Friend or Foe: Hybrid proline-rich proteins determine how plants interact with and respond to beneficial and pathogenic microbes

Plant plastids generate signals, including some derived from lipids, that need to be mobilized to effect signaling. We used informatics to discover potential plastid membrane proteins involved in microbial responses. Among these are proteins co-regulated with the systemic immunity component AZI1, a hybrid proline-rich protein (HyPRP) and HyPRP superfamily members. HyPRPs have a transmembrane domain, a proline-rich region (PRR) and a lipid transfer protein domain. The precise subcellular location(s) and function(s) is unknown for most HyPRP family members. As predicted by informatics, a subset of HyPRPs have a pool of protein that targets plastid outer envelope membranes (OEMs) via a mechanism that requires the PRR. Additionally, two HyPRPs may be associated with thylakoid membranes. Most of the plastid and non-plastid localized family members also have pools that localize to endoplasmic reticulum, plasma membrane or plasmodesmata. HyPRPs with plastid pools regulate, positively or negatively, systemic immunity against the pathogen Pseudomonas syringae. HyPRPs also regulate the interaction with the plant growth promoting rhizobacteria Pseudomonas simiae WCS417 in the roots to influence colonization, root system architecture and/or biomass. Thus, HyPRPs have broad and distinct roles in immune, development and growth responses to microbes and reside at sites that may facilitate signal molecule transport.