Stabilization of membrane topologies by proteinaceous remorin scaffolds

Su, Chao; Rodriguez‐Franco, Marta; Lace, Beatrice; Nebel, Nils; Hernández‐Reyes, Casandra; Liang, Peida; Schulze, Eija; Mymrikov, Evgeny V.; Gross, Nikolas; Knerr, Julian; Wang, Hong; Siukstaite, Lina; Keller, Jean; Libourel, Cyril; Fischer, Alexandra; Gabor, Katharina; Mark, Eric; Popp, Claudia; Hunte, Carola; Weber, Wilfried; Wendler, Petra; Stanislas, Thomas; Delaux, Pierre-Marc; Einsle, Oliver; Grosse, Robert; Römer, Winfried; Ott, Thomas

doi:10.1038/s41467-023-35976-5

Cited by 19 publications

(13 citation statements)

References 98 publications

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“…The cell wall modifying enzyme NPL, which is essential for IT initiation and elongation in both L. japonicus and M. truncatula ( Xie et al, 2012 ; Liu et al, 2019a ) is secreted to the IT apoplast and accumulates particularly at IT tip regions in M. truncatula ( Liu et al, 2019a ; Su et al, 2023a ), strongly suggesting that its tip-targeted secretion is required for IT polar extension. To evaluate the role of RPG in NPL targeting, we compared the localization pattern of this enzyme in WT and rpg-1 infected root hairs.…”

Section: Resultsmentioning

confidence: 99%

“…IT maintenance and progression require a highly coordinated interplay between the migrating nucleus, a cytosolic column ahead of the IT, actin, and dense microtubule arrays ( Fournier et al, 2015 ; Perrine-Walker et al, 2014 ; Qiu et al, 2015 ; Timmers et al, 1999 ; Yokota et al, 2009 ). IT propagation in underlying cortical tissues is supported by local cell wall modifications ( Su et al, 2023a ) and repolarization of these cells, forming pre-infection thread (PIT) structures ( van Brussel et al, 1992 ). This ensures guidance of the symbionts towards the newly divided cortical cells constituting the core of the nodule primordium.…”

Section: Introductionmentioning

confidence: 99%

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RPG acts as a central determinant for infectosome formation and cellular polarization during intracellular rhizobial infections

Lace

Perez

et al. 2023

eLife

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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 tip-growth. 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 cytoskeleton-mediated connectivity between the IT tip and the nucleus and affects 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.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

RPG acts as a central determinant for infectosome formation and cellular polarization during intracellular rhizobial infections

Lace

Perez

et al. 2023

eLife

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“…REM proteins display a wide range of physiological functions and are proposed to function as scaffold proteins 43,44,55 . Group 1 REMs have been shown to be involved in viral immunity, playing apparent contradictory roles depending on the virus genera 8,44,56 .…”

Section: Discussionmentioning

confidence: 99%

Interdependence of plasma membrane nanoscale dynamics of a kinase and its cognate substrate underliesArabidopsisresponse to viral infection

Jolivet,

Deroubaix,

Boudsocq

et al. 2023

Preprint

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Plant viruses represent a risk to agricultural production and as only few treatments exist, it is urgent to identify resistance mechanisms and factors. In plant immunity, plasma membrane (PM)-localized proteins are playing an essential role in sensing the extracellular threat presented by bacteria, fungi or herbivores. Viruses being intracellular pathogens, the role of the plant PM in detection and resistance against viruses is often overlooked. We investigated the role of the partially PM-bound Calcium-dependent protein kinase 3 (CPK3) in viral infection and we discovered that it displayed a specific ability to hamper viral propagation over CPK isoforms that are involved in immune response to extracellular pathogens. More and more evidence support that the lateral organization of PM proteins and lipids underlies signal transduction in plants. We showed here that CPK3 diffusion in the PM is reduced upon activation as well as upon viral infection and that such immobilization depended on its substrate, Remorin (REM1.2), a scaffold protein. Furthermore, we discovered that the viral infection induced a CPK3-dependent increase of REM1.2 PM diffusion. Such interdependence was also observable regarding viral propagation. This study unveils a complex relationship between a kinase and its substrate that contrasts with the commonly described co-stabilisation upon activation while it proposes a PM-based mechanism involved in decreased sensitivity to viral infection in plants.

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“…Further, actin disruption has been recently proposed as an immune response leading to callose deposition (Leontovyčová et al, 2020) and both AtADF4 and REMORINs are required for callose deposition in response to bacterial elicitors (Li et al, 2012;Ma et al, 2022). Since StREM1.3 regulates callose deposition at PD (Perraki et al, 2018) and that StADF2 limits PVX in a REMORIN-dependent manner (Figure 4C Arabidopsis REM1.2 promotes type-I Formin ND organization to foster actin nucleation in response to bacterial flagellin (Ma et al, 2022) while SYMREM1-induced membrane topology modifications during symbiosis depends on the actin cytoskeleton (Su et al, 2023). Our observations further reinforce the tight functional interplay between REMORINs and the actin cytoskeleton.…”

Section: Discussionmentioning

confidence: 99%

“…Recently, evidences indicate that REMORINs and the actin cytoskeleton are working hand in hand during plant-microbe interactions. Arabidopsis REM1.2 promotes type-I Formin ND organization to foster actin nucleation in response to bacterial flagellin (Ma et al, 2022) while SYMREM1-induced membrane topology modifications during symbiosis depends on the actin cytoskeleton (Su et al, 2023). Our observations further reinforce the tight functional interplay between REMORINs and the actin cytoskeleton.…”

Section: Discussionmentioning

confidence: 99%

The actin depolymerizing factor StADF2 alters StREM1.3 plasma membrane nanodomains to inhibit thePotato Virus X

Jolivet¹,

Gouguet²,

Legrand³

et al. 2023

Preprint

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The dynamic regulation of the plasma membrane (PM) organization at the nanoscale emerged as a key element shaping the outcome of host-microbe interactions. Protein organization into nanodomains (ND) is often assumed to be linked to the activation of cellular processes. In contrast, we have previously shown that the phosphorylation of the Solanum tuberosum REM1.3 (StREM1.3) N-terminal domain disperses its native ND organization and promotes its inhibitory effect on Potato Virus X (PVX) cell-to-cell movement. Here, we show that the phosphorylation of StREM1.3 modify the chemical environment of numerous residues in its intrinsically-disordered N-terminal domain. We leveraged exploratory screens to identify potential phosphorylation-dependent interactors of StREM1.3. Herewith, we uncovered uncharacterized regulators of PVX cell-to-cell movement, linking StREM1.3 to autophagy, water channels and the actin cytoskeleton. We show that the Solanum tuberosum actin depolymerizing factors 2 (StADF2) alters StREM1.3 NDs and limits PVX cell-to-cell movement in a REMORIN-dependent manner. Mutating a conserved single residue reported to affect ADFs affinity to actin inhibits StADF2 effect on StREM1.3 ND organization and PVX cell-to-cell movement. These observations provide functional links between the organization of plant PM and the actin cytoskeleton and suggests that the alteration of StREM1.3 ND organization promotes plant anti-viral responses. We envision that analogous PM re-organization applies for additional signaling pathways in plants and in other organisms.

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Stabilization of membrane topologies by proteinaceous remorin scaffolds

Cited by 19 publications

References 98 publications

RPG acts as a central determinant for infectosome formation and cellular polarization during intracellular rhizobial infections

RPG acts as a central determinant for infectosome formation and cellular polarization during intracellular rhizobial infections

Interdependence of plasma membrane nanoscale dynamics of a kinase and its cognate substrate underliesArabidopsisresponse to viral infection

The actin depolymerizing factor StADF2 alters StREM1.3 plasma membrane nanodomains to inhibit thePotato Virus X

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