The ARP2/3 complex and formins are the only known plant actin nucleators. Besides their actin-related functions, both systems also modulate microtubule organization and dynamics. Loss of the main housekeeping Arabidopsis thaliana Class I membrane-targeted formin FH1 (At3g25500) is known to increase cotyledon pavement cell lobing, while mutations affecting ARP2/3 subunits exhibit an opposite effect. Here we examine the role of FH1 and the ARP2/3 complex subunit ARPC5 (At4g01710) in epidermal cell morphogenesis with focus on pavement cells and trichomes using a model system of single fh1 and arpc5, as well as double fh1 arpc5 mutants. While cotyledon pavement cell shape in double mutants mostly resembled single arpc5 mutants, analysis of true leaf epidermal morphology, as well as actin and microtubule organization and dynamics, revealed a more complex relationship between the two systems and similar, rather than antagonistic, effects on some parameters. Both fh1 and arpc5 mutations increased actin network density and increased cell shape complexity in pavement cells and trichomes of first true leaves, in contrast to cotyledons. Thus, while the two actin nucleation systems have complementary roles in some aspects of cell morphogenesis in cotyledon pavement cells, they may act in parallel in other cell types and developmental stages.

Department of Experimental Plant Biology Faculty of Science Charles University Prague Czechia

Institute of Experimental Botany Academy of Sciences of the Czech Republic Prague Czechia

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Altartouri B., Bidhendi A. J., Tani T., Suzuki J., Conrad C., Chebli Y., et al. (2019). Pectin chemistry and cellulose crystallinity govern pavement cell morphogenesis in a multi-step mechanism. Plant Physiol. 181, 127–141.  10.1104/pp.19.00303 PubMed DOI PMC

Armour W. J., Barton D. A., Law A. M. K., Overall R. L. (2015). Differential growth in periclinal and anticlinal walls during lobe formation in Arabidopsis cotyledon pavement cells. Plant Cell 27, 2484–2500.  10.1105/tpc.114.126664 PubMed DOI PMC

Bartolini F., Gundersen G. G. (2010). Formins and microtubules. Biochim. Biophys. Acta 1803, 164–173.  10.1016/j.bbamcr.2009.07.006 PubMed DOI PMC

Bashline L., Lei L., Li S., Gu Y. (2014). Cell wall, cytoskeleton, and cell expansion in higher plants. Mol. Plant 7, 586–600.  10.1093/mp/ssu018 PubMed DOI

Basu D., El-Assal S. E. D., Le J., Mallery E. L., Szymanski D. B. (2004). Interchangeable functions of Arabidopsis PIROGI and the human WAVE complex subunit SRA1 during leaf epidermal development. Development 131, 4345–4355.  10.1242/dev.01307 PubMed DOI

Basu D., Le J., El-Assal S. E. D., Huang S., Zhang C. H., Mallery E. L., et al. (2005). DISTORTED3/SCAR2 is a putative Arabidopsis WAVE complex subunit that activates the Arp2/3 complex and is required for epidermal morphogenesis. Plant Cell 17, 502–524.  10.1105/tpc.104.027987 PubMed DOI PMC

Belteton S. A., Sawchuk M. G., Donohoe B. S., Scarpella E., Szymanski D. B. (2018). Reassessing the roles of PIN proteins and anticlinal microtubules during pavement cell morphogenesis. Plant Physiol. 176, 432–449.  10.1104/pp.17.01554 PubMed DOI PMC

Blanchoin L., Staiger C. J. (2010). Plant formins: diverse isoforms and unique molecular mechanism. Biochim. Biophys. Acta 1803, 201–206.  10.1016/j.bbamcr.2008.09.015 PubMed DOI

Blanchoin L., Boujemaa-Paterski R., Henty J. L., Khurana P., Staiger C. J. (2010). Actin dynamics in plant cells: a team effort from multiple proteins orchestrates this very fast-paced game. Curr. Opin. Plant Biol. 13, 714–723.  10.1016/j.pbi.2010.09.013 PubMed DOI

Bouton S., Leboeuf E., Mouille G., Leydecker M. T., Talbotec J., Granier F., et al. (2002). QUASIMODO1 encodes a putative membrane-bound glycosyltransferase required for normal pectin synthesis and cell adhesion in Arabidopsis. Plant Cell 14, 2577–2590.  10.1105/tpc.004259 PubMed DOI PMC

Buschmann H., Hauptmann M., Niessing D., Lloyd C. W., Schäffner A. R. (2009). Helical growth of the Arabidopsis mutant tortifolia2 does not depend on cell division patterns but involves handed twisting of isolated cells. Plant Cell 21, 2090–2106.  10.1105/tpc.108.061242 PubMed DOI PMC

Cabrera R., Suo J., Young E., Chang E. C. (2011). Schizosaccharomyces pombe Arc3 is a conserved subunit of the Arp2/3 complex required for polarity, actin organization, and endocytosis. Yeast 28, 495–503.  10.1002/yea.1853 PubMed DOI PMC

Campellone K. G., Webb N. J., Znameroski E. A., Welch M. D. (2008). WHAMM is an Arp2/3 complex activator that binds microtubules and functions in ER to Golgi transport. Cell 134, 148–161.  10.1016/j.cell.2008.05.032 PubMed DOI PMC

Cao L., Henty-Ridilla J. L., Blanchoin L., Staiger C. J. (2016). Profilin-dependent nucleation and assembly of actin filaments controls cell elongation in Arabidopsis. Plant Physiol. 170, 220–233.  10.1104/pp.15.01321 PubMed DOI PMC

Carlier M. F., Shekhar S. (2017). Global treadmilling coordinates actin turnover and controls the size of actin networks. Nat. Rev. Mol. Cell Biol. 18, 389–401.  10.1038/nrm.(2016)172 PubMed DOI

Carnahan R. H., Gould K. L. (2003). The PCH family protein, Cdc15p, recruits two F-actin nucleation pathways to coordinate cytokinetic actin ring formation in Schizosaccharomyces pombe . J. Cell Biol. 162, 851–862.  10.1083/jcb.200305012 PubMed DOI PMC

Copeland S. J., Thurston S. F., Copeland J. W. (2016). Actin- and microtubule-dependent regulation of Golgi morphology by FHDC1. Mol. Biol. Cell 27, 260–276.  10.1091/mbc.e15-02-0070 PubMed DOI PMC

Cvrčková F., Oulehlová D. (2017). A new kymogram-based method reveals unexpected effects of marker protein expression and spatial anisotropy of cytoskeletal dynamics in plant cell cortex. Plant Methods 13, 19.  10.1186/s13007-017-0171-9 PubMed DOI PMC

Cvrčková F., Oulehlová D., Žárský V. (2014). Formins: linking cytoskeleton and endomembranes in plant cells. Int. J. Mol. Sci. 16, 1–18.  10.3390/ijms16010001 PubMed DOI PMC

Cvrčková F., Oulehlová D., Žárský V. (2016). On growth and formins. Plant Signal. Behav. 11, e1155017.  10.1080/15592324.2016.1155017 PubMed DOI PMC

Cvrčková F. (2013). Formins and membranes: anchoring cortical actin to the cell wall and beyond. Front. Plant Sci. 4, 436.  10.3389/fpls.2013.00436 PubMed DOI PMC

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, 1209–1215.  10.1242/jcs.065557 PubMed DOI

Di Nardo A., Cicchetti G., Falet H., Hartwig J. H., Stossel T. P., Kwiatkowski D. J. (2005). Arp2/3 complex-deficient mouse fibroblasts are viable and have normal leading-edge actin structure and function. Proc. Natl. Acad. Sci. U.S.A. 102, 16263–16268.  10.1073/pnas.0508228102 PubMed DOI PMC

Diao M., Ren S., Wang Q., Qian L., Shen J., Liu Y., et al. (2018). Arabidopsis formin 2 regulates cell-to-cell trafficking by capping and stabilizing actin filaments at plasmodesmata. eLfe 7, e36316.  10.7554/eLife.36316 PubMed DOI PMC

Djakovic S., Dyachok J., Burke M., Frank M. J., Smith L. G. (2006). BRICK1/HSPC300 functions with SCAR and the ARP2/3 complex to regulate epidermal cell shape in Arabidopsis. Development 133, 1091–1100.  10.1242/dev.02280 PubMed DOI

Dominguez R. (2016). The WH2 domain and actin nucleation: necessary but insufficient. Trends Biochem. Sci. 41, 478–490.  10.1016/j.tibs.2016.03.004 PubMed DOI PMC

Dyachok J., Sparks J. A., Liao F., Wang Y. S., Blancaflor E. B. (2014). Fluorescent protein-based reporters of the actin cytoskeleton in living plant cells: fluorophore variant, actin binding domain, and promoter considerations. Cytoskeleton 71, 311–327.  10.1002/cm.21174 PubMed DOI

Edwards M., Zwolak A., Schafer D. A., Sept D., Dominguez R., Cooper J. A. (2014). Capping protein regulators fine-tune actin assembly dynamics. Nat. Rev. Mol. Cell Biol. 15, 677–689.  10.1038/nrm3869 PubMed DOI PMC

El-Assal S. E. D., Le J., Basu D., Mallery E. L., Szymanski D. B. (2004). Arabidopsis GNARLED encodes a NAP125 homolog that positively regulates ARP2/3. Curr. Biol. 14, 1405–1409.  10.1016/j.cub.2004.06.062 PubMed DOI

Facette M. R., Park Y., Sutimantanapi D., Luo A., Cartwright H. N., Yang B., et al. (2015). The SCAR/WAVE complex polarizes PAN receptors and promotes division asymmetry in maize. Nat. Plants 1, 14024.  10.1038/nplants.2014.24 PubMed DOI

Fišerová J., Schwarzerová K., Petrášek J., Opatrný Z. (2006). ARP2 and ARP3 are localized to sites of actin filament nucleation in tobacco BY-2 cells. Protoplasma 227, 119–128.  10.1007/s00709-006-0146-6 PubMed DOI

Finka A., Saidi Y., Goloubinoff P., Neuhaus J. M., Zryd J. P., Schaefer D. G. (2008). The knock-out of ARP3a gene affects F-actin cytoskeleton organization altering cellular tip growth, morphology and development in moss Physcomitrella patens . Cytoskeleton 65, 769–784.  10.1002/cm.20298 PubMed DOI

Fu Y., Li H., Yang Z. B. (2002). The ROP2 GTPase controls the formation of cortical fine F-actin and the early phase of directional cell expansion during Arabidopsis organogenesis. Plant Cell 14, 777–794.  10.1105/tpc.001537 PubMed DOI PMC

Gavrin A., Jansen V., Ivanov S., Bisseling T., Fedorova E. (2015). ARP2/3-mediated actin nucleation associated with symbiosome membrane is essential for the development of symbiosomes in infected cells of Medicago truncatula root nodules. Mol. Plant-Microbe Int. 28, 605–614.  10.1094/MPMI-12-14-0402-R PubMed DOI

Grikscheit K., Grosse R. (2016). Formins at the junction. Trends Biochem. Sci. 41, 148–159.  10.1016/j.tibs.2015.12.002 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, 115.  10.1186/1471-2148-8-115 PubMed DOI PMC

Gurel P. S., Hatch A. L., Higgs H. N. (2014). Connecting the cytoskeleton to the endoplasmic reticulum and Golgi. Curr. Biol. 24, R660–R672.  10.1016/j.cub.2014.05.033 PubMed DOI PMC

Hammer Ø., Harper D. A. T., Ryan P. D. (2001). PAST: Paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4, 1–9.

Harries P. A., Pan A., Quatrano R. S. (2005). Actin-related protein2/3 complex component ARPC1 is required for proper cell morphogenesis and polarized cell growth in Physcomitrella patens . Plant Cell 17, 2327–2339.  10.1105/tpc.105.033266 PubMed DOI PMC

Havelková L., Nanda G., Martinek J., Bellinvia E., Sikorová L., Šlajcherová K., et al. (2015). Arp2/3 complex subunit ARPC2 binds to microtubules. Plant Sci. 241, 96–108.  10.1016/j.plantsci.2015.10.001 PubMed DOI

Henty-Ridilla J. L., Rankova A., Eskin J. A., Kenny K., Goode B. L. (2016). Accelerated actin filament polymerization from microtubule plus ends. Science 352, 1004–1009.  10.1126/science.aaf1709 PubMed DOI PMC

Higaki T., Kutsuna N., Sano T., Kondo N., Hasezawa S. (2010). Quantification and cluster analysis of actin cytoskeletal structures in plant cells: role of actin bundling in stomatal movement during diurnal cycles in Arabidopsis guard cells. Plant J. 61, 156–165.  10.1111/j.1365-313x.2009.04032.x PubMed DOI

Hossain M. D., Liao J., James E. K., Sato S., Tabata S., Jurkiewicz A., et al. (2012). Lotus japonicus ARPC1 is required for rhizobial infection. Plant Physiol. 160, 917–928.  10.1104/pp.112.202572 PubMed DOI PMC

Huang J., Kim C. M., Xuan Y., Liu J., Kim T. H., Kim B. K., et al. (2013). Formin homology 1 (OsFH1) regulates root-hair elongation in rice (Oryza sativa). Planta 237, 1227–1239.  10.1007/s00425-013-1838-8 PubMed DOI

Hubert T., Perdu S., Vandekerckhove J., Gettemans J. (2011). γ-Tubulin localizes at actin-based membrane protrusions and inhibits formation of stress-fibers. Biochem. Biophys. Res. Commun. 408, 248–252.  10.1016/j.bbrc.2011.04.007 PubMed DOI

Ivakov A., Persson S. (2013). Plant cell shape: modulators and measurements. Front. Plant Sci. 4, 439.  10.3389/fpls.2013.00439 PubMed DOI PMC

Jimenez-Lopez J. C., Wang X., Kotchoni S. O., Huang S., Szymanski D. B., Staiger J. C. (2014). Heterodimeric capping protein from Arabidopsis is a membrane-associated, actin-binding protein. Plant Physiol. 166, 1312–1328.  10.1104/pp.114.242487 PubMed DOI PMC

Kijima S. T., Staiger C. J., Katoh K., Nagasaki A., Ito K., Uyeda T. Q. P. (2018). Arabidopsis vegetative actin isoforms, AtACT2 and AtACT7, generate distinct filament arrays in living plant cells. Sci. Rep. 8, 4381.  10.1038/s41598-018-22707-w PubMed DOI PMC

Le J., El Assal S. E. D., Basu D., Saad M. E., Szymanski D. B. (2003). Requirements for Arabidopsis ATARP2 and ATARP3 during epidermal development. Curr. Biol. 13, 1341–1347.  10.1016/S0960-9822(03)00493-7 PubMed DOI

Lei Y., Lu L., Liu H. Y., Li S., Xing F., Chen L. L. (2014). CRISPR-P: A web tool for synthetic single-guide RNA design of CRISPR-system in plants. Mol. Plant 7, 1494–1496.  10.1093/mp/ssu044 PubMed DOI

Li S. D., Blanchoin L., Yang Z. B., Lord E. M. (2003). The putative Arabidopsis Arp2/3 complex controls leaf cell morphogenesis. Plant Physiol. 132, 2034–2044.  10.1104/pp.103.028563 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, 2710–2726.  10.1105/tpc.110.075507 PubMed DOI PMC

Li X., Li J. H., Wang W., Chen N. Z., Ma T. S., et al. (2013). ARP2/3 complex-mediated actin dynamics is required for hydrogen peroxide-induced stomatal closure in Arabidopsis. Plant Cell Environ. 37, 1547–1560.  10.1111/pce.12259 PubMed DOI

Li J., Staiger B. H., Henty-Ridilla J. L., Abu-Abied M., Sadot E., Blanchoin L., et al. (2014). The availability of filament ends modulates actin stochastic dynamics in live plant cells. Mol. Biol. Cell 25, 1263–1275.  10.1091/mbc.e13-07-0378 PubMed DOI PMC

Liu R., Abreu-Blanco M. T., Barry K. C., Linardopoulou E. V., Osborn G. E., Parkhurst S. M. (2009). Wash functions downstream of Rho and links linear and branched actin nucleation factors. Development 136, 2849–2860.  10.1242/dev.035246 PubMed DOI PMC

Martinière 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, 354–365.  10.1111/j.1365-313X.2011.04497.x PubMed DOI

Mathur J., Chua N. H. (2000). Microtubule stabilization leads to growth reorientation in Arabidopsis trichomes. Plant Cell 12, 465–477.  10.1105/tpc.12.4.465 PubMed DOI PMC

Mathur J., Spielhofer P., Kost B., Chua N. (1999). The actin cytoskeleton is required to elaborate and maintain spatial patterning during trichome cell morphogenesis in Arabidopsis thaliana . Development 126, 5559–5568. PubMed

Mathur J., Mathur N., Kernebeck B., Hülskamp M. (2003. a). Mutations in actin-related proteins 2 and 3 affect cell shape development in Arabidopsis. Plant Cell 15, 1632–1645.  10.1105/tpc.011676 PubMed DOI PMC

Mathur J., Mathur N., Kirik V., Kernebeck B., Srinivas B. P., Hülskamp M. (2003. b). Arabidopsis CROOKED encodes for the smallest subunit of the ARP2/3 complex and controls cell shape by region specific fine F-actin formation. Development 130, 3137–3146.  10.1242/dev.00549 PubMed DOI

Mathur J. (2005). The ARP2/3 complex: giving plant cells a leading edge. Bioessays 27, 377–387.  10.1002/bies.20206 PubMed DOI

Michelot A., Berro J., Guérin C., Boujemaa-Paterski R., Staiger C. J., Martiel J. L., et al. (2007). Actin-filament stochastic dynamics mediated by ADF/Cofilin. Curr. Biol. 17, 825–833.  10.1016/j.cub.2007.04.037 PubMed DOI

Möller B., Poeschl Y., Plötner R., Bürstenbinder K. (2017). PaCeQuant: a tool for high-throughput quantification of pavement cell shape characteristics. Plant Physiol. 175, 998–1017.  10.1104/pp.17.00961 PubMed DOI PMC

Möller B., Poeschl Y., Klemm S., Bürstenbinder K. (2019). Morphological analysis of leaf epidermis pavement cells with PaCeQuant. Methods Mol. Biol. 1992, 329–349.  10.1007/978-1-4939-9469-4_22 PubMed DOI

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

Panteris E., Galatis B. (2005). The morphogenesis of lobed plant cells in the mesophyll and epidermis: organization and distinct roles of cortical microtubules and actin filaments. New Phytol. 167, 721–732.  10.1111/j.1469-8137.2005.01464.x PubMed DOI

Paredez A. R., Somerville C. R., Ehrhardt D. W. (2006). Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312, 1491–1495.  10.1126/science.1126551 PubMed DOI

Peremyslov V. V., Cole R. A., Fowler J. E., Dolja V. V. (2015). Myosin-powered membrane compartment drives cytoplasmic streaming, cell expansion and plant development. PloS One 10, e0139331.  10.1371/journal.pone.0139331 PubMed DOI PMC

Phillips P. C. (2008). Epistasis – the essential role of gene interactions in the structure and evolution of genetic systems. Nat. Rev. Genet. 9, 855–867.  10.1038/nrg2452 PubMed DOI PMC

Pizarro-Cerdá J., Chorev D. S., Geiger B., Cossart P. (2017). The diverse family of Arp2/3 complexes. Trends Cell Biol. 27, 93–100.  10.1016/j.tcb.2016.08.001 PubMed DOI PMC

Pleskot R., Pejchar P., Žárský V., Staiger C. J., Potocký M. (2012). Structural insights into the inhibition of actin-capping protein by interactions with phosphatidic acid and phosphatidylinositol (4,5)-bisphosphate. PloS Comput. Biol. 8, e1002765.  10.1371/journal.pcbi.1002765 PubMed DOI PMC

Qi J., Greb T. (2017). Cell polarity in plants: the Yin and Yang of cellular functions. Curr. Opin. Plant Biol. 35, 105–110.  10.1016/j.pbi.2016.11.015 PubMed DOI PMC

Qi T., Wang J., Sun Q., Day B., Guo J., Ma Q. (2017). TaARPC3 contributes to wheat resistance against the stripe rust fungus. Front. Plant Sci. 8, 1245.  10.3389/fpls.2017.01245 PubMed DOI PMC

Qiu L., Lin J., Xu J., Sato S., Parniske M., Wang T. L., et al. (2015). SCARN, a novel class of SCAR protein that is required for root hair infection during legume nodulation. PloS Genet. 11, e1005623.  10.1371/journal.pgen.1005623 PubMed DOI PMC

Rosero A., Žárský V., Cvrčková F. (2013). AtFH1 formin mutation affects actin filament and microtubule dynamics in Arabidopsis thaliana . J. Exp. Bot. 64, 585–597.  10.1093/jxb/ers351 PubMed DOI PMC

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

Rosero A., Oulehlová D., Žárský V., Cvrčková F. (2019). Visualizing and quantifying in vivo cortical cytoskeleton structure and dynamics. Meth. Mol. Biol. 1992, 135–149.  10.1007/978-1-4939-9469-4_9 PubMed DOI

Rosero A. (2013). Role of formins in the organization and dynamics of intracellular structures in Arabidopsis thaliana. [PhD thesis]. [Prague (CZ)]: Charles University; Available at https://is.cuni.cz/webapps/zzp/detail/84878/(accessed December 28, 2019).

Rotty J. D., Wu C., Bear J. E. (2013). New insights into the regulation and cellular functions of the ARP2/3 complex. Nat. Rev. Mol. Cell Biol. 14, 7–12.  10.1038/nrm3492 PubMed DOI

Rotty J. D., Wu C., Haynes E. M., Suarez C., Winkelman J. D., Johnson H. E., et al. (2015). Profilin-1 serves as a gatekeeper for actin assembly by Arp2/3-dependent and -independent pathways. Dev. Cell 32, 54–67.  10.1016/j.devcel.2014.10.026 PubMed DOI PMC

Saedler R., Mathur N., Srinivas B. P., Kernebeck B., Hülskamp M., Mathur J. (2004). Actin control over microtubules suggested by DISTORTED2 encoding the Arabidopsis ARPC2 subunit homolog. Plant. Cell Physiol. 45, 813–822.  10.1093/pcp/pch103 PubMed DOI

Sahi V. P., Cifrová P., García-González J., Kotannal Baby I., Mouillé G., Gineau E., et al. (2018). Arabidopsis thaliana plants lacking the ARP2/3 complex show defects in cell wall assembly and auxin distribution. Ann. Bot. 122, 777–789.  10.1093/aob/mcx178 PubMed DOI PMC

Sambade A., Findlay K., Schäffner A. R., Lloyd C. W., Buschmann H. (2014). Actin-dependent and -independent functions of cortical microtubules in the differentiation of arabidopsis leaf trichomes. Plant Cell 26, 1629–1644.  10.1105/tpc.113.118273 PubMed DOI PMC

Sampathkumar A., Gutierrez R., McFarlane H. E., Bringmann M., Lindeboom J., Emons A. M., et al. (2013). Patterning and lifetime of plasma membrane-localized cellulose synthase is dependent on actin organization in Arabidopsis interphase cells. Plant Physiol. 162, 675–688.  10.1104/pp.113.215277 PubMed DOI PMC

Sampathkumar A., Krupinski P., Wightman R., Milani P., Berquand A., Boudaoud A., et al. (2014). Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells. eLife 3, e01967.  10.7554/eLife.01967 PubMed DOI PMC

Sapala A., Runions J., Routier-Kierzkowska A. L., Das Gupta M., Hong L., Hofhuis H., et al. (2018). Why plants make puzzle cells, and how their shape emerges. eLife 7, e32794.  10.7554/eLife.32794 PubMed DOI PMC

Savaldi-Goldstein S., Peto C., Chory J. (2007). The epidermis both drives and restricts plant shoot growth. Nature 446, 199–202.  10.1038/nature05618 PubMed DOI

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

Schwab B., Mathur J., Saedler R., Schwarz H., Frey B., Scheidegger C., et al. (2003). Regulation of cell expansion by the DISTORTED genes in Arabidopsis thaliana: actin controls the spatial organization of microtubules. Mol. Genet. Genomics 269, 350–360.  10.1007/s00438-003-0843-1 PubMed DOI

Smith L. G., Oppenheimer D. G. (2005). Spatial control of cell expansion by the plant cytoskeleton. Annu. Rev. Cell. Dev. Biol. 21, 271–295.  10.1146/annurev.cellbio.21.122303.114901 PubMed DOI

Spitzer M., Wildenhain J., Rappsilber J., Tyers M. (2014). BoxPlotR: a web tool for generation of box plots. Nat. Methods 11, 121–122.  10.1038/nmeth.2811 PubMed DOI PMC

Staiger C. J., Sheahan M. B., Khurana P., Wang X., McCurdy D. W., Blanchoin L. (2009). Actin filament dynamics are dominated by rapid growth and severing activity in the Arabidopsis cortical array. J. Cell Biol. 184, 269–280.  10.1083/jcb.200806185 PubMed DOI PMC

Suarez C., Carroll R. T., Burke T. A., Christensen J. R., Bestul A. J., Sees J. A., et al. (2015). Profilin regulates F-actin network homeostasis by favoring formin over Arp2/3 complex. Dev. Cell 32, 43–53.  10.1016/j.devcel.2014.10.027 PubMed DOI PMC

Szymanski D. B., Cosgrove D. J. (2009). Dynamic coordination of cytoskeletal and cell wall systems during plant cell morphogenesis. Curr. Biol. 19, R800–R811.  10.1016/j.cub.2009.07.056 PubMed DOI

Szymanski D. B., Marks M. D., Wick S. M. (1999). Organized F-actin is essential for normal trichome morphogenesis in Arabidopsis. Plant Cell 11, 2331–2347.  10.1105/tpc.11.12.2331 PubMed DOI PMC

Tian J., Han L., Feng Z., Wang G., Liu W., Ma Y., et al. (2015). Orchestration of microtubules and the actin cytoskeleton in trichome cell shape determination by a plant-unique kinesin. eLife 4, e09351.  10.7554/eLife.09351 PubMed DOI PMC

Tsukaya H., Tsuge T., Uchimiya H. (1994). The cotyledon: a superior system for studies of leaf development. Planta 195, 309–312.  10.1007/BF00199692 DOI

Ueda K., Matsuyama T., Hashimoto T. (1999). Visualization of microtubules in living cells of transgenicArabidopsis thaliana . Protoplasma 206, 201–206.  10.1007/BF01279267 DOI

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

van der Honing H. S., van Bezouwen L. S., Emons A. M., Ketelaar T. (2011). High expression of Lifeact in Arabidopsis thaliana reduces dynamic reorganization of actin filaments but does not affect plant development. Cytoskeleton 68, 578–587.  10.1002/cm.20534 PubMed DOI

van der Kammen R., Song J. Y., de Rink I., Janssen H., Madonna S., Scarponi C., et al. (2017). Knockout of the Arp2/3 complex in epidermis causes a psoriasis-like disease hallmarked by hyperactivation of transcription factor Nrf2. Development 144, 4588–4603.  10.1242/dev.156323 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)P(2) is essential for polarized growth. J. Cell Biol. 198, 235–250.  10.1083/jcb.201112085 PubMed DOI PMC

Verger S., Chabout S., Gineau E., Mouille G. (2016). Cell adhesion in plants is under the control of putative O-fucosyltransferases. Development 143, 2536–2540.  10.1242/dev.132308 PubMed DOI PMC

Voigt B., Timmers A. C., Šamaj J., Müller J., Baluška F., Menzel D. (2005). GFP-FABD2 fusion construct allows in vivo visualization of the dynamic actin cytoskeleton in all cells of Arabidopsis seedlings. Eur. J. Cell Biol. 84, 95–608.  10.1016/j.ejcb.2004.11.011 PubMed DOI

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–S107.  10.1007/s00709-011-0368-0 PubMed DOI

Wang J., Zhang Y., Wu J., Meng L., Ren H. (2013). AtFH16, an Arabidopsis type II formin, binds and bundles both microfilaments and microtubules, and preferentially binds to microtubules. J. Int. Plant Biol. 55, 1002–1015.  10.1111/jipb.12089 PubMed DOI

Wang P., Richardson C., Hawes C., Hussey P. J. (2016). Arabidopsis NAP1 regulates the formation of autophagosomes. Curr. Biol. 26, 2060–2069.  10.1016/j.cub.2016.06.008 PubMed DOI

Winter D. C., Choe E. Y., Li R. (1999). Genetic dissection of the budding yeast Arp2/3 complex: a comparison of the in vivo and structural roles of individual subunits. Proc. Natl. Acad. Sci. U.S.A. 96, 7288–7293.  10.1073/pnas.96.13.7288 PubMed DOI PMC

Xing H. L., Dong L., Wang Z. P., Zhang H. Y., Han C. Y., Liu B., et al. (2014). A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol. 14, 327.  10.1186/s12870-014-0327-y PubMed DOI PMC

Yanagisawa M., Zhang C., Szymanski D. B. (2013). ARP2/3-dependent growth in the plant kingdom: SCARs for life. Front. Plant Sci. 4, 166.  10.3389/fpls.2013.00166 PubMed DOI PMC

Yanagisawa M., Desyatova A. S., Belteton S. A., Mallery E. L., Turner J. A., Szymanski D. B. (2015). Patterning mechanisms of cytoskeletal and cell wall systems during leaf trichome morphogenesis. Nat. Plants 1, 15014.  10.1038/nplants.2015.14 PubMed DOI

Yanagisawa M., Alonso J. M., Szymanski D. B. (2018). Microtubule-dependent confinement of a cell signaling and actin polymerization control module regulates polarized cell growth. Curr. Biol. 28, 2459–2466.  10.1016/j.cub.2018.05.076 PubMed DOI

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, 661–680.  10.1105/tpc.110.081802 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, 255–272.  10.1111/j.1469-8137.2009.02880.x PubMed DOI

Zhang X., Dyachok J., Krishnakumar S., Smith L. G., Oppenheimer D. G. (2005). IRREGULAR TRICHOME BRANCH1 in Arabidopsis encodes a plant homolog of the actin-related protein2/3 complex activator Scar/WAVE that regulates actin and microtubule organization. Plant Cell 17, 2314–2326.  10.1105/tpc.104.028670 PubMed DOI PMC

Zhang C., Mallery E. L., Schlueter J., Huang S., Fan Y., Brankle S., et al. (2008). Arabidopsis SCARs function interchangeably to meet Actin-related protein 2/3 activation thresholds during morphogenesis. Plant Cell 20, 995–1011.  10.1105/tpc.107.055350 PubMed DOI PMC

Zhang C., Halsey L. E., Szymanski D. B. (2011). The development and geometry of shape change in Arabidopsis thaliana cotyledon pavement cells. BMC Plant Biol. 11, 27.  10.1186/1471-2229-11-27 PubMed DOI PMC

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, 681–700.  10.1105/tpc.110.081349 PubMed DOI PMC

Zhang C., Mallery E., Reagan S., Boyko V. P., Kotchoni S. O., Szymanski D. B. (2013. a). The endoplasmic reticulum is a reservoir for WAVE/SCAR regulatory complex signaling in the Arabidopsis leaf. Plant Physiol. 162, 689–706.  10.1104/pp.113.217422 PubMed DOI PMC

Zhang C., Mallery E. L., Szymanski D. B. (2013. b). ARP2/3 localization in Arabidopsis leaf pavement cells: a diversity of intracellular pools and cytoskeletal interactions. Front. Plant Sci. 4, 238.  10.3389/fpls.2013.00238 PubMed DOI PMC

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