A Defense Pathway Linking Plasma Membrane and Chloroplasts and Co-opted by Pathogens

Abstract

Chloroplasts are crucial players in the activation of defensive hormonal responses during plant-pathogen interactions. Here, we show that a plant virus-encoded protein re-localizes from the plasma membrane to chloroplasts upon activation of plant defense, interfering with the chloroplast-dependent anti-viral salicylic acid (SA) biosynthesis. Strikingly, we have found that plant pathogens from different kingdoms seem to have convergently evolved to target chloroplasts and impair SA-dependent defenses following an association with membranes, which relies on the co-existence of two subcellular targeting signals, an N-myristoylation site and a chloroplast transit peptide. This pattern is also present in plant proteins, at least one of which conversely activates SA defenses from the chloroplast. Taken together, our results suggest that a pathway linking plasma membrane to chloroplasts and activating defense exists in plants and that such pathway has been co-opted by plant pathogens during host-pathogen co-evolution to promote virulence through suppression of SA responses.

Kinases and protein motifs required for AZI1 plastid localization and trafficking during plant defense induction

“…This targeting and/or stability in the plastid pool of AZI1 is impacted by two key defense associated kinases, MPK3 and MPK6, probably for a tight modulation during defense induction against pathogens and possible other stresses. This could be especially important considering how fundamental plastids are for many types of defense responses (Caplan et al ., 2008; Grant and Jones, 2009; Nomura et al ., 2012; Zeier, 2013; de Torres Zabala et al ., 2015; Cecchini et al ., 2015a; Medina‐Puche et al ., 2020). In particular, a timely regulation of the AZI1 pool in plastids could grant an efficient movement of AZA for the establishment of systemic defenses.…”

Chloroplast: The Emerging Battlefield in Plant–Microbe Interactions

“…Once PTI or ETI signal is relayed to the chloroplast, Ca 2+ from the thylakoid lumen, which contains a high concentration of Ca 2+ , are transported to the stroma by CAS, resulting in a continuous high concentration of Ca 2+ in the stroma, and the signal is then transduced from the chloroplast to the nucleus through the 1 O 2 -mediated retrograde signaling pathway (Kim and Apel, 2013), which regulates the defense responses through transcriptional reprogramming of defenserelated genes (Nomura et al, 2012). Another outstanding example is that the calcium protein kinase 16 (CPK16), localized on the PM, undergoes N-myristoylation in normal condition and relocalizes from the PM to chloroplasts upon flg22 or immune elicitors treatment to promote chloroplast-dependent defenses (Medina-Puche et al, 2020).…”

“…This pattern is observed in plant and several plant pathogens from different kingdoms. In plants, there may be a pathway that connects the PM to the chloroplast to activate the defense that is utilized by different pathogens to promote their infection by inhibiting the biosynthesis of SA and possible retrograde signaling (Medina-Puche et al, 2020).…”

Keeping in Touch with Type-III Secretion System Effectors: Mass Spectrometry-Based Proteomics to Study Effector–Host Protein–Protein Interactions

“…Further research proved that IncE binding to sorting nexins (SNXs) 5/6 relocated them to the inclusion membrane. This observation was followed up by comparing the AP-MS interaction profiles of wild-type versus SNX5 mutated at the IncE binding surface, overall leading to the discovery that IncE disrupts a native interaction between cation-independent mannose-6-phosphate receptor (CI-MPR) and SNX5 and thus most likely represents an example of host mimicry [50]. Sontag et al made use of AP-MS and came up with a collection of high-confident EH-PPIs of eight Salmonella and four Citrobacter effectors [51].…”