Chloroplasts alter their morphology and accumulate at the pathogen interface during infection by Phytophthora infestans

Zachary Savage, Cian Duggan, Alexia Toufexi, Pooja Pandey, Yuxi Liang, María Eugenia Segretin, Lok Him Yuen, David C A Gaboriau, Alexandre Y Leary, Yasin Tumtas, Virendrasinh Khandare, Andrew D Ward, Stanley W Botchway, Benji C Bateman, Indranil Pan, Martin Schattat, Imogen Sparkes, Tolga O Bozkurt*

*Corresponding author for this work

Research output: Contribution to journalArticle (Academic Journal)peer-review

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Abstract

Upon immune activation, chloroplasts switch off photosynthesis, produce anti-microbial compounds, and associate with the nucleus through tubular extensions called stromules. Although it is well-established that chloroplasts alter their position in response to light, little is known about the dynamics of chloroplasts movement in response to pathogen attack. Here, we report that chloroplasts accumulate at the pathogen interface during infection by the Irish potato famine pathogen Phytophthora infestans, associating with the specialized membrane that engulfs the pathogen haustorium. Chemical inhibition of actin polymerization reduces the accumulation of chloroplasts at the pathogen haustoria, suggesting this process is partially dependent on the actin cytoskeleton. However, chloroplast accumulation at haustoria does not necessarily rely on movement of the nucleus to this interface and is not affected by light conditions. Stromules are typically induced during infection, embracing haustoria and facilitating chloroplast interactions, to form dynamic organelle clusters. We found that infection-triggered stromule formation relies on BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED KINASE 1 (BAK1) mediated surface immune signaling, whereas chloroplast repositioning towards haustoria does not. Consistent with the defense-related induction of stromules, effector mediated suppression of BAK1 mediated immune signaling reduced stromule formation during infection. On the other hand, immune recognition of the same effector stimulated stromules, presumably via a different pathway. These findings implicate chloroplasts in a polarized response upon pathogen attack and point to more complex functions of these organelles in plant-pathogen interactions.

Original languageEnglish
Number of pages17
JournalPlant Journal
Volume(2021)
Early online date12 Jul 2021
DOIs
Publication statusE-pub ahead of print - 12 Jul 2021

Bibliographical note

Funding Information:
We thank Dr Alex Jones (Warwick) for initiating the collaboration with IS, Dr Sebastian Schornack (SLCU) for initiating collaboration with MS, Prof. Peter Nixon (Imperial) for providing CpGFP plant seeds and Prof. Savithramma Dinesh‐Kumar for providing us with the RecA‐cTP HyPer construct. TOB’s lab is funded by the Biotechnology and Biological Sciences Research Council (BBSRC; BB/M002462/1). The Facility for Imaging by Light Microscopy (FILM) at Imperial College London is part supported by funding from the Wellcome Trust (grant 104931/Z/14/Z) and BBSRC (grant BB/L015129/1).

Publisher Copyright:
© 2021 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.

Keywords

  • haustorium
  • stromule
  • Phytophthora infestans
  • chloroplast movement
  • laser capture
  • focalimmunity
  • effectors

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