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RPG acts as a central determinant for infectosome formation and cellular polarization during intracellular rhizobial infections
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Edité par CCSD ; eLife Sciences Publication -
International audience. Host-controlled intracellular accommodation of nitrogen-fixing bacteria is essential for the establishment of a functional Root Nodule Symbiosis (RNS). In many host plants, this occurs via transcellular tubular structures (infection threads -ITs) that extend across cell layers via polar tipgrowth. Comparative phylogenomic studies have identified RPG (RHIZOBIUM-DIRECTED POLAR GROWTH) among the critical genetic determinants for bacterial infection. In Medicago truncatula, RPG is required for effective IT progression within root hairs but the cellular and molecular function of the encoded protein remains elusive. Here, we show that RPG resides in the protein complex formed by the core endosymbiotic components VAPYRIN (VPY) and LUMPY INFECTION (LIN) required for IT polar growth, co-localizes with both VPY and LIN in IT tip-and perinuclear-associated puncta of M. truncatula root hairs undergoing infection and is necessary for VPY recruitment into these structures. Fluorescence Lifetime Imaging Microscopy (FLIM) of phosphoinositide species during bacterial infection revealed that functional RPG is required to sustain strong membrane polarization at the advancing tip of the IT. In addition, loss of RPG functionality alters the cytoskeletonmediated connectivity between the IT tip and the nucleus and affects the polar secretion of the cell wall modifying enzyme NODULE PECTATE LYASE (NPL). Our results integrate RPG into a core host machinery required to support symbiont accommodation, suggesting that its occurrence in plant host genomes is essential to co-opt a multimeric protein module committed to endosymbiosis to sustain IT-mediated bacterial infection.
This work addresses a fundamental question in symbiosis, placing a classic nodulation defective mutant (rpg) into a plausible protein complex and establishing a hierarchy of "infectosome" assembly. It will be of particular interest to cell biologists and those studying host-microbe interactions. The study includes compelling microscopy data for subcellular localization of components during the establishment and maintenance of infection and includes new FLIM-based imaging techniques to distinguish signals from closely associated domains in plant cells.
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