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Genome-wide analysis of the cell-layer specific expression of pathogen-induced genes in the Arabidopsis root

Subject Area Organismic Interactions, Chemical Ecology and Microbiomes of Plant Systems
Term from 2012 to 2021
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 226284840
 
Final Report Year 2021

Final Report Abstract

Plant roots are constantly challenged by a multitude of surrounding microbes. As roots are built of concentric cell-layers, it has been anticipated, that these respond to microbial infection by employing specific, genetically defined programs. Nevertheless, the functional impact of the radial organization remains largely elusive, particularly due to the lack of adequate genome-wide techniques to monitor expression on cell-layer resolution. Here, cell-type specific expression of tagged ribosomes enabled isolation and sequencing of ribosome-bound mRNA to obtain celllayer translatomes (TRAPseq, infection-based Translating Ribosome Affinity Purification followed by sequencing). Our analyses clearly supported the view that neighbouring root celllayers responded to microbial infections with highly unique gene expression patterns. After inoculation with the vascular pathogen Verticillium longisporum, the pathogenic oomycete Phytophthora parasitica or the mutualistic endophyte Serendipita indica, we determined root celllayer responses reflecting the fundamentally different colonization strategies of the microbes. Mining the data-sets, we identified a Verticillium-specific suppression of endodermal gene expression related to Casparian strip formation and suberization. These findings highlight a novel function of the endodermis as a barrier restricting fungal propagation. Consequently, specific virulence factors can be proposed enabling the fungus to weaken the endodermal barrier and to perform its vascular life-style. Moreover, we compared localized gene expression related to the biosynthesis of antimicrobial compounds, particularly found upon pathogen infection. Whereas expression of ethylene biosynthesis is induced and essential for defence towards the pathogens, no changes in ethylene related gene expression was observed upon infestation with the mutualist. These examples highlight the power of this resource in generating testable hypotheses to gain insights into root-microbe-interactions and to develop novel strategies in crop improvement.

Publications

  • (2017). The Arabidopsis bZIP11 transcription factor links low-energy signalling to auxin-mediated control of primary root growth. PLoS Genet. 13: e1006607
    Weiste, C., Pedrotti, L., Selvanayagam, J., Muralidhara, P., Fröschel, C., Novák, O., Ljung, K., Hanson, J., and Dröge-Laser, W.
    (See online at https://doi.org/10.1371/journal.pgen.1006607)
  • (2019) A Gain-of-Function Screen reveals redundant ERF Transcription Factors providing Opportunities for Resistance Breeding towards the vascular fungal Pathogen Verticillium longisporum. Mol. Plant Microbe Inter. 32: 1095- 1109
    Fröschel, C., Iven, T., Walper, E., Bachmann, V., Weiste, C., Dröge-Laser, W.
    (See online at https://doi.org/10.1094/MPMI-02-19-0055-R)
  • (2020) In-depth evaluation of root infection systems with the vascular fungus Verticillium longisporum as soil-borne model pathogen. BioaRchive
    Fröschel, C.
    (See online at https://doi.org/10.1101/2020.12.28.424556)
  • (2021) Plant roots employ cell-layer specific programs to respond to pathogenic and beneficial microbes. Cell Host Microbe
    Fröschel, C., Komorek, J., Attard, A., Marsell, A, Lopez-Arboleda, W.A., Le Berre, J., Wolf, E., Geldner, N., Waller, F., Korte, A., Dröge-Laser, W.
    (See online at https://doi.org/10.1016/j.chom.2020.11.014)
 
 

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