RISAP Is a TGN-Associated RAC5 Effector Regulating Membrane Traffic during Polar Cell Growth in Tobacco

Stephan, Octavian O H; Cottier, Stéphanie; Fahlén, Sara; Montes-Rodriguez, Adriana; Sun, Jun; Eklund, D. Magnus; Klahre, Ulrich; Kost, Benedikt

doi:10.1105/tpc.114.131078

Cited by 52 publications

(76 citation statements)

References 85 publications

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“…In addition to their general roles in intracellular motility and cell growth, certain MyoBs are involved in more specialized processes. Thus, a pollen-specific MyoB has been implicated in pollen tube growth in tobacco (36), whereas maize MyoBs have been found in association with protein bodies specific to maize endosperm (37,38).…”

Section: Discussionmentioning

confidence: 99%

Myosin-driven transport network in plants

Kurth

Peremyslov

Turner

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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We investigate the myosin XI-driven transport network in Arabidopsis using protein-protein interaction, subcellular localization, gene knockout, and bioinformatics analyses. The two major groups of nodes in this network are myosins XI and their membrane-anchored receptors (MyoB) that, together, drive endomembrane trafficking and cytoplasmic streaming in the plant cells. The network shows high node connectivity and is dominated by generalists, with a smaller fraction of more specialized myosins and receptors. We show that interaction with myosins and association with motile vesicles are common properties of the MyoB family receptors. We identify previously uncharacterized myosin-binding proteins, putative myosin adaptors that belong to two unrelated families, with four members each (MadA and MadB). Surprisingly, MadA1 localizes to the nucleus and is rapidly transported to the cytoplasm, suggesting the existence of myosin XI-driven nucleocytoplasmic trafficking. In contrast, MadA2 and MadA3, as well as MadB1, partition between the cytosolic pools of motile endomembrane vesicles that colocalize with myosin XI-K and diffuse material that does not. Gene knockout analysis shows that MadB1-4 contribute to polarized root hair growth, phenocopying myosins, whereas MadA1-4 are redundant for this process. Phylogenetic analysis reveals congruent evolutionary histories of the myosin XI, MyoB, MadA, and MadB families. All these gene families emerged in green algae and show concurrent expansions via serial duplication in flowering plants. Thus, the myosin XI transport network increased in complexity and robustness concomitantly with the land colonization by flowering plants and, by inference, could have been a major contributor to this process.myosins | receptors | adaptors | cytoplasmic streaming | nuclear transport F or half of a century, it had been assumed that rapid organelle trafficking and cytoplasmic streaming in plant cells rely on myosin motors (1) and, in particular, class XI myosins that are homologous to fungal and animal class V myosins (2). Over the past decade, a massive amount of information on specific functions of myosins and mechanisms of myosin XI-dependent processes in plants has been obtained (3-5). The first genetic evidence of myosin function in cell expansion involved the demonstration of a dramatic reduction of the polarized root hair growth upon inactivation of the myosin XI-K and XI-2 genes (6, 7). Subsequently, it has been shown that myosindependent trafficking is required for the growth of multiple cell types, as well as normal plant growth and development (4,(8)(9)(10). Among the 13 paralogous myosins XI encoded in the Arabidopsis thaliana genome, the highly expressed myosins XI-K, XI-1, and XI-2 have been shown to provide the most pronounced, functionally redundant contributions to each of these processes. In contrast, another highly expressed paralog, myosin XI-I, plays only limited roles in cell and plant growth but has a specialized function in nuclear repositioning through binding nuclear e...

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Section: Discussionmentioning

confidence: 99%

Myosin-driven transport network in plants

Kurth

Peremyslov

Turner

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…RISAP is ;33% identical to the Arabidopsis family of myosin binding proteins at the amino acid level (Peremyslov et al, 2013). It was proposed that the RISAP-mediated interaction between the actin cytoskeleton and endomembrane system is an essential component of the tip growth machinery in pollen tubes (Stephan et al, 2014). Another family of plant-specific proteins that mediate actin-endomembrane crosstalk is the 13-member Networked (NET) proteins.…”

Section: Introductionmentioning

confidence: 99%

HLB1 Is a Tetratricopeptide Repeat Domain-Containing Protein That Operates at the Intersection of the Exocytic and Endocytic Pathways at the TGN/EE in Arabidopsis

et al. 2016

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The endomembrane system plays essential roles in plant development, but the proteome responsible for its function and organization remains largely uncharacterized in plants. Here, we identified and characterized the HYPERSENSITIVE TO LATRUNCULIN B1 (HLB1) protein isolated through a forward-genetic screen in Arabidopsis thaliana for mutants with heightened sensitivity to actin-disrupting drugs. HLB1 is a plant-specific tetratricopeptide repeat domain-containing protein of unknown function encoded by a single Arabidopsis gene. HLB1 associated with the trans-Golgi network (TGN)/early endosome (EE) and tracked along filamentous actin, indicating that it could link post-Golgi traffic with the actin cytoskeleton in plants. HLB1 was found to interact with the ADP-ribosylation-factor guanine nucleotide exchange factor, MIN7/BEN1 (HOPM INTERACTOR7/BREFELDIN A-VISUALIZED ENDOCYTIC TRAFFICKING DEFECTIVE1) by coimmunoprecipitation. The min7/ben1 mutant phenocopied the mild root developmental defects and latrunculin B hypersensitivity of hlb1, and analyses of a hlb1/ min7/ben1 double mutant showed that hlb1 and min7/ben1 operate in common genetic pathways. Based on these data, we propose that HLB1 together with MIN7/BEN1 form a complex with actin to modulate the function of the TGN/EE at the intersection of the exocytic and endocytic pathways in plants.

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“…Until now, direct evidence for endomembrane-localized myosin XI cargoes was limited to Rab GTPases of the RabC and RabD clades (Hashimoto et al, 2008), and the enigmatic MyoB family (Peremyslov et al, 2013;Stephan et al, 2014). MyoB is a myosin XI effector that localizes to an unknown endomembrane compartment that polarizes to the tip of growing root hairs, as expected for a protein family associated with polarized transport (Peremyslov et al, 2013;Kurth et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

Myosin XI Interacting with a RabE GTPase Is Required for Polarized Growth

Orr

Furt

Warner

et al. 2019

Preprint

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The fundamental eukaryotic process of intracellular trafficking requires the interconnected activity of molecular motors trafficking vesicular cargo within a dynamic cytoskeletal network. However, in plants, few mechanistic details are known about how molecular motors associate with their secretory cargo to support the ubiquitous processes of polarized growth and cell division. A yeast two-hybrid screen of a Physcomitrella patens library identified a RabE GTPase as an interactor of myosin XI and subsequently demonstrated all five RabE members interact with myosin XI. Consistent with a role in polarized transport, we observed RabE at the growing cell apex and at the expanding cell plate during cell division. An in vivo cross-correlation analysis of fluorescently tagged RabE and myosin XI revealed that both species are spatiotemporally coupled, demonstrating their simultaneous involvement in polarized growth. To determine if myosin XI and RabE are directly coupled, we first computationally predicted myosin XI:RabE interface through a homology modeling-directed approach. We identified a structurally conserved residue on myosin XI, V1422, that when mutated abolished RabE binding in the yeast two-hybrid system and resulted in unpolarized plants instead of the characteristic network of filamentous cells when regenerated from single cells. Together, this work demonstrates the requirement of a direct myosin XI:RabE interaction for polarized growth in plants. Fendrych, M., Synek, L., Pečenková, T., Toupalová, H., Cole, R., Drdová, E., Nebesářová, J., Šedinová, M., Hála, M., and Fowler, J.E. (2010). The Arabidopsis exocyst complex is involved in cytokinesis and cell plate maturation. Plant Cell 22, 3053-3065. Furt, F., Lemoi, K., Tuzel, E., and Vidali, L. (2012). Quantitative analysis of organelle distribution and dynamics in Physcomitrella patens protonemal cells. . PHYML Online--a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res. 33, W557-559. Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W., and Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307-321. Hammer, J.A., and Sellers, J.R. (2012). Walking to work: roles for class V myosins as cargo transporters. Nat Rev Mol Cell Bio 13, 13-26. Hashimoto, K., Igarashi, H., Mano, S., Takenaka, C., Shiina, T., Yamaguchi, M., Demura, T., Nishimura, M., Shimmen, T., and Yokota, E. (2008). An isoform of Arabidopsis myosin XI interacts with small GTPases in its C-terminal tail region. J. Exp. Bot. 59, 3523-3531. Heider, M.R., and Munson, M. (2012). Exorcising the exocyst complex. Traffic 13, 898-907. Hepler, P.K., and Winship, L.J. (2015). The pollen tube clear zone: Clues to the mechanism of polarized growth. . (2018). The Physcomitrella patens chromosome-scale assembly reveals moss genome structure and evolution. Plant J 93, 515-533. Lepore, D., Spassibojko, O., Pinto, G., and Collins, R.N. (2016). Cell cycle-dependent phosphory...

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RISAP Is a TGN-Associated RAC5 Effector Regulating Membrane Traffic during Polar Cell Growth in Tobacco

Cited by 52 publications

References 85 publications

Myosin-driven transport network in plants

Myosin-driven transport network in plants

HLB1 Is a Tetratricopeptide Repeat Domain-Containing Protein That Operates at the Intersection of the Exocytic and Endocytic Pathways at the TGN/EE in Arabidopsis

Myosin XI Interacting with a RabE GTPase Is Required for Polarized Growth

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