic Matter journal October 2015
Iron Uptake, Translocation, and Regulation in Higher Plants journal June 2012
Differential expression analysis for sequence count data journal October 2010
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 journal December 2014
Metatranscriptomic Study of Common and Host-Specific Patterns of Gene Expression between Pines and Their Symbiotic Ectomycorrhizal Fungi in the Genus Suillus journal October 2016
Cutadapt removes adapter sequences from high-throughput sequencing reads journal May 2011
Consistent and Clear Reporting of Results from Diverse Modeling Techniques: The A3 Method journal January 2015
The role of fungi in weathering journal June 2004
Heterospecific Neighbor Plants Impact Root Microbiome Diversity and Molecular Function of Root Fungi journal November 2021
Allocation of Heme Is Differentially Regulated by Ferrochelatase Isoforms in Arabidopsis Cells journal August 2016
Importance of the Rhizosphere Microbiota in Iron Biofortification of Plants journal December 2021
Mfuzz: A software package for soft clustering of microarray data journal May 2007
Competition-function tradeoffs in ectomycorrhizal fungi journal January 2016

Similar Records

Related Subjects

36 MATERIALS SCIENCE
59 BASIC BIOLOGICAL SCIENCES
Ectomycorrhizal fungi
Suillus
ectomycorrhizal fungi
iron cycling
meta-transcriptomics
nuclear magnetic resonance spectroscopy
x-ray micro-fluorescence