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Original Research ARTICLE Provisionally accepted The full-text will be published soon. Notify me

Front. Plant Sci. | doi: 10.3389/fpls.2019.01138

Analysis of barley leaf epidermis and extrahaustorial proteomes during powdery mildew infection reveals that the PR5 thaumatin-like protein TLP5 is required for susceptibility towards Blumeria graminis f.sp. hordei.

Sebastien Lambertucci1,  Kate M. Orman1, 2, Shaoli DasGupta1, James P. Fisher1,  Snehi Gazal1,  Ryan J. Williamson3,  Rainer Cramer3 and  Laurence V. Bindschedler4*
  • 1School of Biological Sciences, Royal Holloway, University of London, United Kingdom
  • 2School of Chemistry, Faculty of Science, University of East Anglia, United Kingdom
  • 3School of Chemistry, Food & Pharmacy, University of Reading, United Kingdom
  • 4School of Biological Sciences, Royal Holloway, University of London, United Kingdom

Powdery mildews are biotrophic pathogens causing fungal diseases in many economically important crops, including cereals, which are affected by Blumeria graminis. Powdery mildews only invade the epidermal cell layer of leaf tissues, in which they form haustorial structures. Haustoria are at the centre of the biotrophic interaction by taking up nutrients from the host and by delivering effectors in the invaded cells to jeopardise plant immunity. Haustoria are composed of a fungal core delimited by a haustorial plasma membrane and cell wall. Surrounding these, is the extrahaustorial complex, of which the extrahaustorial membrane is of plant origin. Although haustoria transcriptomes and proteomes have been investigated for Blumeria, the proteomes of barley epidermis upon infection and the barley components of the extrahaustorial complex remains unexplored.
When comparing proteomes of infected and non-infected epidermis, several classical pathogenesis-related (PR) proteins were relatively more abundant in infected epidermis. These included peroxidases, chitinases, cysteine-rich venom secreted proteins/ PR1 and two thaumatin-like PR5 protein isoforms, of which, TLP5 was previously shown to interact with the Blumeria effector BEC1054 (CSEP0064). Against expectations, transient TLP5 gene silencing suggested that TLP5 does not contribute to resistance but modulates susceptibility towards B. graminis. In a second proteomics comparison, haustorial structures were enriched from infected epidermal strips to identify plant proteins closely associated with the extrahaustorial complex. In these haustoria enriched samples, relative abundances were higher for several V-type ATP synthase/ ATPase subunits suggesting the generation of proton gradients in the extrahaustorial space. Other haustoria associated proteins included secreted or membrane proteins such as a PIP2 aguaporin, an early nodulin-like protein 9, an aspartate protease and other proteases, a lipase, a lipid transfer protein, all of which are potential modulators of immunity, or the targets of pathogen effectors. Moreover, the ER HSP40/ DNAJ homologue and a BIP-like HSP70, may link ER stress response, and the idea of ER-like properties previously attributed to the extrahaustorial membrane.
This initial investigation exploring the barley proteomes of Blumeria infected tissues and haustoria, associated with a transient gene silencing approach is invaluable to gain first insight of key players of resistance and susceptibility.

Keywords: plant proteomics, biotic stress, Biotrophic plan pathogen, powdery mildew, haustoria, Blumeria graminis (syn. Erysiphe graminis) f. sp. hordei, susceptibility factors, Barley ( Hordeum vulgare L.), Plant Epidermis, plant disease

Received: 27 Feb 2019; Accepted: 20 Aug 2019.

Copyright: © 2019 Lambertucci, Orman, DasGupta, Fisher, Gazal, Williamson, Cramer and Bindschedler. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Laurence V. Bindschedler, Royal Holloway, University of London, School of Biological Sciences, Egham, TW20 0EX, Surrey, United Kingdom, Laurence.Bindschedler@rhul.ac.uk