Formins are evolutionarily conserved eukaryotic proteins participating in actin and microtubule organization. Land plants have three formin clades, with only two - Class I and II - present in angiosperms. Class I formins are often transmembrane proteins, residing at the plasmalemma and anchoring the cortical cytoskeleton across the membrane to the cell wall, while Class II formins possess a PTEN-related membrane-binding domain. Lower plant Class III and non-plant formins usually contain domains predicted to bind RHO GTPases that are membrane-associated. Thus, some kind of membrane anchorage appears to be a common formin feature. Direct interactions between various non-plant formins and integral or peripheral membrane proteins have indeed been reported, with varying mechanisms and biological implications. Besides of summarizing new data on Class I and Class II formin-membrane relationships, this review surveys such "non-classical" formin-membrane interactions and examines which, if any, of them may be evolutionarily conserved and operating also in plants. FYVE, SH3 and BAR domain-containing proteins emerge as possible candidates for such conserved membrane-associated formin partners.

Department of Experimental Plant Biology Faculty of Science Charles University Prague Czech Republic

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Alexandropoulos K., Cheng G., Baltimore D. (1995). Proline-rich sequences that bind to Src homology 3 domains with individual specificities. Proc. Natl. Acad. Sci. U.S.A. 92 3110–311410.1073/pnas.92.8.3110 PubMed DOI PMC

Aspenström P. (2010). Formin-binding proteins: modulators of formin-dependent actin polymerization. Biochim. Biophys. Acta 1803 174–18210.1016/j.bbamcr.2009.06.002 PubMed DOI

Aspenström P., Richnau N., Johansson A. S. (2006). 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. 312 2180–219410.1016/j.yexcr.2006.03.013 PubMed DOI

Bak G., Lee E. J., Lee Y., Kato M., Segami S., Sze H., et al. (2013). Rapid structural changes and acidification of guard cell vacuoles during stomatal closure require phosphatidylinositol 3,5-bisphosphate. Plant Cell 25 2202–221610.1105/tpc.113.110411 PubMed DOI PMC

Banno H., Chua N. H. (2000). Characterization of the arabidopsis formin-like protein AFH1 and its interacting protein. Plant Cell Physiol. 41 617–62610.1093/pcp/41.5.617 PubMed DOI

Bartolini F., Gundersen G. G. (2010). Formins and microtubules. Biochim. Biophys. Acta 1803 164–17310.1016/j.bbamcr.2009.07.006 PubMed DOI PMC

Campos-Parra A. D., Hernández-Cuevas N. A., Hernández-Rivas R., Vargas M. (2010). EhNCABP166: a nucleocytoplasmic actin-binding protein from Entamoeba histolytica. Mol. Biochem. Parasitol. 172 19–3010.1016/j.molbiopara.2010.03.010 PubMed DOI

Castanon L., Abrami L., Holtzer C. P., Heisenberg F., van der Goot G, Gonzáles-Gaitán M. (2013). Anthrax toxin receptor 2a controls mitotic spindle positioning. Nat. Cell Biol. 15 28–3910.1038/ncb2632 PubMed DOI

Chalkia D., Nikolaidis N., Makalowski W., Klein J., Nei M. (2008). Origins and evolution of the formin multigene family that is involved in the formation of actin filaments. Mol. Biol. Evol. 25 2717–273310.1093/molbev/msn215 PubMed DOI PMC

Chesarone M. A., DuPage A. G., Goode B. L. (2010). Unleashing formins to remodel the actin and microtubule cytoskeletons. Nat. Rev. Mol. Cell Biol. 11 62–7410.1038/nrm2816 PubMed DOI

Cheung A. Y., Niroomand S., Zou Y., Wu H. (2010). A transmembrane formin nucleates subapical actin assembly and controls tip-focused growth in pollen tubes. Proc. Natl. Acad. Sci. U.S.A. 107 16390–1639510.1073/pnas.1008527107 PubMed DOI PMC

Cheung A. Y., Wu H. (2004). Overexpression of an Arabidopsis formin stimulates supernumerary actin cable formation from pollen tube cell membrane. Plant Cell 16 257–26910.1105/tpc.016550 PubMed DOI PMC

Chhabra E. S., Ramabhadran V., Gerber S. A., Higgs H. N. (2009). INF2 is an endoplasmic reticulum-associated formin protein. J. Cell Sci. 122 1430–144010.1242/jcs.040691 PubMed DOI PMC

Cvrčková F. (2000). Are plant formins integral membrane proteins? Genome Biol. 1, Research 001.10.1186/gb-2000-1-1-research001 PubMed DOI PMC

Cvrčková F. (2012). Formins: emerging players in the dynamic plant cell cortex. Scientifica 2012, Article ID 712605.10.6064/2012/712605 PubMed DOI PMC

Cvrčková F., Grunt M., Bezvoda R., Hála M., Kulich I., Rawat A., et al. (2012). Evolution of the land plant exocyst complexes. Front. Plant Sci. 3:15910.3389/fpls.2012.00159 PubMed DOI PMC

Cvrčková F., Novotný M., Pïcková D., Žárský V. (2004). Formin homology 2 domains occur in multiple contexts in angiosperms. BMC Genomics 5:4410.1186/1471-2164-5-44 PubMed DOI PMC

Deeks M. J., Cvrčková F., Machesky L. M., Mikitová V., Ketelaar T., Žárský V., et al. (2005). Arabidopsis group Ie formins localize to specific cell membrane domains, interact with actin-binding proteins and cause defects in cell expansion upon aberrant expression. New Phytol. 168 529–54010.1111/j.1469-8137.2005.01582.x PubMed DOI

Deeks M. J., Fendrych M., Smertenko A., Bell K. S., Oparka K., Cvrčková F., et al. (2010). The plant formin AtFH4 interacts with both actin and microtubules, and contains a newly identified microtubule-binding domain. J. Cell Sci. 123 1209–121510.1242/jcs.065557 PubMed DOI

Deeks M. J., Hussey P., Davies B. (2002). Formins: intermediates in signal transduction cascades that affect cytoskeletal reorganization. Trends Plant Sci. 7 492–49810.1016/S1360-1385(02)02341-5 PubMed DOI

Dempsey B. R., Razvanpour A., Lee T. W., Barber K. R., Junop M. S., Shaw G. S. (2012). Structure of an asymmetric ternary protein complex provides insight for membrane interaction. Structure 20 1737–174510.1016/j.str.2012.08.004 PubMed DOI

Dietrich S., Weiß S., Pleiser S., Kerkhoff E. (2013). Structural and functional insights into the Spir/formin actin nucleator complex. Biol. Chem. 10.1515/hsz-2013-0176 [Epub ahead of print]. PubMed DOI

Evangelista M., Pruyne D., Amberg D. C., Boone C., Bretscher A. (2002). Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast. Nat. Cell Biol. 4 32–4110.1038/ncb718 PubMed DOI

Favery B., Chelysheva L. A., Lebris M., Jammes F., Marmagne A., De Almeida-Engler J., et al. (2004). Arabidopsis formin AtFH6 is a plasma membrane-associated protein upregulated in giant cells induced by parasitic nematodes. Plant Cell 16 2529–254010.1105/tpc.104.024372 PubMed DOI PMC

Feng Y., Hartig S. M., Bechill J. E., Blanchard E. G., Caudell E., Corey S. J. (2010). The Cdc42-interacting protein-4 (CIP4) gene knock-out mouse reveals delayed and decreased endocytosis. J. Biol. Chem. 285 4348–435410.1074/jbc.M109.041038 PubMed DOI PMC

Frazier J., Field C. (1997). Actin cytoskeleton: are FH proteins local organizers? Curr. Biol. 7 R414–R41710.1016/S0960-9822(06)00205-3 PubMed DOI

Gachet Y., Hyams J. (2005). Endocytosis in fission yeast is spatially associated with the actin cytoskeleton during polarised cell growth and cytokinesis. J. Cell Sci. 118 4231–424210.1242/jcs.02530 PubMed DOI

Gasman S., Kalaidzidis Y., Zerial M. (2003). RhoD regulates endosome dynamics through Diaphanous-related formin and Src tyrosine kinase. Nat. Cell Biol. 5 195–20410.1038/ncb935 PubMed DOI

Gill M. B., Roecklein-Canfield J., Sage D. R., Zambela-Soediono M., Longtine N., Uknis M., et al. (2004). EBV attachment stimulates FHOS/FHOD1 redistribution and co-aggregation with CD21: formin interactions with the cytoplasmic domain of human CD21. J. Cell Sci. 117 2709–272010.1242/jcs.01113 PubMed DOI

Goode B. L., Eck M. J. (2007). Mechanism and function of formins in the control of actin assembly. Annu. Rev. Biochem. 76 593–62710.1146/annurev.biochem.75.103004.142647 PubMed DOI

Grunt M., Žárský V., Cvrčková F. (2008). Roots of angiosperm formins: the evolutionary history of plant FH2 domain-containing proteins. BMC Evol. Biol. 8:11510.1186/1471-2148-8-115 PubMed DOI PMC

Haase H. (2007). Ahnak, a new player in beta-adrenergic regulation of the cardiac L-type Ca2+ channel. Cardiovasc. Res. 73 19–2510.1016/j.cardiores.2006.09.001 PubMed DOI

Han Y., Yu G., Sarioglu H., Caballero-Martinez A., Schlott F., Ueffing M., et al. (2013). Proteomic investigation of the interactome of FMNL1 in hematopoietic cells unveils a role in calcium-dependent membrane plasticity. J. Proteomics 78 72–8210.1016/j.jprot.2012.11.015 PubMed DOI

Heath R. J., Insall R. H. (2008). F-BAR domains: multifunctional regulators of membrane curvature. J. Cell Sci. 121 1951–195410.1242/jcs.023895 PubMed DOI

Heil-Chapdelaine R., Adames N., Cooper J. A. (1999). Formin’ the connection between microtubules and the cell cortex. J. Cell Biol. 144 809–81110.1083/jcb.144.5.809 PubMed DOI PMC

Higgs H. N. (2005). Formin proteins: a domain-based approach. Trends Biochem. Sci. 30 342–35310.1016/j.tibs.2005.04.014 PubMed DOI

Higgs H. N., Peterson K. J. (2005). Phylogenetic analysis of the formin homology 2 domain. Mol. Biol. Cell 16 1–1310.1091/mbc.E04-07-0565 PubMed DOI PMC

Hirano T., Matsuzawa T., Takegawa K., Sato M. H. (2011). Loss-of-function and gain-of-function mutations in FAB1A/B impair endomembrane homeostasis, conferring pleiotropic developmental abnormalities in Arabidopsis. Plant Physiol. 155 797–80710.1104/pp.110.167981 PubMed DOI PMC

Hirano T., Sato M. H. (2011). Arabidopsis FAB1A/B is possibly involved in the recycling of auxin transporters. Plant Signal. Behav. 6 583–58510.1104/pp.110.16798 PubMed DOI PMC

Huett A., Ng A., Cao Z., Kuballa P., Komatsu M., Daly M. J., et al. (2009). A novel hybrid yeast-human network analysis reveals an essential role for FNBP1L in antibacterial autophagy. J. Immunol. 182 4917–493010.4049/jimmunol.0803050 PubMed DOI PMC

Idone V., Tam C., Andrews N. W. (2008). Two-way traffic on the road to membrane repair. Trends Cell Biol. 18 552–55910.1016/j.tcb.2008.09.001 PubMed DOI PMC

Ingouff M., FitzGerald J. N., Guerin C., Robert H., Sorensen M. B., Van Damme D., et al. (2005). Plant formin AtFH5 is an evolutionarily conserved actin nucleator involved in cytokinesis. Nat. Cell Biol. 7 374–38010.1038/ncb1238 PubMed DOI

Jacot D., Daher W., Soldati-Favre D. (2013). Toxoplasma gondii myosin F, an essential motor for centrosomes positioning and apicoplast inheritance. EMBO J. 32 1702–171610.1038/emboj.2013.113 PubMed DOI PMC

Kerkhoff E. (2011). Actin dynamics at intracellular membranes: the Spir/formin nucleator complex. Eur. J. Cell Biol. 90 922–92510.1016/j.ejcb.2010.10.011 PubMed DOI

Korobova F., Ramabhadran V., Higgs H. N. (2013). An actin-dependent step in mitochondrial fission mediated by the ER-associated formin INF2. Science 339 464–46710.1126/science.1228360 PubMed DOI PMC

Lam B. C., Sage T. L., Bianchi F., Blumwald E. (2001). Role of SH3 domain-containing proteins in clathrin-mediated vesicle trafficking in Arabidopsis. Plant Cell 13 2499–251210.1105/tpc.010279 PubMed DOI PMC

Li Y., Shen Y., Cai C., Zhong C., Zhu L., Yuan M., et al. (2010). The type II Arabidopsis formin14 interacts with microtubules and microfilaments to regulate cell division. Plant Cell 22 2710–272610.1105/tpc.110.075507 PubMed DOI PMC

Martiniere A., Gayral P., Hawes C., Runions J. (2011). Building bridges: formin1 of Arabidopsis forms a connection between the cell wall and the actin cytoskeleton. Plant J. 66 354–36510.1111/j.1365-313X.2011.04497.x PubMed DOI

Martiniere A., Lavagi I., Nageswaran G., Rolfe D. J., Maneta-Peyret L., Luu D. T., et al. (2012). Cell wall constrains lateral diffusion of plant plasma-membrane proteins. Proc. Natl. Acad. Sci. U.S.A. 109 12805–1281010.1073/pnas.1202040109 PubMed DOI PMC

Miyagi Y., Yamashita T., Fukaya M., Sonoda T., Okuno T., Yamada K., et al. (2002). Delphilin: a novel PDZ and formin homology domain-containing protein that synaptically colocalizes and interacts with glutamate receptor delta 2 subunit. J. Neurosci. 22 802–814 PubMed PMC

Mucha E., Fricke I., Schaefer A., Wittinghofer A., Berken A. (2011). Rho proteins of plants–functional cycle and regulation of cytoskeletal dynamics. Eur. J. Cell Biol. 90 934–94310.1016/j.ejcb.2010.11.009 PubMed DOI

Nelson B., Parsons A. B., Evangelista M., Schaefer K., Kennesy K., Ritchie S., et al. (2004). Fus1p interacts with components of the Hog1p mitogen-activated protein kinase and Cdc42p morphogenesis signaling pathways to control cell fusion during yeast mating. Genetics 166 67–7710.1534/genetics.166.1.67 PubMed DOI PMC

Otomo T., Tomchick D. R., Otomo C., Panchal S. C., Machius M., Rosen M. K. (2005). Structural basis of actin filament nucleation and processive capping by a formin homology 2 domain. Nature 433 488–49410.1038/nature03251 PubMed DOI

Pearson C. L., Xu K., Sharpless K. E., Harris S. D. (2004). MesA, a novel fungal protein required for the stabilization of polarity axes in Aspergillus nidulans. Mol. Biol. Cell 15 3658–367210.1091/mbc.E03-11-0803 PubMed DOI PMC

Prosser D., Drivas T., Maldonado L., Wendland B. (2011). Existence of a novel clathrin-independent endocytic pathway in yeast that depends on Rho1 and formin. J. Cell Sci. 195 657–67110.1083/jcb.201104045 PubMed DOI PMC

Pruyne D., Evangelista M., Yang C., Bi E., Zigmond S. H., Bretscher A., et al. (2002). Role of formins in actin assembly: nucleation and barbed-end association. Science 297 612–61510.1126/science.1072309 PubMed DOI

Quinlan M. E., Heuser J. E., Kerkhoff E., Mullins R. D. (2005). Drosophila Spire is an actin nucleation factor. Nature 433 382–38810.1038/nature03241 PubMed DOI

Rivero F., Muramoto T., Meyer A.-K., Urushihara H., Uyeda T. Q., Kitayama C. (2005). A comparative sequence analysis reveals a common GBD/FH3-FH1-FH2-DAD architecture in formins from Dictyostelium, fungi and metazoa. BMC Genomics 6:2810.1186/1471-2164-6-28 PubMed DOI PMC

Roberts-Galbraith R. H., Gould K. L. (2010). Setting the F-BAR: functions and regulation of the F-BAR protein family. Cell Cycle 9 4091–409710.4161/cc.9.20.13587 PubMed DOI

Rosero A., Žárský V., Cvrčková F. (2013). AtFH1 formin mutation affects actin filament and microtubule dynamics in Arabidopsis thaliana. J. Exp. Bot. 64 585–59710.1093/jxb/ers351 PubMed DOI PMC

Rousso T., Shewan A. M., Mostov K. E., Schejter E. D., Shilo B.-Z. (2013). Apical targeting of the formin Diaphanous in Drosophila tubular epithelia. ELife 2 e000666 10.7554/eLife.00666 PubMed DOI PMC

Rundle D. R., Gorbsky G., Tsokas L. (2004). PKD2 interacts and co-localizes with mDia1 to mitotic spindles of dividing cells: role of mDia1 in PKD2 localization to mitotic spindles. J. Biol. Chem. 279 29728–2973910.1074/jbc.M400544200 PubMed DOI

Sagot I., Klee S. K., Pellman D. (2002). Yeast formins regulate cell polarity by controlling the assembly of actin cables. Nat. Cell Biol. 4 42–5010.1038/ncb719 PubMed DOI

Shisheva A. (2008). PIKfyve: partners, significance, debates and paradoxes. Cell Biol. Int. 32 591–60410.1016/j.cellbi.2008.01.006 PubMed DOI PMC

Snaith H. A., Thompson J., Yates J. R., III., Sawin K. E. (2011). Characterization of Mug33 reveals complementary roles for actin cable-dependent transport and exocyst regulators in fission yeast exocytosis. J. Cell Sci. 124 2187–219910.1242/jcs.084038 PubMed DOI PMC

Toguchi M., Richnau N., Ruusala A, Aspenström P. (2010). Members of the CIP4 family of proteins participate in the regulation of platelet-derived growth factor receptor-beta-dependent actin reorganization and migration. Biol. Cell 102 215–23010.1042/BC20090033 PubMed DOI

Tong A. H., Drees B., Nardelli G., Bader G. D., Brannetti B., Castagnoli L., et al. (2002). A combined experimental and computational strategy to define protein interaction networks for peptide recognition modules. Science 295 321–32410.1126/science.1064987 PubMed DOI

Uetz P., Fumagalli S., James D., Zeller R. (1996). Molecular interaction between limb deformity proteins (formins) and Src family kinases. J. Biol. Chem. 271 33525–3353010.1074/jbc.271.52.33525 PubMed DOI

van Gisbergen P. A., Bezanilla M. (2013). Plant formins:membrane anchors for actin polymerization. Trends Cell Biol. 28 227–23310.1016/j.tcb.2012.12.001 PubMed DOI

van Gisbergen P. A., Li M., Wu S. Z., Bezanilla M. (2012). Class II formin targeting to the cell cortex by binding PI(3,5)P2 is essential for polarized growth. J. Cell Biol. 198 235–25010.1083/jcb.201112085 PubMed DOI PMC

Vaškovičová K., Žárský V., Rosel D., Nikoliè M., Buccione R., Cvrčková F., et al. (2013). Invasive cells in animals and plants: searching for LECA machineries in later eukaryotic life. Biol. Dir. 8, 8 10.1186/1745-6150-8-8 PubMed DOI PMC

Vidali L., van Gisbergen P. A., Guerin C., Franco P., Li M., Burkart G. M., et al. (2009). Rapid formin-mediated actin-filament elongation is essential for polarized plant cell growth. Proc. Natl. Acad. Sci. U.S.A. 106 13341–1334610.1073/pnas.0901170106 PubMed DOI PMC

Wakita Y., Kakimoto T., Katoh H., Negishi M. (2011). The F-BAR protein Rapostlin regulates dendritic spine formation in hippocampal neurons. J. Biol. Chem. 286 32672–3268310.1074/jbc.M111.236265 PubMed DOI PMC

Wang J., Xue X., Ren H. (2012). New insights into the role of plant formins: regulating the organization of the actin and microtubule cytoskeleton. Protoplasma 249 s101–s10710.1007/s00709-011-0368-0 PubMed DOI

Wang Y., Zhang W. Z., Song L. F., Zou J. J., Su Z., Wu W. H. (2008). Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis. Plant Physiol. 148 1201–121110.1104/pp.108.126375 PubMed DOI PMC

Watanabe N., Madaule P., Reid T., Ishizaki T., Watanabe G., Kakizuka A., et al. (1997). p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. EMBO J. 16 3044–305610.1093/emboj/16.11.3044 PubMed DOI PMC

Whitley P., Hinz S., Doughty J. (2009). Arabidopsis FAB1/PIKfyve proteins are essential for development of viable pollen. Plant Physiol. 151 1812–182210.1104/pp.109.146159 PubMed DOI PMC

Wyvial E., Singh S M. (2010). Identification and structural characterization of FYVE domain-containing proteins of Arabidopsis thaliana. BMC Plant Biol. 10:15710.1186/1471-2229-10-157 PubMed DOI PMC

Xu Y., Moseley J. B., Sagot I., Poy F., Pellman D., Goode B. L., et al. (2004). Crystal structures of a formin homology-2 domain reveal a tethered dimer architecture. Cell 116 711–72310.1016/S0092-8674(04)00210-7 PubMed DOI

Xue X., Guo C., Du F., Lu Q., Zhang C., Ren H. (2011). AtFH8 is involved in root development under effect of low-dose Latrunculin B in dividing cells. Mol. Plant 4 264–27810.1093/mp/ssq085 PubMed DOI

Yan S., Lv Z., Winterhoff M., Wenzl C., Zobel T., Faix J., et al. (2013). The F-BAR protein Cip4/Toca-1 antagonizes the formin Diaphanous in membrane stabilization and compartmentalization. J. Cell Sci. 126 1796–180510.1242/jcs.118422 PubMed DOI PMC

Yang C., Svitkina T. (2011). Filopodia initiation: focus on the Arp2/3 complex and formins. Cell Adh. Migr. 5 402–40810.4161/cam.5.5.16971 PubMed DOI PMC

Yang W., Ren S., Zhang X., Gao M., Ye S., Qi Y., et al. (2011). BENT UPPERMOST INTERNODE1 encodes the class II formin FH5 crucial for actin organization and rice development. Plant Cell 23 661–68010.1105/tpc.110.081802 PubMed DOI PMC

Ye J., Zheng Y., Yan A., Chen N., Wang Z., Huang S., et al. (2009). Arabidopsis formin3 directs the formation of actin cables and polarized growth in pollen tubes. Plant Cell 21 3868–388410.1105/tpc.109.068700 PubMed DOI PMC

Yi K., Guo C., Chen D., Zhao B., Yang B., Ren H. (2005). Cloning and functional characterization of a formin-like protein (AtFH8) from Arabidopsis. Plant Physiol. 138 1071–108210.1104/pp.104.055665 PubMed DOI PMC

Žárský V., Cvrčková F., Potocký M., Hála M. (2009). Exocytosis and cell polarity in plants - exocyst and recycling domains. New Phytol. 183 255–27210.1111/j.1469-8137.2009.02880.x PubMed DOI

Zhang Z., Zhang Y., Tan H., Wang Y., Li G., Liang W., et al. (2011). RICE MORPHOLOGY DETERMINANT encodes the type II formin FH5 and regulates rice morphogenesis. Plant Cell 23 681–70010.1105/tpc.110.081349 PubMed DOI PMC

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