The Plant Membrane-Associated REMORIN1.3 Accumulates in Discrete Perihaustorial Domains and Enhances Susceptibility to Phytophthora infestans    

Abstract

Filamentous pathogens such as the oomycete Phytophthora infestans infect plants by developing specialized structures termed haustoria inside the host cells. Haustoria are thought to enable the secretion of effector proteins into the plant cells. Haustorium biogenesis, therefore, is critical for pathogen accommodation in the host tissue. Haustoria are enveloped by a specialized hostderived membrane, the extrahaustorial membrane (EHM), which is distinct from the plant plasma membrane. The mechanisms underlying the biogenesis of the EHM are unknown. Remarkably, several plasma membrane-localized proteins are excluded from the EHM, but the remorin REM1.3 accumulates around P. infestans haustoria. Here, we used overexpression, colocalization with reporter proteins, and superresolution microscopy in cells infected by P. infestans to reveal discrete EHM domains labeled by REM1.3 and the P. infestans effector AVRblb2. Moreover, SYNAPTOTAGMIN1, another previously identified perihaustorial protein, localized to subdomains that are mainly not labeled by REM1.3 and AVRblb2. Functional characterization of REM1.3 revealed that it is a susceptibility factor that promotes infection by P. infestans. This activity, and REM1.3 recruitment to the EHM, require the REM1.3 membrane-binding domain. Our results implicate REM1.3 membrane microdomains in plant susceptibility to an oomycete pathogen.

Homologues of the RPW8 Resistance Protein Are Localized to the Extrahaustorial Membrane that Is Likely Synthesized De Novo

“…In this regard, it is worth noting that several PM-proteins (PEN1, FLS2, and REM1.3, PDLP1, etc. ), Golgi marker proteins (SYP32 and Got1p) and endosomal markers (RabC1 and Ara7) were found in the perihaustorial membrane encasing oomycete haustoria in tobacco or Arabidopsis cells (Lu et al, 2012;Bozkurt et al, 2014;Caillaud et al, 2014). However, based on our observations, PM-localized proteins such as GFP-PEN1 ) and YFP-SYP131 (Fig.…”

Plant immune and growth receptors share common signalling components but localise to distinct plasma membrane nanodomains

“…REMs form a large plant-specific protein family with characteristic PM nanodomain localisation patterns (Jarsch et al, 2014). Moreover, different members of this family have previously been associated with plant-microbe interactions (Raffaele et al, 2009; Lefebvre et al, 2010; Tóth et al, 2012; Perraki et al, 2012, 2014; Bozkurt et al, 2014) and with SERK-dependent processes (Gui et al, 2016). …”

Across the great divide: the plant cell surface continuum

“…During Blumeria graminis infection, Mildew resistance locus O (MLO) gene has been shown using live cell imaging to form a microdomain in the PM beneath the appresoria during entry into the host [17]. Furthermore, REM1.3 has been shown to localize to the peri-haustorial matrix during oomycyte interactions [18 ]. Interestingly, a number of general PM-localized proteins are excluded from the peri-haustorial membrane.…”

“…REM1.3 was shown to be important for pathogenicity upon Phytophera infestans infection. The precise role of REM1.3 at the peri-haustorial matrix is yet to be identified [18 ]. The legume-specific SYMREM1 has been shown to localize to infection threads during microbial symbiosis and root nodule formation [19].…”