Primary root growth is required by the plant to anchor in the soil and reach out for nutrients and water, while dealing with obstacles. Efficient root elongation and bending depends upon the coordinated action of environmental sensing, signal transduction, and growth responses. The actin cytoskeleton is a highly plastic network that constitutes a point of integration for environmental stimuli and hormonal pathways. In this review, we present a detailed compilation highlighting the importance of the actin cytoskeleton during primary root growth and we describe how actin-binding proteins, plant hormones, and actin-disrupting drugs affect root growth and root actin. We also discuss the feedback loop between actin and root responses to light and gravity. Actin affects cell division and elongation through the control of its own organization. We remark upon the importance of longitudinally oriented actin bundles as a hallmark of cell elongation as well as the role of the actin cytoskeleton in protein trafficking and vacuolar reshaping during this process. The actin network is shaped by a plethora of actin-binding proteins; however, there is still a large gap in connecting the molecular function of these proteins with their developmental effects. Here, we summarize their function and known effects on primary root growth with a focus on their high level of specialization. Light and gravity are key factors that help us understand root growth directionality. The response of the root to gravity relies on hormonal, particularly auxin, homeostasis, and the actin cytoskeleton. Actin is necessary for the perception of the gravity stimulus via the repositioning of sedimenting statoliths, but it is also involved in mediating the growth response via the trafficking of auxin transporters and cell elongation. Furthermore, auxin and auxin analogs can affect the composition of the actin network, indicating a potential feedback loop. Light, in its turn, affects actin organization and hence, root growth, although its precise role remains largely unknown. Recently, fundamental studies with the latest techniques have given us more in-depth knowledge of the role and organization of actin in the coordination of root growth; however, there remains a lot to discover, especially in how actin organization helps cell shaping, and therefore root growth.

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

Laboratory of Hormonal Regulations in Plants Institute of Experimental Botany Czech Academy of Sciences Prague Czechia

Plant Ecophysiology Department of Biology Faculty of Science Utrecht University Utrecht Netherlands

Zobrazit více v PubMed

Abu-Abied M., Belausov E., Hagay S., Peremyslov V., Dolja V., Sadot E. (2018). Myosin XI-K is involved in root organogenesis, polar auxin transport, and cell division. J. Exp. Bot. 69, 2869–2881. doi: 10.1093/jxb/ery112, PMID: PubMed DOI PMC

Arieti R. S., Staiger C. J. (2020). Auxin-induced actin cytoskeleton rearrangements require AUX1. New Phytol. 226, 441–459. doi: 10.1111/nph.16382, PMID: PubMed DOI PMC

Baluška F., Hasenstein K. H. (1997). Root cytoskeleton: its role in perception of and response to gravity. Planta 203, S69–S78. doi: 10.1007/PL00008117, PMID: PubMed DOI

Baluška F., Hlavačka A., Šamaj J., Palme K., Robinson D. G., Matoh T., et al. . (2002). F-actin-dependent endocytosis of cell wall pectins in meristematic root cells. Insights from brefeldin A-induced compartments. Plant Physiol. 130, 422–431. doi: 10.1104/pp.007526, PMID: PubMed DOI PMC

Baluška F., Jasik J., Edelmann H. G., Salajová T., Volkmann D. (2001). Latrunculin B-induced plant dwarfism: plant cell elongation is F-actin-dependent. Dev. Biol. 231, 113–124. doi: 10.1006/dbio.2000.0115, PMID: PubMed DOI

Baluška F., Vitha S., Barlow P. W., Volkmann D. (1997). Rearrangements of F-actin arrays in growing cells of intact maize root apex tissues: a major developmental switch occurs in the postmitotic transition region. Eur. J. Cell Biol. 72, 113–121. PMID: PubMed

Barrada A., Montané M.-H., Robaglia C., Menand B. (2015). Spatial regulation of root growth: placing the plant TOR pathway in a developmental perspective. Int. J. Mol. Sci. 16, 19671–19697. doi: 10.3390/ijms160819671, PMID: PubMed DOI PMC

Blancaflor E. B. (2002). The cytoskeleton and gravitropism in higher plants. J. Plant Growth Regul. 21, 120–136. doi: 10.1007/s003440010041, PMID: PubMed DOI

Blancaflor E. B. (2013). Regulation of plant gravity sensing and signaling by the actin cytoskeleton. Am. J. Bot. 100, 143–152. doi: 10.3732/ajb.1200283, PMID: PubMed DOI

Blancaflor E. B., Hasenstein K. H. (1997). The organization of the actin cytoskeleton in vertical and graviresponding primary roots of maize. Plant Physiol. 113, 1447–1455. doi: 10.1104/pp.113.4.1447, PMID: PubMed DOI PMC

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. doi: 10.1016/j.pbi.2010.09.013, PMID: PubMed DOI

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. doi: 10.1104/pp.15.01321, PMID: PubMed DOI PMC

Cifrová P., Oulehlová D., Kollárová E., Martinek J., Rosero A., Žárský V., et al. . (2020). Division of labor between two actin nucleators—the formin FH1 and the ARP2/3 complex—in Arabidopsis epidermal cell morphogenesis. Front. Plant Sci. 11:148. doi: 10.3389/fpls.2020.00148, PMID: PubMed DOI PMC

Clément M., Ketelaar T., Rodiuc N., Banora M. Y., Smertenko A., Engler G., et al. . (2009). Actin-depolymerizing factor2-mediated actin dynamics are essential for root-knot nematode infection of Arabidopsis. Plant Cell 21, 2963–2979. doi: 10.1105/tpc.109.069104, PMID: PubMed DOI PMC

Crowell E. F., Bischoff V., Desprez T., Rolland A., Stierhof Y.-D., Schumacher K., et al. . (2009). Pausing of golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis. Plant Cell 21, 1141–1154. doi: 10.1105/tpc.108.065334, PMID: PubMed DOI PMC

Cvrčková F. (2012). Formins: emerging players in the dynamic plant cell cortex. Scientifica 2012:712605. doi: 10.6064/2012/712605, PMID: PubMed DOI PMC

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

de Bang L., Paez-Garcia A., Cannon A. E., Chin S., Kolape J., Liao F., et al. . (2020). Brassinosteroids inhibit autotropic root straightening by modifying filamentous-actin organization and dynamics. Front. Plant Sci. 11:5. doi: 10.3389/fpls.2020.00005, PMID: PubMed DOI PMC

Deeks M. J., Calcutt J. R., Ingle E. K. S., Hawkins T. J., Chapman S., Richardson A. C., et al. . (2012). A superfamily of actin-binding proteins at the actin-membrane nexus of higher plants. Curr. Biol. 22, 1595–1600. doi: 10.1016/j.cub.2012.06.041, PMID: PubMed DOI

Deeks M. J., Cvrcková F., Machesky L. M., Mikitová V., Ketelaar T., Zársky 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, 529–540. doi: 10.1111/j.1469-8137.2005.01582.x, PMID: PubMed DOI

Dhonukshe P., Grigoriev I., Fischer R., Tominaga M., Robinson D. G., Hasek J., et al. . (2008). Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes. Proc. Natl. Acad. Sci. U. S. A. 105, 4489–4494. doi: 10.1073/pnas.0711414105, PMID: PubMed DOI PMC

Dong C. H., Kost B., Xia G., Chua N. H. (2001a). Molecular identification and characterization of the Arabidopsis AtADF1, AtADFS, and AtADF6 genes. Plant Mol. Biol. 45, 517–527. doi: 10.1023/a:1010687911374, PMID: PubMed DOI

Dong C. H., Xia G. X., Hong Y., Ramachandran S., Kost B., Chua N. H. (2001b). ADF proteins are involved in the control of flowering and regulate F-actin organization, cell expansion, and organ growth in Arabidopsis. Plant Cell 13, 1333–1346. doi: 10.1105/tpc.13.6.1333, PMID: PubMed DOI PMC

Dünser K., Gupta S., Herger A., Feraru M. I., Ringli C., Kleine-Vehn J. (2019). Extracellular matrix sensing by FERONIA and leucine-rich repeat extensins controls vacuolar expansion during cellular elongation in Arabidopsis thaliana. EMBO J. 38, 1–12. doi: 10.15252/embj.2018100353, PMID: PubMed DOI PMC

Dyachok J., Shao M.-R., Vaughn K., Bowling A., Facette M., Djakovic S., et al. . (2008). Plasma membrane-associated SCAR complex subunits promote cortical F-actin accumulation and normal growth characteristics in Arabidopsis roots. Mol. Plant 1, 990–1006. doi: 10.1093/mp/ssn059, PMID: PubMed DOI

Dyachok J., Zhu L., Liao F., He J., Huq E., Blancaflor E. B. (2011). SCAR mediates light-induced root elongation in Arabidopsis through photoreceptors and proteasomes. Plant Cell 23, 3610–3626. doi: 10.1105/tpc.111.088823, PMID: PubMed DOI PMC

El-Assal S. E. D., Le J., Basu D., Mallery E. L., Szymanski D. B., El-Din El-Assal S., et al. . (2004). DISTORTED2 encodes an ARPC2 subunit of the putative Arabidopsis ARP2/3 complex. Plant J. 38, 526–538. doi: 10.1111/j.1365-313X.2004.02065.x, PMID: PubMed DOI

Evans M. L., Ishikawa H., Estelle M. A. (1994). Responses of Arabidopsis roots to auxin studied with high temporal resolution: comparison of wild type and auxin-response mutants. Planta 194, 215–222. doi: 10.1007/BF01101680 DOI

Fan T., Zhai H., Shi W., Wang J., Jia H., Xiang Y., et al. . (2013). Overexpression of profilin 3 affects cell elongation and F-actin organization in Arabidopsis thaliana. Plant Cell Rep. 32, 149–160. doi: 10.1007/s00299-012-1349-2, PMID: PubMed DOI

Fendrych M., Akhmanova M., Merrin J., Glanc M., Hagihara S., Takahashi K., et al. . (2018). Rapid and reversible root growth inhibition by TIR1 auxin signalling. Nat. Plants 4, 453–459. doi: 10.1038/s41477-018-0190-1, PMID: PubMed DOI PMC

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. doi: 10.1007/s00709-006-0146-6, PMID: PubMed DOI

Friml J., Wiśniewska J., Benková E., Mendgen K., Palme K. (2002). Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415, 806–809. doi: 10.1038/415806a, PMID: PubMed DOI

García-González J., Kebrlová Š., Semerák M., Lacek J., Kotannal Baby I., Petrášek J., et al. . (2020). Arp2/3 complex is required for auxin-driven cell expansion through regulation of auxin transporter homeostasis. Front. Plant Sci. 11:486. doi: 10.3389/fpls.2020.00486, PMID: PubMed DOI PMC

Geldner N., Friml J., Stierhof Y. D., Jürgens G., Palme K. (2001). Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413, 425–428. doi: 10.1038/35096571, PMID: PubMed DOI

Gilliland L. U., Pawloski L. C., Kandasamy M. K., Meagher R. B. (2003). Arabidopsis actin gene ACT7 plays an essential role in germination and root growth. Plant J. 33, 319–328. doi: 10.1046/j.1365-313X.2003.01626.x, PMID: PubMed DOI

Glanc M., Fendrych M., Friml J. (2019). PIN2 polarity establishment in Arabidopsis in the absence of an intact cytoskeleton. Biomolecules 9:222. doi: 10.3390/BIOM9060222, PMID: PubMed DOI PMC

Grunt M., Zárský V., Cvrcková F. (2008). Roots of angiosperm formins: the evolutionary history of plant FH2 domain-containing proteins. BMC Evol. Biol. 8:115. doi: 10.1186/1471-2148-8-115, PMID: 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. doi: 10.1016/j.plantsci.2015.10.001, PMID: PubMed DOI

Henty J. L., Bledsoe S. W., Khurana P., Meagher R. B., Day B., Blanchoin L., et al. . (2011). Arabidopsis actin depolymerizing factor4 modulates the stochastic dynamic behavior of actin filaments in the cortical array of epidermal cells. Plant Cell 23, 3711–3726. doi: 10.1105/tpc.111.090670, PMID: PubMed DOI PMC

Henty-Ridilla J. L., Shimono M., Li J., Chang J. H., Day B., Staiger C. J. (2013). The plant actin cytoskeleton responds to signals from microbe-associated molecular patterns. PLoS Pathog. 9:e1003290. doi: 10.1371/journal.ppat.1003290, PMID: PubMed DOI PMC

Higaki T., Kutsuna N., Okubo E., Sano T., Hasezawa S. (2006). Actin microfilaments regulate vacuolar structures and dynamics: dual observation of actin microfilaments and vacuolar membrane in living tobacco BY-2 cells. Plant Cell Physiol. 47, 839–852. doi: 10.1093/pcp/pcj056, PMID: PubMed DOI

Hou G., Mohamalawari D. R., Blancaflor E. B. (2003). Enhanced gravitropism of roots with a disrupted cap actin cytoskeleton. Plant Physiol. 131, 1360–1373. doi: 10.1104/pp.014423, PMID: PubMed DOI PMC

Huang S., Qu X., Zhang R. (2015). Plant villins: versatile actin regulatory proteins. J. Integr. Plant Biol. 57, 40–49. doi: 10.1111/jipb.12293, PMID: PubMed DOI

Huang J.-B., Zou Y., Zhang X., Wang M., Dong Q., Tao L.-Z. (2020). RIBOSE PHOSPHATE ISOMERSASE 1 influences root development by acting on cell wall biosynthesis, actin organization, and auxin transport in Arabidopsis. Front. Plant Sci. 10:1641. doi: 10.3389/FPLS.2019.01641, PMID: PubMed DOI PMC

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

Ioio R. D., Linhares F. S., Scacchi E., Casamitjana-Martinez E., Heidstra R., Costantino P., et al. . (2007). Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Curr. Biol. 17, 678–682. doi: 10.1016/j.cub.2007.02.047, PMID: PubMed DOI

Ioio R. D., Nakamura K., Moubayidin L., Perilli S., Taniguchi M., Morita M. T., et al. . (2008). A genetic framework for the control of cell division and differentiation in the root meristem. Science 322, 1380–1384. doi: 10.1126/science.1164147, PMID: PubMed DOI

Iwabuchi K., Minamino R., Takagi S. (2010). Actin reorganization underlies phototropin-dependent positioning of nuclei in Arabidopsis leaf cells. Plant Physiol. 152, 1309–1319. doi: 10.1104/pp.109.149526, PMID: PubMed DOI PMC

Jacques E., Lewandowski M., Buytaert J., Fierens Y., Verbelen J.-P., Vissenberg K. (2013). Microfilament analyzer identifies actin network organizations in epidermal cells of Arabidopsis thaliana roots. Plant Signal. Behav. 8:e24821. doi: 10.4161/psb.24821, PMID: PubMed DOI PMC

Kaiser S., Eisa A., Kleine-Vehn J., Scheuring D. (2019). NET4 modulates the compactness of vacuoles in Arabidopsis thaliana. Int. J. Mol. Sci. 20:4752. doi: 10.3390/ijms20194752, PMID: PubMed DOI PMC

Kaiser S., Scheuring D. (2020). To lead or to follow: contribution of the plant vacuole to cell growth. Front. Plant Sci. 11:553. doi: 10.3389/fpls.2020.00553, PMID: PubMed DOI PMC

Kandasamy M. K., Burgos-Rivera B., McKinney E. C., Ruzicka D. R., Meagher R. B. (2007). Class-specific interaction of profilin and ADF isovariants with actin in the regulation of plant development. Plant Cell 19, 3111–3126. doi: 10.1105/tpc.107.052621, PMID: PubMed DOI PMC

Kandasamy M. K., Gilliland L. U., McKinney E. C., Meagher R. B. (2001). One plant actin isovariant, ACT7, is induced by auxin and required for normal callus formation. Plant Cell 13, 1541–1554. doi: 10.1105/TPC.010026, PMID: PubMed DOI PMC

Kandasamy M. K., McKinney E. C., Meagher R. B. (2002). Plant profilin isovariants are distinctly regulated in vegetative and reproductive tissues. Cell Motil. Cytoskeleton 52, 22–32. doi: 10.1002/cm.10029, PMID: PubMed DOI

Kandasamy M. K., McKinney E. C., Meagher R. B. (2009). A single vegetative actin isovariant overexpressed under the control of multiple regulatory sequences is sufficient for normal Arabidopsis development. Plant Cell 21, 701–718. doi: 10.1105/tpc.108.061960, PMID: PubMed DOI PMC

Kato T., Morita M. T., Tasaka M. (2010). Defects in dynamics and functions of actin filament in Arabidopsis caused by the dominant-negative actin fiz1-induced fragmentation of actin filament. Plant Cell Physiol. 51, 333–338. doi: 10.1093/pcp/pcp189, PMID: PubMed DOI

Ketelaar T., Allwood E. G., Anthony R., Voigt B., Menzel D., Hussey P. J. (2004). The actin-interacting protein AIP1 is essential for actin organization and plant development. Curr. Biol. 14, 145–149. doi: 10.1016/j.cub.2004.01.004, PMID: PubMed DOI

Khurana P., Henty J. L., Huang S., Staiger A. M., Blanchoin L., Staiger C. J. (2010). Arabidopsis VILLIN1 and VILLIN3 have overlapping and distinct activities in actin bundle formation and turnover. Plant Cell 22, 2727–2748. doi: 10.1105/tpc.110.076240, PMID: PubMed DOI PMC

Klahre U., Chua N. H. (1999). The Arabidopsis ACTIN-RELATED PROTEIN 2 (AtARP2) promoter directs expression in xylem precursor cells and pollen. Plant Mol. Biol. 41, 65–73. doi: 10.1023/A:1006247600932, PMID: PubMed DOI

Klahre U., Friederich E., Kost B., Louvard D., Chua N. H. (2000). Villin-like actin-binding proteins are expressed ubiquitously in Arabidopsis. Plant Physiol. 122, 35–48. doi: 10.1104/pp.122.1.35, PMID: PubMed DOI PMC

Kleine-Vehn J., Ding Z., Jones A. R., Tasaka M., Morita M. T., Friml J. (2010). Gravity-induced PIN transcytosis for polarization of auxin fluxes in gravity-sensing root cells. Proc. Natl. Acad. Sci. U. S. A. 107, 22344–22349. doi: 10.1073/pnas.1013145107, PMID: PubMed DOI PMC

Kleine-Vehn J., Huang F., Naramoto S., Zhang J., Michniewicz M., Offringa R., et al. . (2009). PIN auxin efflux carrier polarity is regulated by PINOID kinase-mediated recruitment into GNOM-independent trafficking in Arabidopsis. Plant Cell 21, 3839–3849. doi: 10.1105/tpc.109.071639, PMID: PubMed DOI PMC

Kushwah S., Jones A. M., Laxmi A. (2011). Cytokinin-induced root growth involves actin filament reorganization. Plant Signal. Behav. 6, 1848–1850. doi: 10.4161/psb.6.11.17641, PMID: PubMed DOI PMC

Lanza M., Garcia-Ponce B., Castrillo G., Catarecha P., Sauer M., Rodriguez-Serrano M., et al. . (2012). Role of actin cytoskeleton in brassinosteroid signaling and in its integration with the auxin response in plants. Dev. Cell 22, 1275–1285. doi: 10.1016/j.devcel.2012.04.008, PMID: PubMed DOI

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. doi: 10.1016/S0960-9822(03)00493-7, PMID: PubMed DOI

Leontovyčová H., Kalachova T., Janda M. (2020). Disrupted actin: a novel player in pathogen attack sensing? New Phytol. 227, 1605–1609. doi: 10.1111/nph.16584, PMID: PubMed DOI

Leontovyčová H., Kalachova T., Trdá L., Pospíchalová R., Lamparová L., Dobrev P. I., et al. . (2019). Actin depolymerization is able to increase plant resistance against pathogens via activation of salicylic acid signalling pathway. Sci. Rep. 9, 1–10. doi: 10.1038/s41598-019-46465-5, PMID: PubMed DOI PMC

Leucci M. R., Di Sansebastiano G.-P., Gigante M., Dalessandro G., Piro G. (2006). Secretion marker proteins and cell-wall polysaccharides move through different secretory pathways. Planta 225, 1001–1017. doi: 10.1007/S00425-006-0407-9, PMID: PubMed DOI

Li S., Blanchoin L., Yang Z., Lord E. M. (2003). The putative Arabidopsis Arp2/3 complex controls leaf cell morphogenesis. Plant Physiol. 132, 2034–2044. doi: 10.1104/pp.103.028563, PMID: PubMed DOI PMC

Li P., Day B. (2019). Battlefield cytoskeleton: turning the tide on plant immunity. Mol. Plant-Microbe Interact. 32, 25–34. doi: 10.1094/MPMI-07-18-0195-FI, PMID: PubMed DOI PMC

Li G., Liang W., Zhang X., Ren H., Hu J., Bennett M. J., et al. . (2014). Rice actin-binding protein RMD is a key link in the auxin-actin regulatory loop that controls cell growth. Proc. Natl. Acad. Sci. U. S. A. 111, 10377–10382. doi: 10.1073/pnas.1401680111, PMID: PubMed DOI PMC

Li L.-J., Ren F., Gao X.-Q., Wei P.-C., Wang X.-C. (2013). The reorganization of actin filaments is required for vacuolar fusion of guard cells during stomatal opening in Arabidopsis. Plant Cell Environ. 36, 484–497. doi: 10.1111/j.1365-3040.2012.02592.x, PMID: PubMed DOI

Li L., Xu J., Xu Z.-H., Xue H.-W. (2005). Brassinosteroids stimulate plant tropisms through modulation of polar auxin transport in Brassica and Arabidopsis. Plant Cell 17, 2738–2753. doi: 10.1105/tpc.105.034397, PMID: PubMed DOI PMC

Ma Q., Robert S. (2014). Auxin biology revealed by small molecules. Physiol. Plant. 151, 25–42. doi: 10.1111/ppl.12128, PMID: PubMed DOI

Maeda K., Sasabe M., Hanamata S., Machida Y., Hasezawa S., Higaki T. (2020). Actin filament disruption alters phragmoplast microtubule dynamics during the initial phase of plant cytokinesis. Plant Cell Physiol. 61, 445–456. doi: 10.1093/pcp/pcaa003, PMID: PubMed DOI

Mancuso S., Barlow P. W., Volkmann D., Baluška F. (2006). Actin turnover-mediated gravity response in maize root apices: gravitropism of decapped roots implicates gravisensing outside of the root cap. Plant Signal. Behav. 1, 52–58. doi: 10.4161/psb.1.2.2432, PMID: PubMed DOI PMC

Mao H., Nakamura M., Viotti C., Grebe M. (2016). A framework for lateral membrane trafficking and polar tethering of the PEN3 ATP-binding cassette transporter. Plant Physiol. 172, 2245–2260. doi: 10.1104/pp.16.01252, PMID: PubMed DOI PMC

Mathur J., Mathur N., Kirik V., Kernebeck B., Srinivas B. P., Hülskamp M. (2003). 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. doi: 10.1242/dev.00549, PMID: PubMed DOI

McDowell J. M., Huang S., McKinney E. C., An Y. Q., Meagher R. B. (1996). Structure and evolution of the actin gene family in Arabidopsis thaliana. Genetics 142, 587–602. doi: 10.1093/genetics/142.2.587, PMID: PubMed DOI PMC

McKinney E. C., Kandasamy M. K., Meagher R. B. (2001). Small changes in the regulation of one Arabidopsis profilin isovariant, PRF1, alter seedling development. Plant Cell 13, 1179–1191. doi: 10.1105/tpc.13.5.1179, PMID: PubMed DOI PMC

Meagher R. B., McKinney E. C., Kandasamy M. K. (2000). “The significance of diversity in the plant actin gene family” in Actin: A Dynamic Framework for Multiple Plant Cell Functions. eds. C. J. Staiger, F. Baluška, D. Volkmann, and P. W. Barlow (Dordrecht: Springer Netherlands; ), 3–27.

Meagher R. B., McKinney E. C., Vitale A. V. (1999). The evolution of new structures: clues from plant cytoskeletal genes. Trends Genet. 15, 278–284. doi: 10.1016/S0168-9525(99)01759-X, PMID: PubMed DOI

Michelot A., Guérin C., Huang S., Ingouff M., Richard S., Rodiuc N., et al. . (2005). The formin homology 1 domain modulates the actin nucleation and bundling activity of Arabidopsis FORMIN1. Plant Cell 17, 2296–2313. doi: 10.1105/tpc.105.030908, PMID: PubMed DOI PMC

Müssar K. J., Kandasamy M. K., McKinney E. C., Meagher R. B. (2015). Arabidopsis plants deficient in constitutive class profilins reveal independent and quantitative genetic effects. BMC Plant Biol. 15:177. doi: 10.1186/s12870-015-0551-0, PMID: PubMed DOI PMC

Nakamura M., Nishimura T., Morita M. T. (2019). Gravity sensing and signal conversion in plant gravitropism. J. Exp. Bot. 70, 3495–3506. doi: 10.1093/jxb/erz158, PMID: PubMed DOI

Nakamura M., Toyota M., Tasaka M., Morita M. T. (2011). An Arabidopsis E3 ligase, SHOOT GRAVITROPISM9, modulates the interaction between statoliths and F-actin in gravity sensing. Plant Cell 23, 1830–1848. doi: 10.1105/tpc.110.079442, PMID: PubMed DOI PMC

Nan Q., Qian D., Niu Y., He Y., Tong S., Niu Z., et al. . (2017). Plant actin-depolymerizing factors possess opposing biochemical properties arising from key amino acid changes throughout evolution. Plant Cell 29, 395–408. doi: 10.1105/tpc.16.00690, PMID: PubMed DOI PMC

Nick P., Han M.-J., An G. (2009). Auxin stimulates its own transport by shaping actin filaments. Plant Physiol. 151, 155–167. doi: 10.1104/pp.109.140111, PMID: PubMed DOI PMC

Nishimura T., Yokota E., Wada T., Shimmen T., Okada K. (2003). An Arabidopsis ACT2 dominant-negative mutation, which disturbs F-actin polymerization, reveals its distinctive function in root development. Plant Cell Physiol. 44, 1131–1140. doi: 10.1093/pcp/pcg158, PMID: PubMed DOI

Ötvös K., Marconi M., Vega A., O’Brien J., Johnson A., Abualia R., et al. . (2021). Modulation of plant root growth by nitrogen source-defined regulation of polar auxin transport. EMBO J. 40:e106862. doi: 10.15252/embj.2020106862, PMID: PubMed DOI PMC

Oulehlová D., Kollárová E., Cifrová P., Pejchar P., Žàrský 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. doi: 10.1093/pcp/pcz102, PMID: PubMed DOI

Paez-Garcia A., Sparks J. A., de Bang L., Blancaflor E. B. (2018). “Plant actin cytoskeleton: new functions from old scaffold” in Cell Biology - History and Evolution. eds. Sahi V. P., Baluška F. (Cham: Springer International Publishing: ), 103–137.

Peremyslov V. V., Klocko A. L., Fowler J. E., Dolja V. V. (2012). Arabidopsis myosin XI-K localizes to the motile endomembrane vesicles associated with F-actin. Front. Plant Sci. 3:184. doi: 10.3389/fpls.2012.00184, PMID: PubMed DOI PMC

Peremyslov V. V., Prokhnevsky A. I., Dolja V. V. (2010). Class XI myosins are required for development, cell expansion, and F-actin organization in Arabidopsis. Plant Cell 22, 1883–1897. doi: 10.1105/tpc.110.076315, PMID: PubMed DOI PMC

Pospich S., Merino F., Raunser S. (2020). Structural effects and functional implications of phalloidin and jasplakinolide binding to actin filaments. Structure 28, 437–449.e5. doi: 10.1016/j.str.2020.01.014, PMID: PubMed DOI

Pozhvanov G. A., Suslov D. V., Medvedev S. S. (2013). Actin cytoskeleton rearrangements during the gravitropic response of Arabidopsis roots. Cell Tissue Biol. 7, 185–191. doi: 10.1134/S1990519X13020120, PMID: PubMed DOI

Rahman A., Bannigan A., Sulaman W., Pechter P., Blancaflor E. B., Baskin T. I. (2007). Auxin, actin and growth of the Arabidopsis thaliana primary root. Plant J. 50, 514–528. doi: 10.1111/j.1365-313X.2007.03068.x, PMID: PubMed DOI

Ramachandran S., Christensen H. E. M., Ishimaru Y., Dong C. H., Chao-Ming W., Cleary A. L., et al. . (2000). Profilin plays a role in cell elongation, cell shape maintenance, and flowering in Arabidopsis. Plant Physiol. 124, 1637–1647. doi: 10.1104/pp.124.4.1637, PMID: PubMed DOI PMC

Reboulet J. C., Kumar P., Kiss J. Z. (2010). DIS1 and DIS2 play a role in tropisms in Arabidopsis thaliana. Environ. Exp. Bot. 67, 474–478. doi: 10.1016/j.envexpbot.2009.07.002 DOI

Rodríguez-Serrano M., Pazmiño D. M., Sparkes I., Rochetti A., Hawes C., Romero-Puertas M. C., et al. . (2014). 2,4-dichlorophenoxyacetic acid promotes S-nitrosylation and oxidation of actin affecting cytoskeleton and peroxisomal dynamics. J. Exp. Bot. 65, 4783–4793. doi: 10.1093/jxb/eru237, PMID: 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. doi: 10.1093/jxb/ers351, PMID: PubMed DOI PMC

Rutten J. P., Tusscher K. T. (2019). In silico roots: room for growth. Trends Plant Sci. 24, 250–262. doi: 10.1016/j.tplants.2018.11.005, PMID: PubMed DOI

Ruzicka D. R., Kandasamy M. K., McKinney E. C., Burgos-Rivera B., Meagher R. B. (2007). The ancient subclasses of Arabidopsis actin depolymerizing factor genes exhibit novel and differential expression. Plant J. 52, 460–472. doi: 10.1111/j.1365-313X.2007.03257.x, PMID: PubMed DOI

Růzǐčka K., Šimášková M., Duclercq J., Petrášek J., Zažímalová E., Simon S., et al. . (2009). Cytokinin regulates root meristem activity via modulation of the polar auxin transport. Proc. Natl. Acad. Sci. U. S. A. 106, 4284–4289. doi: 10.1073/pnas.0900060106, PMID: PubMed DOI PMC

Ryan J. M., Nebenführ A. (2018). Update on myosin motors: molecular mechanisms and physiological functions. Plant Physiol. 176, 119–127. doi: 10.1104/pp.17.01429, PMID: PubMed DOI PMC

Sack F. D. (1997). Plastids and gravitropic sensing. Planta 203, S63–S68. doi: 10.1007/pl00008116 PubMed DOI

Sahi V. P., Cifrová P., Garciá-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. doi: 10.1093/aob/mcx178, PMID: PubMed DOI PMC

Šamaj J., Peters M., Volkmann D., Baluška F. (2000). Effects of myosin ATPase inhibitor 2,3-butanedione 2-monoxime on distributions of myosins, F-actin, microtubules, and cortical endoplasmic reticulum in maize root apices. Plant Cell Physiol. 41, 571–582. doi: 10.1093/pcp/41.5.571, PMID: PubMed DOI

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. doi: 10.1104/pp.113.215277, PMID: PubMed DOI PMC

Sassi M., Lu Y., Zhang Y., Wang J., Dhonukshe P., Blilou I., et al. . (2012). COP1 mediates the coordination of root and shoot growth by light through modulation of PIN1- and PIN2-dependent auxin transport in Arabidopsis. Development 139, 3402–3412. doi: 10.1242/dev.078212, PMID: PubMed DOI

Scheuring D., Löfke C., Krüger F., Kittelmann M., Eisa A., Hughes L., et al. . (2016). Actin-dependent vacuolar occupancy of the cell determines auxin-induced growth repression. Proc. Natl. Acad. Sci. U. S. A. 113, 452–457. doi: 10.1073/pnas.1517445113, PMID: PubMed DOI PMC

Silva-Navas J., Moreno-Risueno M. A., Manzano C., Pallero-Baena M., Navarro-Neila S., Téllez-Robledo B., et al. . (2015). D-root: a system for cultivating plants with the roots in darkness or under different light conditions. Plant J. 84, 244–255. doi: 10.1111/tpj.12998, PMID: PubMed DOI

Silva-Navas J., Moreno-Risueno M. A., Manzano C., Téllez-Robledo B., Navarro-Neila S., Carrasco V., et al. . (2016). Flavonols mediate root phototropism and growth through regulation of proliferation-to-differentiation transition. Plant Cell 28, 1372–1387. doi: 10.1105/tpc.15.00857, PMID: PubMed DOI PMC

Šlajcherová K., Fišerová J., Fischer L., Schwarzerová K., Yang M. (2012). Multiple actin isotypes in plants: diverse genes for diverse roles? Front. Plant Sci. 3:226. doi: 10.3389/fpls.2012.00226, PMID: 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. doi: 10.1083/jcb.200806185, PMID: PubMed DOI PMC

Su S. H., Gibbs N. M., Jancewicz A. L., Masson P. H. (2017). Molecular mechanisms of root gravitropism. Curr. Biol. 27, R964–R972. doi: 10.1016/j.cub.2017.07.015, PMID: PubMed DOI

Takahashi M., Umetsu K., Oono Y., Higaki T., Blancaflor E. B., Rahman A. (2017). Small acidic protein 1 and SCFTIR1 ubiquitin proteasome pathway act in concert to induce 2,4-dichlorophenoxyacetic acid-mediated alteration of actin in Arabidopsis roots. Plant J. 89, 940–956. doi: 10.1111/tpj.13433, PMID: PubMed DOI

Takatsuka H., Higaki T., Umeda M. (2018). Actin reorganization triggers rapid cell elongation in roots. Plant Physiol. 178, 1130–1141. doi: 10.1104/pp.18.00557, PMID: PubMed DOI PMC

Takatsuka H., Ito M. (2020). Cytoskeletal control of planar polarity in root hair development. Front. Plant Sci. 11:580935. doi: 10.3389/fpls.2020.580935, PMID: PubMed DOI PMC

Takatsuka H., Umeda M. (2014). Hormonal control of cell division and elongation along differentiation trajectories in roots. J. Exp. Bot. 65, 2633–2643. doi: 10.1093/jxb/ert485, PMID: PubMed DOI

Tolmie F., Poulet A., McKenna J., Sassmann S., Graumann K., Deeks M., et al. . (2017). The cell wall of Arabidopsis thaliana influences actin network dynamics. J. Exp. Bot. 68, 4517–4527. doi: 10.1093/jxb/erx269, PMID: PubMed DOI

Tominaga M., Kimura A., Yokota E., Haraguchi T., Shimmen T., Yamamoto K., et al. . (2013). Cytoplasmic streaming velocity as a plant size determinant. Dev. Cell 27, 345–352. doi: 10.1016/j.devcel.2013.10.005, PMID: PubMed DOI

van der Honing H. S., Kieft H., Emons A. M. C., Ketelaar T. (2012). Arabidopsis VILLIN2 and VILLIN3 are required for the generation of thick actin filament bundles and for directional organ growth. Plant Physiol. 158, 1426–1438. doi: 10.1104/pp.111.192385, PMID: PubMed DOI PMC

van Gelderen K., Kang C., Pierik R. (2018). Light signaling, root development, and plasticity. Plant Physiol. 176, 1049–1060. doi: 10.1104/pp.17.01079, PMID: PubMed DOI PMC

Vanstraelen M., Benková E. (2012). Hormonal interactions in the regulation of plant development. Annu. Rev. Cell Dev. Biol. 28, 463–487. doi: 10.1146/annurev-cellbio-101011-155741, PMID: PubMed DOI

Vaškebová L., Šamaj J., Ovecka M. (2018). Single-point ACT2 gene mutation in the Arabidopsis root hair mutant der1-3 affects overall actin organization, root growth and plant development. Ann. Bot. 122, 889–901. doi: 10.1093/aob/mcx180, PMID: PubMed DOI PMC

Verbelen J. P., De Cnodder T., Le J., Vissenberg K., Baluška F. (2006). The root apex of Arabidopsis thaliana consists of four distinct zones of growth activities: meristematic zone, transition zone, fast elongation zone and growth terminating zone. Plant Signal. Behav. 1, 296–304. doi: 10.4161/psb.1.6.3511, PMID: PubMed DOI PMC

Voigt B., Timmers A. C. J., 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, 595–608. doi: 10.1016/j.ejcb.2004.11.011, PMID: PubMed DOI

Volkmann D., Baluška F., Lichtscheidl I., Driss-Ecole D., Perbal G. (1999). Statoliths motions in gravity-perceiving plant cells: does actomyosin counteract gravity? FASEB J. 13, S143–S147. doi: 10.1096/fasebj.13.9001.s143, PMID: PubMed DOI

Wan Y., Jasik J., Wang L., Hao H., Volkmann D., Menzel D., et al. . (2012). The signal transducer NPH3 integrates the phototropin1 photosensor with PIN2-based polar auxin transport in Arabidopsis root phototropism. Plant Cell 24, 551–565. doi: 10.1105/tpc.111.094284, PMID: PubMed DOI PMC

Wang P., Hussey P. J. (2015). Interactions between plant endomembrane systems and the actin cytoskeleton. Front. Plant Sci. 6:422. doi: 10.3389/fpls.2015.00422, PMID: PubMed DOI PMC

Wang X., Mao T. (2019). Understanding the functions and mechanisms of plant cytoskeleton in response to environmental signals. Curr. Opin. Plant Biol. 52, 86–96. doi: 10.1016/j.pbi.2019.08.002, PMID: PubMed DOI

Wang Y.-S., Motes C. M., Mohamalawari D. R., Blancaflor E. B. (2004). Green fluorescent protein fusions to Arabidopsis fimbrin 1 for spatio-temporal imaging of F-actin dynamics in roots. Cell Motil. Cytoskeleton 59, 79–93. doi: 10.1002/cm.20024, PMID: PubMed DOI

White R. G., Sack F. D. (1990). Actin microfilaments in presumptive statocytes of root caps and coleoptiles. Am. J. Bot. 77, 17–26. doi: 10.1002/j.1537-2197.1990.tb13523.x, PMID: PubMed DOI

Wolverton C., Mullen J. L., Ishikawa H., Evans M. L. (2002). Root gravitropism in response to a signal originating outside of the cap. Planta 215, 153–157. doi: 10.1007/s00425-001-0726-9, PMID: PubMed DOI

Wolverton C., Paya A. M., Toska J. (2011). Root cap angle and gravitropic response rate are uncoupled in the Arabidopsis pgm-1 mutant. Physiol. Plant. 141, 373–382. doi: 10.1111/j.1399-3054.2010.01439.x, PMID: PubMed DOI

Wybouw B., De Rybel B. (2019). Cytokinin—a developing story. Trends Plant Sci. 24, 177–185. doi: 10.1016/j.tplants.2018.10.012, PMID: PubMed DOI

Xue X.-H. H., Guo C.-Q. Q., Du F., Lu Q.-L. L., Zhang C.-M. M., Ren H.-Y. Y. (2011). AtFH8 is involved in root development under effect of low-dose latrunculin B in dividing cells. Mol. Plant 4, 264–278. doi: 10.1093/mp/ssq085, PMID: PubMed DOI

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

Yang K., Wang L., Le J., Dong J. (2020). Cell polarity: regulators and mechanisms in plants. J. Integr. Plant Biol. 62, 132–147. doi: 10.1111/jipb.12904, PMID: PubMed DOI PMC

Zhang Z., Denans N., Liu Y., Zhulyn O., Rosenblatt H. D., Wernig M., et al. . (2021). Optogenetic manipulation of cellular communication using engineered myosin motors. Nat. Cell Biol. 23, 198–208. doi: 10.1038/S41556-020-00625-2, PMID: PubMed DOI PMC

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

Zhang H., Qu X., Bao C., Khurana P., Wang Q., Xie Y., et al. . (2010). Arabidopsis VILLIN5, an actin filament bundling and severing protein, is necessary for normal pollen tube growth. Plant Cell 22, 2749–2767. doi: 10.1105/tpc.110.076257, PMID: PubMed DOI PMC

Zhang K. X., Xu H. H., Yuan T. T., Zhang L., Lu Y. T. (2013b). Blue-light-induced PIN3 polarization for root negative phototropic response in Arabidopsis. Plant J. 76, 308–321. doi: 10.1111/tpj.12298, PMID: PubMed DOI

Zhao S., Zhang Q., Liu M., Zhou H., Ma C., Wang P. (2021). Regulation of plant responses to salt stress. Int. J. Mol. Sci. 22:4609. doi: 10.3390/ijms22094609, PMID: PubMed DOI PMC

Zheng Z., Zou J., Li H., Xue S., Wang Y., Le J. (2015). Microrheological insights into the dynamics of amyloplasts in root gravity-sensing cells. Mol. Plant 8, 660–663. doi: 10.1016/j.molp.2014.12.021, PMID: PubMed DOI

Zhu J., Bailly A., Zwiewka M., Sovero V., Di Donato M., Ge P., et al. . (2016). TWISTED DWARF1 mediates the action of auxin transport inhibitors on actin cytoskeleton dynamics. Plant Cell 28, 930–948. doi: 10.1105/tpc.15.00726, PMID: PubMed DOI PMC

Zhu J., Geisler M. (2015). Keeping it all together: auxin-actin crosstalk in plant development. J. Exp. Bot. 66, 4983–4998. doi: 10.1093/jxb/erv308, PMID: PubMed DOI

Zimmermann U., Hüsken D., Schulze E. D. (1980). Direct turgor pressure measurements in individual leaf cells of Tradescantia virginiana. Planta 149, 445–453. doi: 10.1007/BF00385746, PMID: PubMed DOI

Zou M., Ren H., Li J. (2019). An auxin transport inhibitor targets villin-mediated actin dynamics to regulate polar auxin transport. Plant Physiol. 181, 161–178. doi: 10.1104/pp.19.00064, PMID: PubMed DOI PMC

Zou J. J., Zheng Z. Y., Xue S., Li H. H., Wang Y. R., Le J. (2016). The role of Arabidopsis actin-related protein 3 in amyloplast sedimentation and polar auxin transport in root gravitropism. J. Exp. Bot. 67, 5325–5337. doi: 10.1093/jxb/erw294, PMID: PubMed DOI PMC

Recent insights into metabolic and signalling events of directional root growth regulation and its implications for sustainable crop production systems