SH3P2 (At4g34660), an Arabidopsis thaliana SH3 and Bin/amphiphysin/Rvs (BAR) domain-containing protein, was reported to have a specific role in cell plate assembly, unlike its paralogs SH3P1 (At1g31440) and SH3P3 (At4g18060). SH3P family members were also predicted to interact with formins-evolutionarily conserved actin nucleators that participate in microtubule organization and in membrane-cytoskeleton interactions. To trace the origin of functional specialization of plant SH3Ps, we performed phylogenetic analysis of SH3P sequences from selected plant lineages. SH3Ps are present in charophytes, liverworts, mosses, lycophytes, gymnosperms, and angiosperms, but not in volvocal algae, suggesting association of these proteins with phragmoplast-, but not phycoplast-based cell division. Separation of three SH3P clades, represented by SH3P1, SH3P2, and SH3P3 of A. thaliana, appears to be a seed plant synapomorphy. In the yeast two hybrid system, Arabidopsis SH3P3, but not SH3P2, binds the FH1 and FH2 domains of the formin FH5 (At5g54650), known to participate in cytokinesis, while an opposite binding specificity was found for the dynamin homolog DRP1A (At5g42080), confirming earlier findings. This suggests that the cytokinetic role of SH3P2 is not due to its interaction with FH5. Possible determinants of interaction specificity of SH3P2 and SH3P3 were identified bioinformatically.

Department of Experimental Plant Biology Faculty of Sciences Charles University Viničná 5 CZ 128 43 Prague Czech Republic

Zobrazit více v PubMed

Panteris E. Cortical actin filaments at the division site of mitotic plant cells: A reconsideration of the actin-depleted zone. New Phytol. 2008;179:334–341. doi: 10.1111/j.1469-8137.2008.02474.x. PubMed DOI

Rasmussen C.G., Wright A.J., Müller S. The role of the cytoskeleton and associated proteins in determination of the plant cell division plane. Plant J. 2013;75:258–269. doi: 10.1111/tpj.12177. PubMed DOI

Müller S. Plant cell division—Defining and finding the sweet spot for cell plate insertion. Curr. Opin. Cell Biol. 2019;60:9–18. doi: 10.1016/j.ceb.2019.03.006. PubMed DOI

Fujimoto M., Arimura S., Nakazono M., Tsutsumi N. Arabidopsis dynamin-related protein DRP2B is co-localized with DRP1A on the leading edge of the forming cell plate. Plant Cell Rep. 2008;27:1581–1586. doi: 10.1007/s00299-008-0583-0. PubMed DOI

Bednarek S.Y., Backues S.K. Plant dynamin-related protein families DRP1 and DRP2 in plant development. Biochem. Soc. Trans. 2010;38:797–806. doi: 10.1042/BST0380797. PubMed DOI PMC

Smertenko A. Phragmoplast expansion: The four-stroke engine that powers plant cytokinesis. Curr. Opin. Plant Biol. 2018;46:130–137. doi: 10.1016/j.pbi.2018.07.011. PubMed DOI

Buschmann H., Zachgo S. The evolution of cell division: From streptophyte algae to land plants. Trends Plant Sci. 2016;21:872–883. doi: 10.1016/j.tplants.2016.07.004. PubMed DOI

Cross F.R., Umen J.G. The Chlamydomonas cell cycle. Plant J. 2015;82:370–392. doi: 10.1111/tpj.12795. PubMed DOI PMC

Smertenko A., Assaad F., Baluška F., Bezanilla M., Buschmann H., Drakakaki G., Hauser M.T., Janson M., Mineyuki Y., Moore I., et al. Plant cytokinesis: Terminology for structures and processes. Trends Cell Biol. 2017;27:885–894. doi: 10.1016/j.tcb.2017.08.008. PubMed DOI

Ahn G., Kim H., Kim D.H., Hanh H., Yoon Y., Singaram I., Wijesinghe K.J., Johnson K.A., Zhuang X., Liang Z., et al. SH3 domain-containing protein 2 plays a crucial role at the step of membrane tubulation during cell plate formation. Plant Cell. 2017;29:1388–1405. doi: 10.1105/tpc.17.00108. PubMed DOI PMC

Peter B.J., Kent H.M., Mills I.G., Vallis Y., Butler P.J.G., Evans P.R., McMahon H.T. BAR domains as sensors of membrane curvature: The amphiphysin BAR structure. Science. 2004;303:495–499. doi: 10.1126/science.1092586. PubMed DOI

Dawson J.C., Legg J.A., Machesky L.M. Bar domain proteins: A role in tubulation, scission and actin assembly in clathrin-mediated endocytosis. Trends Cell Biol. 2006;16:493–498. doi: 10.1016/j.tcb.2006.08.004. PubMed DOI

Musacchio A., Noble M., Pauptit R., Wierenga R., Saraste M. Crystal structure of a Src-homology 3 (SH3) domain. Nature. 1992;359:851–855. doi: 10.1038/359851a0. PubMed DOI

Shah N.H., Amacher J.F., Nocka L.M., Kuriyan J. The Src module: An ancient scaffold in the evolution of cytoplasmic tyrosine kinases. Crit. Rev. Biochem. Mol. Biol. 2018;53:535–563. doi: 10.1080/10409238.2018.1495173. PubMed DOI PMC

Carman P.J., Dominguez R. BAR domain proteins-a linkage between cellular membranes, signaling pathways, and the actin cytoskeleton. Biophys. Rev. 2018;10:1587–1604. doi: 10.1007/s12551-018-0467-7. PubMed DOI PMC

Aspenström P., Richnau N., Johansson A.S. The diaphanous-related formin DAAM1 collaborates with the Rho GTPases RhoA and Cdc42, CIP4 and Src in regulating cell morphogenesis and actin dynamics. Exp. Cell Res. 2006;312:2180–2194. doi: 10.1016/j.yexcr.2006.03.013. PubMed DOI

Huett A., Ng A., Cao Z., Kuballa P., Komatsu M., Daly M.J., Podolsky D.K., Xavier R.J. A novel hybrid yeast-human network analysis reveals an essential role for FNBP1L in antibacterial autophagy. J. Immunol. 2009;182:4917–4930. doi: 10.4049/jimmunol.0803050. PubMed DOI PMC

Wakita Y., Kakimoto T., Katoh H., Negishi M. The F-BAR protein Rapostlin regulates dendritic spine formation in hippocampal neurons. J. Biol. Chem. 2011;286:32672–32683. doi: 10.1074/jbc.M111.236265. PubMed DOI PMC

Suetsugu S., Gautreau A. synergistic BAR-NPF interactions in actin-driven membrane remodeling. Trends Cell Biol. 2012;22:141–150. doi: 10.1016/j.tcb.2012.01.001. PubMed DOI

Cvrčková F. Formins and membranes: Anchoring cortical actin to the cell wall and beyond. Front. Plant Sci. 2013;4:436. doi: 10.3389/fpls.2013.00436. PubMed DOI PMC

Lam B.C., Sage T.L., Bianchi F., Blumwald E. Role of SH3 domain-containing proteins in clathrin-mediated vesicle trafficking in Arabidopsis. Plant Cell. 2001;13:2499–2512. doi: 10.1105/tpc.13.11.2499. PubMed DOI PMC

Kolb C., Nagel M.K., Kalinowska K., Hagmann J., Ichikawa M., Anzenberger F., Alkofer A., Sato M.H., Braun P., Isono E. FYVE1 is essential for vacuole biogenesis and intracellular trafficking in Arabidopsis. Plant Physiol. 2015;167:1361–1373. doi: 10.1104/pp.114.253377. PubMed DOI PMC

Lam B.C., Sage T.L., Bianchi F., Blumwald E. Regulation of ADL6 activity by its associated molecular network. Plant J. 2002;31:565–576. doi: 10.1046/j.1365-313X.2002.01377.x. PubMed DOI

Zhuang X., Wang H., Lam S.K., Gao C., Wang X., Cai Y., Jiang L. A BAR-domain protein, SH3P2, which binds to phosphatidylinositol 3-phosphate and ATG8, regulates autophagosome formation in Arabidopsis. Plant Cell. 2013;25:4596–4615. doi: 10.1105/tpc.113.118307. PubMed DOI PMC

Zhuang X., Jiang L. Autophagosome biogenesis in plants: Roles of SH3P2. Autophagy. 2014;10:704–705. doi: 10.4161/auto.28060. PubMed DOI PMC

Gao C., Zhuang X., Cui Y., Fu X., He Y., Zhao Q., Zeng Y., Shen J., Luo M., Jiang L. Dual roles of an Arabidopsis ESCRT component FREE1 in regulating vacuolar protein transport and autophagic degradation. Proc. Natl. Acad. Sci. USA. 2015;112:1886–1891. doi: 10.1073/pnas.1421271112. PubMed DOI PMC

Nagel M.K., Kalinowska K., Vogel K., Reynolds G.D., Wu Z., Anzenberger F., Ichikawa M., Tsutsumi C., Sato M.H., Kuster B., et al. Arabidopsis SH3P2 is an ubiquitin-binding protein that functions together with ESCRT-I and the deubiquitylating enzyme AMSH3. Proc. Natl. Acad. Sci. USA. 2017;114:7197–7204. doi: 10.1073/pnas.1710866114. PubMed DOI PMC

Johnson A., Vert G. Unraveling K63 polyubiquitination networks by sensor-based proteomics. Plant Physiol. 2016;171:1808–1820. doi: 10.1104/pp.16.00619. PubMed DOI PMC

Winter D., Vinegar B., Nahal H., Ammar R., Wilson G.V., Provart N.J. An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS ONE. 2007;2:e718. doi: 10.1371/journal.pone.0000718. PubMed DOI PMC

Cvrčková F., Novotný M., Pícková D., Žárský V. Formin homology 2 domains occur in multiple contexts in angiosperms. BMC Genom. 2004;5:44. doi: 10.1186/1471-2164-5-44. PubMed DOI PMC

Ingouff M., Fitz Gerald J.N., Guérin C., Robert H., Sørensen M.B., Van Damme D., Geelen D., Blanchoin L., Berger F. Plant formin AtFH5 is an evolutionarily conserved actin nucleator involved in cytokinesis. Nat. Cell Biol. 2005;7:374–380. doi: 10.1038/ncb1238. PubMed DOI

Hori K., Maruyama F., Fujisawa T., Togashi T., Yamamoto N., Seo M., Sato S., Yamada T., Mori H., Tajima N., et al. Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nat. Commun. 2014;5:3978. doi: 10.1038/ncomms4978. PubMed DOI PMC

Vitkup D., Sander C., Church G.M. The amino-acid mutational spectrum of human genetic disease. Genome Biol. 2003;4:R72. doi: 10.1186/gb-2003-4-11-r72. PubMed DOI PMC

Kelley L.A., Mezulis S., Yates C.M., Wass M.N., Sternberg M.J. The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc. 2015;10:845–858. doi: 10.1038/nprot.2015.053. PubMed DOI PMC

Waterhouse A., Bertoni M., Bienert S., Studer G., Tauriello G., Gumienny R., Heer F.T., de Beer T.A.P., Rempfer C., Bordoli L., et al. SWISS-MODEL: Homology modelling of protein structures and complexes. Nucleic Acids Res. 2018;46:296–303. doi: 10.1093/nar/gky427. PubMed DOI PMC

Zhu J., Wang S., Bu D., Xu J. Protein threading using residue co-variation and deep learning. Bioinformatics. 2018;34:263–273. doi: 10.1093/bioinformatics/bty278. PubMed DOI PMC

Adamowski M., Narasimhan M., Kania U., Glanc M., De Jaeger G., Friml J. A functional study of AUXILIN-LIKE1 and 2, two putative clathrin uncoating factors in Arabidopsis. Plant Cell. 2018;30:700–716. doi: 10.1105/tpc.17.00785. PubMed DOI PMC

Xin X., Gfeller D., Cheng J., Tonikian R., Sun L., Guo A., Lopez L., Pavlenco A., Akintobi A., Zhang Y., et al. SH3 interactome conserves general function over specific form. Mol. Syst. Biol. 2013;9:652. doi: 10.1038/msb.2013.9. PubMed DOI PMC

Yoon Y., Zhang X., Cho W. Phosphatidylinositol 4,5-bisphosphate (PtdIns (4,5) P2) specifically induces membrane penetration and deformation by Bin/Amphiphysin/Rvs (BAR) domains. J. Biol. Chem. 2012;287:34078–34090. doi: 10.1074/jbc.M112.372789. PubMed DOI PMC

Neumann S., Schmid S.L. Dual role of BAR domain-containing proteins in regulating vesicle release catalyzed by the GTPase, dynamin-2. J. Biol. Chem. 2013;288:25119–25128. doi: 10.1074/jbc.M113.490474. PubMed DOI PMC

Daumke O., Roux A., Haucke V. BAR domain scaffolds in dynamin-mediated membrane fission. Cell. 2014;156:882–892. doi: 10.1016/j.cell.2014.02.017. PubMed DOI

Pollard T.D. Nine unanswered questions about cytokinesis. J. Cell Biol. 2017;216:3007–3016. doi: 10.1083/jcb.201612068. PubMed DOI PMC

Roberts-Galbraith R.H., Chen J.S., Wang J., Gould K.L. The SH3 domains of two PCH family members cooperate in assembly of the Schizosaccharomyces pombe contractile ring. J. Cell Biol. 2009;184:113–127. doi: 10.1083/jcb.200806044. PubMed DOI PMC

Ren L., Willet A.H., Roberts-Galbraith R.H., McDonald N.A., Feoktistova A., Chen J.S., Huang H., Guillen R., Boone C., Sidhu S.S., et al. The Cdc15 and Imp2 SH3 domains cooperatively scaffold a network of proteins that redundantly ensure efficient cell division in fission yeast. Mol. Biol. Cell. 2015;26:256–269. doi: 10.1091/mbc.E14-10-1451. PubMed DOI PMC

Oh Y., Schreiter J., Nishihama R., Wloka C., Bi E. Targeting and functional mechanisms of the cytokinesis-related F-BAR protein Hof1 during the cell cycle. Mol. Biol. Cell. 2013;24:1305–1320. doi: 10.1091/mbc.e12-11-0804. PubMed DOI PMC

Spencer S., Dowbenko D., Cheng J., Li W., Brush J., Utzig S., Simanis V., Lasky L.A. PSTPIP: A tyrosine phosphorylated cleavage furrow-associated protein that is a substrate for a PEST tyrosine phosphatase. J. Cell Biol. 1997;138:845–860. doi: 10.1083/jcb.138.4.845. PubMed DOI PMC

Arakaki Y., Fujiwara T., Kawai-Toyooka H., Kawafune K., Featherston J., Durand P.M., Miyagishima S.Y., Nozaki H. Evolution of cytokinesis-related protein localization during the emergence of multicellularity in volvocine green algae. BMC Evol. Biol. 2017;17:243. doi: 10.1186/s12862-017-1091-z. PubMed DOI PMC

Pertl-Obermeyer H., Lackner P., Schulze W.X., Hoepflinger M.C., Hoeftberger M., Foissner I., Obermeyer G. Dissecting the subcellular membrane proteome reveals enrichment of H+ (co-)transporters and vesicle trafficking proteins in acidic zones of Chara internodal cells. PLoS ONE. 2018;13:e0201480. doi: 10.1371/journal.pone.0201480. PubMed DOI PMC

Erffelinck M.L., Ribeiro B., Perassolo M., Pauwels L., Pollier J., Storme V., Goossens A. A user-friendly platform for yeast two-hybrid library screening using next generation sequencing. PLoS ONE. 2018;13:e0201270. doi: 10.1371/journal.pone.0201270. PubMed DOI PMC

Fàbregas N., Li N., Boeren S., Nash T.E., Goshe M.B., Clouse S.D., de Vries S., Caño-Delgado A.I. The Brassinosteroid Insensitive1-like3 signalosome complex regulates Arabidopsis root development. Plant Cell. 2013;25:3377–3388. doi: 10.1105/tpc.113.114462. PubMed DOI PMC

Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990;215:403–410. doi: 10.1016/S0022-2836(05)80360-2. PubMed DOI

Goodstein D.M., Shu S., Howson R., Neupane R., Hayes R.D., Fazo J., Mitros T., Dirks W., Hellsten U., Putnam N., et al. Phytozome: A comparative platform for green plant genomics. Nucleic Acids Res. 2012;40:1178–1186. doi: 10.1093/nar/gkr944. PubMed DOI PMC

Sundell D., Mannapperuma C., Netotea S., Delhomme N., Lin Y.C., Sjödin A., Van de Peer Y., Jansson S., Hvidsten T.R., Street N.R. The plant genome integrative explorer resource: PlantGenIE.org. New Phytol. 2015;208:1149–1156. doi: 10.1111/nph.13557. PubMed DOI

Rawat A., Brejšková L., Hála M., Cvrčková F., Žárský V. The Physcomitrella patens exocyst subunit EXO70.3d has distinct roles in growth and development, and is essential for completion of the moss life cycle. New Phytol. 2017;216:438–454. doi: 10.1111/nph.14548. PubMed DOI

Kumar S., Stecher G., Li M., Knyaz C., Tamura K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 2018;35:1547–1549. doi: 10.1093/molbev/msy096. PubMed DOI PMC

Rosero A., Oulehlová D., Stillerová L., Schiebertová P., Grunt M., Žárský V., Cvrčková F. Arabidopsis FH1 formin affects cotyledon pavement cell shape by modulating cytoskeleton dynamics. Plant Cell Physiol. 2016;57:488–504. doi: 10.1093/pcp/pcv209. PubMed DOI

Cvrčková F., Oulehlová D., Žárský V. Formins: Linking cytoskeleton and endomembranes in plant cells. Int. J. Mol. Sci. 2015;16:1–18. doi: 10.3390/ijms16010001. PubMed DOI PMC

Lu Q., Tang X., Tian G., Wang F., Liu K., Nguyen V., Kohalmi S.E., Keller W.A., Tsang E.W., Harada J.J., et al. Arabidopsis homolog of the yeast TREX-2 mRNA export complex: Components and anchoring nucleoporin. Plant J. 2010;61:259–270. doi: 10.1111/j.1365-313X.2009.04048.x. PubMed DOI

Konopka C.A., Bednarek S.Y. Comparison of the dynamics and functional redundancy of the Arabidopsis dynamin-related isoforms DRP1A and DRP1C during plant development. Plant Physiol. 2008;147:1590–1602. doi: 10.1104/pp.108.116863. PubMed DOI PMC

Karimi M., Bleys A., Vanderhaeghen R., Hilson P. Building blocks for plant gene assembly. Plant Physiol. 2007;145:1183–1191. doi: 10.1104/pp.107.110411. PubMed DOI PMC

Pečenková T., Pleskot R., Žárský V. Subcellular localization of Arabidopsis Pathogenesis-related 1 (PR1) protein. Int. J. Mol. Sci. 2017;18:825. doi: 10.3390/ijms18040825. PubMed DOI PMC

Oulehlová D., Kollárová E., Cifrová P., Pejchar P., Žárský V., Cvrčková F. Arabidopsis class I formin FH1 relocates between membrane compartments during root cell ontogeny and associates with plasmodesmata. Plant Cell Physiol. 2019;60:1855–1870. doi: 10.1093/pcp/pcz102. PubMed DOI

Schindelin J., Rueden C.T., Hiner M.C., Eliceiri K.W. The ImageJ ecosystem: An open platform for biomedical image analysis. Mol. Reprod. Dev. 2015;82:518–529. doi: 10.1002/mrd.22489. PubMed DOI PMC

Johansson M.U., Zoete V., Michielin O., Guex N. Defining and searching for structural motifs using DeepView/Swiss-PdbViewer. BMC Bioinform. 2012;13:173. doi: 10.1186/1471-2105-13-173. PubMed DOI PMC

Transmembrane formins as active cargoes of membrane trafficking

Arabidopsis Class II Formins AtFH13 and AtFH14 Can Form Heterodimers but Exhibit Distinct Patterns of Cellular Localization