I am interested in the development of ectomycorrhizal symbioses. This type of symbiosis forms naturally between the majority of temperate and boreal forest trees and soil fungi. Ectomycorrhizal fungi exploit the soil very efficiently to absorb nutrients (N, P) through their extensive hyphal networks. A part of these nutrients is exchanged with the plant for photosynthetic sugars. The nutrient exchange benefits both the plant and the fungus and stimulates their respective growth. Despite the high economic and ecological value of the ectomycorrhizal symbiosis, the molecular mechanisms that trigger ectomycorrhiza establishment remain largely unknown.
JudithFelten 1150
Ectomycorrhizal roots (ECM) (Figure 1) are characterized by three tissues: a fungal mantle surrounding the root from which extramatrical hyphae reach out into the soil to gather nutrients (N, P). These nutrients are exchanged with the plant for photosynthetic derived sugars in the Hartig Net, where a number of specific plant and fungal transport proteins are expressed (Martin and Nehls, Current Opinion in Plant Biology 2009). The structure of the Hartig Net is characterized by fungal hyphae that invade the apoplastic space between root epidermis/cortex cells (Figure 1C).Figure1
Figure 1: A Ectomycorrhizal roots of Populus and Laccaria bicolor. Note the swollen and short nature of the ectomycorrhizal roots. B Light microscopy image of a transverse section through an ectomycorrhizal root. C Magnified light microscopy image of the Hartig Net. Cortex (Co), Epidermis (E), Mantle (M), Hartig Net (HN). Pictures: Judith Felten

Hartig Net development requires loosening of the radial wall between adjacent epidermis cells. This process involves degradation of the middle lamella between these cells. It has been proposed that fungus- and plant-derived enzymes from the Carbohydrate Active Enzyme (CAzyme) family, which have the potential to modify cell wall polymers, could mediate the cell wall release. Fungal genes coding for CAzymes have been identified in Laccaria bicolor and Tuber melanosporum ECM (Balestrini et al., Current Genetics 2012; Veneault-Fourrey et al., Fungal Genetics and Biology 2014; Sillo et al., Planta 2016) and some of these are induced within the HN (Hacquard et al., Environmental Microbiology 2013). However, functional analyses that show the requirement of these genes for Hartig Net formation are still widely lacking. Furthermore, ectomycorrhizal fungi secrete effectors such as Mycorrhiza induced Small Secreted Protein 7 (MiSSP7), which can be taken up into the plant and trigger plant responses that may contribute to cell wall release (Plett et al., Current Biology 2011). MiSSP7 is required for Hartig Net formation and fungal strains of L. bicolor that lack this peptide form only a very shallow Hartig Net, suggesting that even plant-triggered processes are required for Hartig Net formation. Fungal auxin is yet another fungal factor that is likely to contribute to cell wall remodelling and Hartig Net formation (Gay et al., New Phytologist 1994), but again functional studies are needed to prove this assumption and how auxin may interact with effectors and CAzymes remains to be investigated. The different categories of actors potentially contributing to cell wall remodelling and Hartig Net formation are depicted in Figure 2.
Figure 2Figure 2: Processes involved in Hartig Net formation. Fungal hyphae release polysaccharide material and adhere to the root surface. Apoplastic fungal effectors, fungal CAzymes and fungal auxin are released into the apoplastic space and may contribute to the degradation of the middle lamella, permitting fungal invasion of the apoplastic space. The fungus also releases cytoplasmic effectors that are taken up through endocytosis into the plant cell. These effectors trigger plant responses. Such responses could lead to production/release of CAzymes and plant-derived auxin that may participate in the degradation of the middle lamella. Picture: Judith FeltenThe aim of my research is to uncover the nature of cell wall remodelling during Hartig Net establishment and to reveal the crucial molecular factors behind this process and their interplay. In my group we are using an elegant combination of state of the art cell wall analysis techniques together with microscopy, hormone metabolomics, transcriptomics and cell biology on material from ectomycorrhiza from gymnosperm and angiosperm trees with fungi having different mycorrhization capacity, to reveal the nature of cell wall remodelling required for Hartig Net establishment. An important tool that we have extensively developed is Raman micro-spectroscopy (Felten et al., Nature protocols 2015). Data about chemical cell wall remodelling will be combined and correlated with genomics and metabolomics data, revealing the key molecular actors for cell wall remodelling. Another aspect of my research is focused on auxin fluxes between root cells and hyphae and how this process mediates Hartig Net formation.

Publication list

  1. The mycorrhizal tragedy of the commons
    Ecol Lett. 2021 Mar 22 Online ahead of print
  2. Fluorescent protein expression in the ectomycorrhizal fungus Laccaria bicolor: a plasmid toolkit for easy use of fluorescent markers in basidiomycetes
    Curr Genet. 2020 Mar 14 [Epub ahead of print]
  3. Ethylene Signaling Is Required for Fully Functional Tension Wood in Hybrid Aspen
  4. An AP2/ERF transcription factor ERF139 coordinates xylem cell expansion and secondary cell wall deposition
    New Phytol. 2019, 224(4):1585-1599
  5. Ethylene-Related Gene Expression Networks in Wood Formation
  6. Ethylene signaling induces gelatinous layers with typical features of tension wood in hybrid aspen
    New Phytol. 2018, 218 (3):999-1014
  7. Sharing resources for mutual benefit: crosstalk between disciplines deepens the understanding of mycorrhizal symbioses across scales
    New Phytol. 2018, 217(1):29-32
  8. Volatile signalling by sesquiterpenes from ectomycorrhizal fungi reprogrammes root architecture
    Nat Commun. 2015 Feb 23;6:6279
  9. Development of the Populus-Laccaria bicolor ectomycorrhiza modifies root auxin metabolism, signalling and response
    Plant Physiol. 2015, 169(1):890-902
  10. Vibrational spectroscopic image analysis of biological material using multivariate curve resolution-alternating least squares (MCR-ALS)
    Nat Protoc. 2015 Feb;10(2):217-240 Epub 2015 Jan 8
  11. Arabidopsis WAT1 is a vacuolar auxin transport facilitator required for auxin homoeostasis
    Nat Commun. 2013; 4:2625
  12. A genome-wide screen for ethylene-induced ethylene response factors (ERFs) in hybrid aspen stem identifies ERF genes that modify stem growth and wood properties
    New Phytol. 2013; 200(2):511-22

  13. Felten J, Kohler A, Morin E, Bhalerao RP, Palme K, Martin F, Ditengou FA, Legue V
    The ectomycorrhizal fungus Laccaria bicolor stimulates lateral root formation in poplar and Arabidopsis through auxin transport and signaling
    Plant Physiology: 2008 151:1991-2005