Abstract

Upon immune activation, chloroplasts switch off photosynthesis, produce antimicrobial 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 chloroplast movement in response to pathogen attack. Here, we report that during infection with the Irish potato famine pathogen Phytophthora infestans, chloroplasts accumulate at the pathogen interface, associating with the specialized membrane that engulfs the pathogen haustorium. The chemical inhibition of actin polymerization reduces the accumulation of chloroplasts at pathogen haustoria, suggesting that 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 INSENSITIVE1-ASSOCIATED KINASE1 (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.

Highlights

  • Phytophthora infestans is an oomycete pathogen that causes potato late blight, one of the most historically important and economically devastating crop diseases

  • Haustoria are surrounded by the plantderived extrahaustorial membrane (EHM), across which effectors secreted by the pathogen translocate inside the host cell (Wang et al, 2017; Whisson et al, 2007, 2016)

  • Whereas the immune-related roles of chloroplasts in producing antimicrobial compounds and defense signaling molecules are well established, little is known on the subcellular dynamics of chloroplast movement and stromule induction during infection

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Summary

Introduction

Phytophthora infestans is an oomycete pathogen that causes potato late blight, one of the most historically important and economically devastating crop diseases. Haustoria are surrounded by the plantderived extrahaustorial membrane (EHM), across which effectors secreted by the pathogen translocate inside the host cell (Wang et al, 2017; Whisson et al, 2007, 2016). This interface is key to the success or failure of infection and is targeted by focal immune responses of the plant (Bozkurt et al, 2011; Dagdas et al, 2018; Kwon et al, 2008). Continuous with the plasma membrane, there is a stark difference between the biochemical composition of the EHM and that of the plasma membrane (Bozkurt et al, 2014, 2015)

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