Cellular and Molecular Basis of Plant-Fungal Interactions in Mycorrhizas

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Plant Microbe Interactions".

Deadline for manuscript submissions: closed (30 October 2021) | Viewed by 20704

Special Issue Editors


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Guest Editor
Department of Life science and System Biology, Università di Torino, Torino, Italy
Interests: plant-microbe interactions; omics applied to mycorrhizas; microbes and agriculture; endobacteria

E-Mail Website
Guest Editor
Department of Life Sciences and Systems Biology, University of Torino, 10126 Turin, Italy
Interests: molecular and cellular aspects of plant–microbe interactions, mainly during arbuscular mycorrhizal symbiosis; plant response to biotic stress; role of phytohormones in plant growth and in response to microbes; apocarotenoids
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Special Issue Information

Dear Colleagues,

What is the secret of the pervasive power of mycorrhizas and of their ecological success in all the environments of our planet? Mycorrhizal interactions involve more than 300,000 land plants and at least 50,000 fungal species belonging to all the major fungal taxa (from the Mucoromycota to Basidiomycota). They appear equally successful in colonizing different environments, from alpine and boreal zones to tropical forests and grasslands. This immense biodiversity leads to multiple methods of interaction, which differ in environmental adaptations, genetics, and physiology of the partners. However, many interesting similarities can be traced exploring the complexity of cell-to-cell contacts between plants and fungi, the molecules and the signaling pathways, which allow the establishment of the symbiosis, as well as the regulation of molecular determinants, which control downstream events leading to colonization and nutrient exchanges.

The aim of this Special Issue is to provide an updated view of what happens when the evolutionary pathways of fungi and plants cross each other leading to mycorrhizal symbiosis. Both original research and review contributions based on the most updated cell biology, analytical and molecular approaches applied to all the diverse mycorrhizal associations are welcome.

Prof. Dr. Paola Bonfante
Dr. Valentina Fiorilli
Guest Editors

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Keywords

  • confocal microscopy
  • “omics“ approaches
  • mutants
  • signaling molecules
  • effectors
  • plant and fungal membranes
  • epigenetics
  • natural variation
  • Hormones

  • Strigolactones

  • Nutrients

  • Phosphate

  • Defence response

  • Reporter genes

  • Mycorrhiza-induced resistance

  • Plant-mycorrhizal fungi-pathogen interaction

  • Priming

  • Nutrient transfer imaging 

Published Papers (5 papers)

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Research

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23 pages, 3392 KiB  
Article
A Transcriptomic Atlas of the Ectomycorrhizal Fungus Laccaria bicolor
by Joske Ruytinx, Shingo Miyauchi, Sebastian Hartmann-Wittulsky, Maíra de Freitas Pereira, Frédéric Guinet, Jean-Louis Churin, Carine Put, François Le Tacon, Claire Veneault-Fourrey, Francis Martin and Annegret Kohler
Microorganisms 2021, 9(12), 2612; https://doi.org/10.3390/microorganisms9122612 - 17 Dec 2021
Cited by 10 | Viewed by 5356
Abstract
Trees are able to colonize, establish and survive in a wide range of soils through associations with ectomycorrhizal (EcM) fungi. Proper functioning of EcM fungi implies the differentiation of structures within the fungal colony. A symbiotic structure is dedicated to nutrient exchange and [...] Read more.
Trees are able to colonize, establish and survive in a wide range of soils through associations with ectomycorrhizal (EcM) fungi. Proper functioning of EcM fungi implies the differentiation of structures within the fungal colony. A symbiotic structure is dedicated to nutrient exchange and the extramatricular mycelium explores soil for nutrients. Eventually, basidiocarps develop to assure last stages of sexual reproduction. The aim of this study is to understand how an EcM fungus uses its gene set to support functional differentiation and development of specialized morphological structures. We examined the transcriptomes of Laccaria bicolor under a series of experimental setups, including the growth with Populus tremula x alba at different developmental stages, basidiocarps and free-living mycelium, under various conditions of N, P and C supply. In particular, N supply induced global transcriptional changes, whereas responses to P supply seemed to be independent from it. Symbiosis development with poplar is characterized by transcriptional waves. Basidiocarp development shares transcriptional signatures with other basidiomycetes. Overlaps in transcriptional responses of L. bicolor hyphae to a host plant and N/C supply next to co-regulation of genes in basidiocarps and mature mycorrhiza were detected. Few genes are induced in a single condition only, but functional and morphological differentiation rather involves fine tuning of larger gene sets. Overall, this transcriptomic atlas builds a reference to study the function and stability of EcM symbiosis in distinct conditions using L. bicolor as a model and indicates both similarities and differences with other ectomycorrhizal fungi, allowing researchers to distinguish conserved processes such as basidiocarp development from nutrient homeostasis. Full article
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10 pages, 1686 KiB  
Article
Allocation of Carbon from an Arbuscular Mycorrhizal Fungus, Gigaspora margarita, to Its Gram-Negative and Positive Endobacteria Revealed by High-Resolution Secondary Ion Mass Spectrometry
by Yukari Kuga, Ting-Di Wu, Naoya Sakamoto, Chie Katsuyama and Hisayoshi Yurimoto
Microorganisms 2021, 9(12), 2597; https://doi.org/10.3390/microorganisms9122597 - 16 Dec 2021
Cited by 2 | Viewed by 2604
Abstract
Arbuscular mycorrhizal fungi are obligate symbionts of land plants; furthermore, some of the species harbor endobacteria. Although the molecular approach increased our knowledge of the diversity and origin of the endosymbiosis and its metabolic possibilities, experiments to address the functions of the fungal [...] Read more.
Arbuscular mycorrhizal fungi are obligate symbionts of land plants; furthermore, some of the species harbor endobacteria. Although the molecular approach increased our knowledge of the diversity and origin of the endosymbiosis and its metabolic possibilities, experiments to address the functions of the fungal host have been limited. In this study, a C flow of the fungus to the bacteria was investigated. Onion seedlings colonized with Gigaspora margarita, possessing Candidatus Glomeribacter gigasporarum (CaGg, Gram-negative, resides in vacuole) and Candidatus Moeniiplasma glomeromycotorum (CaMg, Gram-positive, resides in the cytoplasm,) were labelled with 13CO2. The 13C localization within the mycorrhiza was analyzed using high-resolution secondary ion mass spectrometry (SIMS). Correlative TEM-SIMS analysis of the fungal cells revealed that the 13C/12C ratio of CaGg was the lowest among CaMg and mitochondria and was the highest in the cytoplasm. By contrast, the plant cells, mitochondria, plastids, and fungal cytoplasm, which are contributors to the host, showed significantly higher 13C enrichment than the host cytoplasm. The C allocation patterns implied that CaMg has a greater impact than CaGg on G. margarita, but both seemed to be less burdensome to the host fungus in terms of C cost. Full article
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13 pages, 2427 KiB  
Article
Novel Microdialysis Technique Reveals a Dramatic Shift in Metabolite Secretion during the Early Stages of the Interaction between the Ectomycorrhizal Fungus Pisolithus microcarpus and Its Host Eucalyptus grandis
by Krista L. Plett, Scott Buckley, Jonathan M. Plett, Ian C. Anderson, Judith Lundberg-Felten and Sandra Jämtgård
Microorganisms 2021, 9(9), 1817; https://doi.org/10.3390/microorganisms9091817 - 26 Aug 2021
Cited by 4 | Viewed by 2847
Abstract
The colonisation of tree roots by ectomycorrhizal (ECM) fungi is the result of numerous signalling exchanges between organisms, many of which occur before physical contact. However, information is lacking about these exchanges and the compounds that are secreted by each organism before contact. [...] Read more.
The colonisation of tree roots by ectomycorrhizal (ECM) fungi is the result of numerous signalling exchanges between organisms, many of which occur before physical contact. However, information is lacking about these exchanges and the compounds that are secreted by each organism before contact. This is in part due to a lack of low disturbance sampling methods with sufficient temporal and spatial resolution to capture these exchanges. Using a novel in situ microdialysis approach, we sampled metabolites released from Eucalyptus grandis and Pisolithus microcarpus independently and during indirect contact over a 48-h time-course using UPLC-MS. A total of 560 and 1530 molecular features (MFs; ESI- and ESI+ respectively) were identified with significant differential abundance from control treatments. We observed that indirect contact between organisms altered the secretion of MFs to produce a distinct metabolomic profile compared to either organism independently. Many of these MFs were produced within the first hour of contact and included several phenylpropanoids, fatty acids and organic acids. These findings show that the secreted metabolome, particularly of the ECM fungus, can rapidly shift during the early stages of pre-symbiotic contact and highlight the importance of observing these early interactions in greater detail. We present microdialysis as a useful tool for examining plant–fungal signalling with high temporal resolution and with minimal experimental disturbance. Full article
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33 pages, 8937 KiB  
Article
Genome-Wide Analysis of Nutrient Signaling Pathways Conserved in Arbuscular Mycorrhizal Fungi
by Xiaoqin Zhou, Jiangyong Li, Nianwu Tang, Hongyun Xie, Xiaoning Fan, Hui Chen, Ming Tang and Xianan Xie
Microorganisms 2021, 9(8), 1557; https://doi.org/10.3390/microorganisms9081557 - 22 Jul 2021
Cited by 9 | Viewed by 4629
Abstract
Arbuscular mycorrhizal (AM) fungi form a mutualistic symbiosis with a majority of terrestrial vascular plants. To achieve an efficient nutrient trade with their hosts, AM fungi sense external and internal nutrients, and integrate different hierarchic regulations to optimize nutrient acquisition and homeostasis during [...] Read more.
Arbuscular mycorrhizal (AM) fungi form a mutualistic symbiosis with a majority of terrestrial vascular plants. To achieve an efficient nutrient trade with their hosts, AM fungi sense external and internal nutrients, and integrate different hierarchic regulations to optimize nutrient acquisition and homeostasis during mycorrhization. However, the underlying molecular networks in AM fungi orchestrating the nutrient sensing and signaling remain elusive. Based on homology search, we here found that at least 72 gene components involved in four nutrient sensing and signaling pathways, including cAMP-dependent protein kinase A (cAMP-PKA), sucrose non-fermenting 1 (SNF1) protein kinase, target of rapamycin kinase (TOR) and phosphate (PHO) signaling cascades, are well conserved in AM fungi. Based on the knowledge known in model yeast and filamentous fungi, we outlined the possible gene networks functioning in AM fungi. These pathways may regulate the expression of downstream genes involved in nutrient transport, lipid metabolism, trehalase activity, stress resistance and autophagy. The RNA-seq analysis and qRT-PCR results of some core genes further indicate that these pathways may play important roles in spore germination, appressorium formation, arbuscule longevity and sporulation of AM fungi. We hope to inspire further studies on the roles of these candidate genes involved in these nutrient sensing and signaling pathways in AM fungi and AM symbiosis. Full article
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Review

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20 pages, 1262 KiB  
Review
An Updated Review on the Modulation of Carbon Partitioning and Allocation in Arbuscular Mycorrhizal Plants
by Isaac A. Salmeron-Santiago, Miguel Martínez-Trujillo, Juan J. Valdez-Alarcón, Martha E. Pedraza-Santos, Gustavo Santoyo, María J. Pozo and Ana T. Chávez-Bárcenas
Microorganisms 2022, 10(1), 75; https://doi.org/10.3390/microorganisms10010075 - 30 Dec 2021
Cited by 22 | Viewed by 4136
Abstract
Arbuscular mycorrhizal fungi (AMF) are obligate biotrophs that supply mineral nutrients to the host plant in exchange for carbon derived from photosynthesis. Sucrose is the end-product of photosynthesis and the main compound used by plants to translocate photosynthates to non-photosynthetic tissues. AMF alter [...] Read more.
Arbuscular mycorrhizal fungi (AMF) are obligate biotrophs that supply mineral nutrients to the host plant in exchange for carbon derived from photosynthesis. Sucrose is the end-product of photosynthesis and the main compound used by plants to translocate photosynthates to non-photosynthetic tissues. AMF alter carbon distribution in plants by modifying the expression and activity of key enzymes of sucrose biosynthesis, transport, and/or catabolism. Since sucrose is essential for the maintenance of all metabolic and physiological processes, the modifications addressed by AMF can significantly affect plant development and stress responses. AMF also modulate plant lipid biosynthesis to acquire storage reserves, generate biomass, and fulfill its life cycle. In this review we address the most relevant aspects of the influence of AMF on sucrose and lipid metabolism in plants, including its effects on sucrose biosynthesis both in photosynthetic and heterotrophic tissues, and the influence of sucrose on lipid biosynthesis in the context of the symbiosis. We present a hypothetical model of carbon partitioning between plants and AMF in which the coordinated action of sucrose biosynthesis, transport, and catabolism plays a role in the generation of hexose gradients to supply carbon to AMF, and to control the amount of carbon assigned to the fungus. Full article
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