Formin-mediated bridging of cell wall, plasma membrane, and cytoskeleton in symbiotic infections of Medicago truncatula

Liang, Peida; Schmitz, Clara; Lace, Beatrice; Ditengou, Franck Anicet; Su, Chao; Schulze, Eija; Knerr, Julian; Grosse, Robert; Keller, Jean; Libourel, Cyril; Delaux, Pierre-Marc; Ott, Thomas

doi:10.1016/j.cub.2021.04.002

Cited by 25 publications

(24 citation statements)

References 52 publications

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“…4K). Furthermore, expression of the symbiotic and actin-associated formin protein SYFO1 14 resulted in a tip-localized signal at these protrusions (Fig. 5B-B’’) further implying that growth of these membrane tubes is, most likely, driven by actin prolongation.…”

Section: Resultsmentioning

confidence: 96%

Remorin proteins serves as membrane topology scaffolds in plants

Rodriguez‐Franco

Lace

et al. 2022

Preprint

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Organization of membrane topologies in plants has so far been mainly attributed to the cell wall and the cytoskeleton. Taking rhizobial infections of legume root cells, where plasma membranes undergo dynamic and large-scale topology changes, as an initial model, we challenged this paradigm and tested whether additional scaffolds such as plant-specific remorins that accumulate on highly curved and often wall-less plasma membrane domains, control local membrane dynamics. Indeed, loss-of-function mutants of the remorin protein SYMREM1 failed to develop stabilized membrane tubes as found in colonized cells in wild-type plants, but released empty membrane spheres instead. Expression of this and other remorins in wall-less protoplasts allowed engineering different membrane topologies ranging from membrane blebs to long membrane tubes. Reciprocally, mechanically induced membrane indentations were equally stabilized by SYMREM1. This function is likely supported by remorin oligomerization into antiparallel dimers and the formation of higher order membrane scaffolding structures. Taken together we describe an evolutionary confined mechanism that allows the stabilization of large-scale membrane conformations and curvatures in plants.

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Section: Resultsmentioning

confidence: 96%

Remorin proteins serves as membrane topology scaffolds in plants

Rodriguez‐Franco

Lace

et al. 2022

Preprint

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“…In Arabidopsis, the vegetative formin AtFH1 is immobilized in the plasma membrane by the interaction of its ECD EXT-like motifs and the cell wall ( Martinière et al , 2011 ). Similarly, it was reported that the interaction between the ECD of SYMBIOTIC FORMIN 1 (SYFO1) and the cell wall is necessary to induce root hair curling during nodule development in Medicago truncatula ( Liang et al , 2021 ). Both reports highlight the importance and versatility of the ECD in formin cell wall anchoring; however, further studies are necessary to elucidate the nature of this interaction.…”

Section: Introductionmentioning

confidence: 95%

O-glycosylation of the extracellular domain of pollen class I formins modulates their plasma membrane mobility

Lara-Mondragón

Dorchak

MacAlister

2022

Journal of Experimental Botany

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In plant cells, linkage between the cytoskeleton, plasma membrane and cell wall is crucial to maintain cell shape. In highly polarized pollen tubes, this coordination is especially important to allow rapid tip-growth and successful fertilization. Class I formins contain cytoplasmic actin-nucleating formin homology domains as well as a Pro-rich extracellular domain (ECD) and are candidate coordination factors. Here, we investigated the functional significance of the extracellular domain of two pollen-expressed class I formins: AtFH3, which does not have a polar localization and AtFH5, which is limited to the growing tip region. We show that the ECD of both is necessary for their function and identify distinct O-glycans attached to these sequences, AtFH5 being Hyp-arabinosylated and AtFH3 carrying arabinogalactan chains. Loss of Hyp-arabinosylation altered the plasma membrane localization of AtFH5 and disrupted actin cytoskeleton organization. Moreover, we show that O-glycans differentially affect lateral mobility in the plasma membrane. Together, our results support a model of protein sub-functionalization where AtFH5 and AtFH3, restricted to specific plasma membrane domains by their ECDs and the glycans attached to them, organize distinct subarrays of actin during pollen tube elongation.

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“…An understanding of the molecular cell biology that drives nitrogen-fixing relationships therefore has potentially transformative value for agriculture and global food security. The discovery reported by Liang et al 2 is a significant step in decoding this process. This study shows that the SYFO1 subclass of formin proteins (which is specific to legumes) has the capacity to drive early morphological changes in the roots of the legume Medicago truncatula to accommodate a species of nitrogen-fixing rhizobia bacteria, but only under the strict condition that the appropriate microbial signal has been perceived 2 .…”

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confidence: 99%

“…New work from Liang et al 2 , published in this issue of Current Biology, reveals how the crosskingdom signalling effects changes in the growth of plant cells to support this relationship between plants and bacteria. Legumes represent a fraction of the calories we consume from domesticated plant species, and staple crops such as cereals require expensive and environmentally damaging additional nitrogen in the form of fertilisers.…”

mentioning

confidence: 99%

“…SYFO1 formins appear to be part of a specialised toolkit that has evolved in legumes to accommodate nitrogen-fixing bacteria within plant tissues 1,3 . However, this new information from Liang et al 2 comes relatively soon after two earlier publications in Current Biology that also linked host formin function to other plant-microbe interactions. Sun et al 4 showed that the profilin PRF3 from the plant Arabidopsis thaliana plays an important role in the Arabidopsis immune response triggered by the bacterial peptide flg22 (a short fragment of flagellin that is commonly used by plant pathologists to elicit basal immune responses).…”

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