Skip to main content

The Actomyosin System in Plant Cell Division: Lessons Learned from Microscopy and Pharmacology

  • Chapter
  • First Online:

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 24))

Abstract

Actin and myosin (i.e., the actomyosin system) play pivotal roles in plants, including organelle movement, cytoplasmic streaming, cell expansion, responses to microbes, cell signaling, and cell division. Among the plant biological processes attributed to actin and myosin function, understanding their precise role in cell division has been one of the more challenging problems to address. The difficulties in linking actomyosin function to cell division come in large part from inconsistent actin labeling in the cell division apparatus to the mild cell division phenotypes of actomyosin mutants. While the latter can be explained by functional redundancy, the presence of actin and myosin in the mitotic spindle has been somewhat controversial. Nonetheless, genetically encoded live actin and myosin probes have confirmed some classic microscopy results reported decades ago while also uncovering unique structures associated with the plant cell division machinery. In this chapter, we discuss how early microscopic work and recent live cell imaging data are beginning to provide a more unified view on how the actomyosin system facilitates cell division in plants.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arima K, Tamaoki D, Mineyuki Y, Yasuhara H, Nakai T, Shimmen T, Yoshihisa T, Sonobe S (2018) Displacement of the mitotic apparatuses by centrifugation reveals cortical actin organization during cytokinesis in cultured tobacco BY-2 cells. J Plant Res 131(5):803–815

    Article  CAS  PubMed  Google Scholar 

  • Avisar D, Abu-Abied M, Belausov E, Sadot E, Hawes C, Sparkes IA (2009) A comparative study of the involvement of 17 Arabidopsis myosin family members on the motility of Golgi and other organelles. Plant Physiol 150:700–709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baskin TI, Miller DD, Vos JW, Wilson JE, Hepler PK (1996) Cryofixing single cells and multicellular specimens enhances structure and immunocytochemistry for light microscopy. J Microsc 182:149–161

    Article  CAS  PubMed  Google Scholar 

  • Cleary AL, Gunning BES, Wasteneys GO, Hepler PK (1992) Microtubule and F-actin dynamics at the division site in living Tradescantia stamen hair cells. J Cell Sci 103:977–988

    CAS  Google Scholar 

  • Ding B, Turgeon R, Parthasarathy MV (1991) Microfilaments in the preprophase band of freeze substituted tobacco root cells. Protoplasma 165:209–211

    Article  Google Scholar 

  • Facette MR, Park Y, Sutimantanapi D, Luo A, Cartwright HN, Yang B, Bennett EJ, Sylvester AW, Smith LG (2015) The SCAR/WAVE complex polarizes PAN receptors and promotes division asymmetry in maize. Nat Plants 1:14024

    Article  CAS  PubMed  Google Scholar 

  • Haraguchi T, Tominaga M, Matsumoto R, Sato K, Nakano A, Yamamoto K, Ito K (2014) Molecular characterization and subcellular localization of Arabidopsis class VIII myosin, ATM1. J Biol Chem 289:12343–12355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasezawa S, Sano T, Nagata T (1994) Oblique cell plate formation in tobacco BY-2 cells originates in double preprophase bands. J Plant Res 107:355–359

    Article  Google Scholar 

  • Hepler PK, Valster A, Molchan T, Vos JW (2002) Roles for kinesin and myosin during cytokinesis. Philos Trans R Soc Lond Ser B Biol Sci 357:761–766

    Article  CAS  Google Scholar 

  • Higaki T, Kutsuna N, Sano T, Hasezawa S (2008) Quantitative analysis of changes in actin microfilament contribution to cell plate development in plant cytokinesis. BMC Plant Biol 8:80

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hoshino H, Yoneda A, Kumagai F, Hasezawa S (2003) Roles of actin-depleted zone and preprophase band in determining the division site of higher-plant cells, a tobacco BY-2 cell line expressing GFP-tubulin. Protoplasma 222:157–165

    Article  CAS  PubMed  Google Scholar 

  • Huxley HE (1963) Electron microscope studies on the structure of natural and synthetic protein filaments from striated muscle. J Mol Biol 7:281–IN230

    Article  CAS  PubMed  Google Scholar 

  • Ingouff M, Fitz Gerald JN, Guerin C, Robert H, Sorensen MB, Van Damme D, Geelen D, Blanchoin L, Berger F (2005) Plant formin AtFH5 is an evolutionarily conserved actin nucleator involved in cytokinesis. Nat Cell Biol 7:374–380

    Article  CAS  PubMed  Google Scholar 

  • Kakimoto T, Shibaoka H (1988) Cytoskeletal ultrastructure of phragmoplast-nuclei complexes isolated from cultured tobacco cells. In: Tazawa M (ed) Cell dynamics protoplasma (Supplementum 2), vol 2. Springer, Vienna, pp 95–103

    Google Scholar 

  • Katsuta J, Hashiguchi Y, Shibaoka H (1990) The role of the cytoskeleton in positioning of the nucleus in premitotic tobacco BY-2 cells. J Cell Sci 95:413–422

    Google Scholar 

  • Kennard JL, Cleary AL (1997) Pre-mitotic nuclear migration in subsidiary mother cells of Tradescantia occurs in G1 of the cell cycle and requires F-actin. Cell Motil Cytoskeleton 36:55–67

    Article  CAS  PubMed  Google Scholar 

  • Ketelaar T, Faivre-Moskalenko C, Esseling JJ, de Ruijter NC, Grierson CS, Dogterom M, Emons AM (2002) Positioning of nuclei in Arabidopsis root hairs: an actin-regulated process of tip growth. Plant Cell 14:2941–2955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ketelaar T, Allwood EG, Anthony R, Voigt B, Menzel D, Hussey PJ (2004) The actin-interacting protein AIP1 is essential for actin organization and plant development. Curr Biol 14:145–149

    Article  CAS  PubMed  Google Scholar 

  • Kijima ST, Staiger CJ, Katoh K, Nagasaki A, Ito K, Uyeda TQP (2018) Arabidopsis vegetative actin isoforms, AtACT2 and AtACT7, generate distinct filament arrays in living plant cells. Sci Rep 8:4381–4381

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kojo KH, Higaki T, Kutsuna N, Yoshida Y, Yasuhara H, Hasezawa S (2013) Roles of cortical actin microfilament patterning in division plane orientation in plants. Plant Cell Physiol 54:1491–1503

    Article  CAS  PubMed  Google Scholar 

  • Komis G, Novak D, Ovecka M, Samajova O, Samaj J (2018) Advances in imaging plant cell dynamics. Plant Physiol 176:80–93

    Article  CAS  PubMed  Google Scholar 

  • Kost B, Spielhofer P, Chua NH (1998) A GFP-mouse talin fusion protein labels plant actin filaments in vivo and visualizes the actin cytoskeleton in growing pollen tubes. Plant J 16:393–401

    Article  CAS  PubMed  Google Scholar 

  • Liu B, Palevitz BA (1992) Organization of cortical microfilaments in dividing root cells. Cell Motil Cytoskeleton 23:252–264

    Article  Google Scholar 

  • Liu AX, Zhang SB, Xu XJ, Ren DT, Liu GQ (2004) Soluble expression and characterization of a GFP-fused pea actin isoform (PEAc1). Cell Res 14:407–414

    Article  CAS  PubMed  Google Scholar 

  • Lloyd CW, Traas JA (1988) The role of F-actin in determining the division plane of carrot suspension cells. Drug studies. Development 102:211–221

    CAS  Google Scholar 

  • Lo YS, Cheng N, Hsiao LJ, Annamalai A, Jauh GY, Wen TN, Dai H, Chiang KS (2011) Actin in mung bean mitochondria and implications for its function. Plant Cell 23:3727–3744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCurdy DW, Gunning BES (1990) Reorganization of cortical actin microfilaments and microtubules at preprophase and mitosis in wheat root-tip cells: a double label immunofluorescence study. Cell Motil Cytoskeleton 15:76–87

    Article  Google Scholar 

  • Mineyuki Y (1999) The preprophase band of microtubules: its function as a cytokinetic apparatus in higher plants. Int Rev Cytol 187:1–49

    Article  Google Scholar 

  • Mineyuki Y, Palevitz BA (1990) Relationship between preprophase band organization, F-actin and the division site in Allium; fluorescence and morphometric studies on cytochalasin-treated cells. J Cell Sci 97:283–295

    CAS  Google Scholar 

  • Molchan TM, Valster AH, Hepler PK (2002) Actomyosin promotes cell plate alignment and late lateral expansion in Tradescantia stamen hair cells. Planta 214:683–693

    Article  CAS  PubMed  Google Scholar 

  • Muller S, Jurgens G (2016) Plant cytokinesis-no ring, no constriction but centrifugal construction of the partitioning membrane. Semin Cell Dev Biol 53:10–18

    Article  PubMed  CAS  Google Scholar 

  • Nebenfuhr A, Frohlick JA, Staehelin LA (2000) Redistribution of Golgi stacks and other organelles during mitosis and cytokinesis in plant cells. Plant Physiol 124:135–151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palevitz BA (1980) Comparative effects of phalloidin and cytochalasin B on motility and morphogenesis in Allium. Can J Bot 58:773–785

    Article  CAS  Google Scholar 

  • Palevitz BA (1987) Actin in the preprophase band of Allium cepa. J Cell Biol 104:1515–1519

    Article  CAS  PubMed  Google Scholar 

  • Peremyslov VV, Prokhnevsky AI, Dolja VV (2010) Class XI myosins are required for development, cell expansion, and F-actin organization in Arabidopsis. Plant Cell 22:1881–1897

    Article  CAS  Google Scholar 

  • Rasmussen CG, Bellinger M (2018) An overview of plant division-plane orientation. New Phytol 219:505–512

    Article  PubMed  Google Scholar 

  • Reichelt S, Knight AE, Hodge TP, Baluška F, Samaj J, Volkmann D, Kendrick-Jones J (1999) Characterization of the unconventional myosin VIII in plant cells and its localization at the post-cytokinetic cell wall. Plant J 19:555–567

    Article  CAS  PubMed  Google Scholar 

  • Riedl J, Crevenna AH, Kessenbrock K, Yu JH, Neukirchen D, Bista M, Bradke F, Jenne D, Holak TA, Werb Z, Sixt M, Wedlich-Soldner R (2008) Lifeact: a versatile marker to visualize F-actin. Nat Methods 5:605–607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rybak K, Steiner A, Synek L, Klaeger S, Kulich I, Facher E, Wanner G, Kuster B, Zarsky V, Persson S, Assaad FF (2014) Plant cytokinesis is orchestrated by the sequential action of the TRAPPII and exocyst tethering complexes. Dev Cell 29:607–620

    Article  CAS  PubMed  Google Scholar 

  • Sano T, Higaki T, Oda Y, Hayashi T, Hasezawa S (2005) Appearance of actin microfilament ‘twin peaks’ in mitosis and their function in cell plate formation, as visualized in tobacco BY-2 cells expressing GFP-fimbrin. Plant J 44:595–605

    Article  CAS  PubMed  Google Scholar 

  • Sano T, Hayashi T, Kutsuna N, Nagata T, Hasezawa S (2012) Role of actin microfilaments in phragmoplast guidance to the cortical division zone. Curr Top Plant Biol 13:87–94

    CAS  Google Scholar 

  • Schmit AC, Lambert AM (1990) Microinjected fluorescent phalloidin in vivo reveals the F-actin dynamics and assembly in higher plant mitotic cells. Plant Cell 2:129–138

    CAS  PubMed  PubMed Central  Google Scholar 

  • Seagull RW, Falconer MM, Weerdenburg CA (1987) Microfilaments: dynamic arrays in higher plant cells. J Cell Biol 104:995–1004

    Article  CAS  PubMed  Google Scholar 

  • Shao W, Dong J (2016) Polarity in plant asymmetric cell division: division orientation and cell fate differentiation. Dev Biol 419:121–131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sinnott EW, Bloch R (1940) Cytoplasmic behavior during division of vacuolate plant cells. Proc Natl Acad Sci USA 26:223–227

    Article  CAS  PubMed  Google Scholar 

  • Skop AR, Liu H, Yates J 3rd, Meyer BJ, Heald R (2004) Dissection of the mammalian midbody proteome reveals conserved cytokinesis mechanisms. Science 305:61–66

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smertenko A, Assaad F, Baluska F, Bezanilla M, Buschmann H, Drakakaki G, Hauser MT, Janson M, Mineyuki Y, Moore I, Muller S, Murata T, Otegui MS, Panteris E, Rasmussen C, Schmit AC, Samaj J, Samuels L, Staehelin LA, Van Damme D, Wasteneys G, Zarsky V (2017) Plant cytokinesis: terminology for structures and processes. Trends Cell Biol 27:885–894

    Article  CAS  PubMed  Google Scholar 

  • Staehelin LA, Hepler PK (1996) Cytokinesis in higher plants. Cell 84:821–824

    Article  CAS  PubMed  Google Scholar 

  • Sun H, Furt F, Vidali L (2018) Myosin XI localizes at the mitotic spindle and along the cell plate during plant cell division in Physcomitrella patens. Biochem Biophys Res Commun 506(2):409–421

    Article  CAS  PubMed  Google Scholar 

  • Takeuchi M, Karahara I, Kajimura N, Takaoka A, Murata K, Misaki K, Yonemura S, Staehelin LA, Mineyuki Y (2016) Single microfilaments mediate the early steps of microtubule bundling during preprophase band formation in onion cotyledon epidermal cells. Mol Biol Cell 27:1809–1820

    Article  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Iwabuchi K, Fukao Y, Kondo M, Okamoto K, Ueda H, Nishimura M, Hara-Nishimura I (2013) Myosin XI-i links the nuclear membrane to the cytoskeleton to control nuclear movement and shape in Arabidopsis. Curr Biol 23:1776–1781

    Article  CAS  PubMed  Google Scholar 

  • Thomas C, Hoffmann C, Dieterle M, Van Troys M, Ampe C, Steinmetz A (2006) Tobacco WLIM1 is a novel F-actin binding protein involved in actin cytoskeleton remodeling. Plant Cell 18:2194–2206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Traas JA, Doonan JH, Rawlins DJ, Shaw PJ, Watts J, Lloyd CW (1987) An actin network is present in the cytoplasm throughout the cell cycle of carrot cells and associates with the dividing nucleus. J Cell Biol 105:387–395

    Article  CAS  PubMed  Google Scholar 

  • Valster AH, Hepler PK (1997) Caffeine inhibition of cytokinesis: effect on the phragmoplast cytoskeleton in living Tradescantia stamen hair cells. Protoplasma 196:155–166

    Article  CAS  Google Scholar 

  • Valster AH, Pierson ES, Valenta R, Hepler PK, Emons A (1997) Probing the plant actin cytoskeleton during cytokinesis and interphase by profilin microinjection. Plant Cell 9:1815–1824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Damme D, Bouget FY, Van Poucke K, Inze D, Geelen D (2004) Molecular dissection of plant cytokinesis and phragmoplast structure: a survey of GFP-tagged proteins. Plant J 40:386–398

    Article  PubMed  CAS  Google Scholar 

  • Van Damme D, Gadeyne A, Vanstraelen M, Inze D, Van Montagu MC, De Jaeger G, Russinova E, Geelen D (2011) Adaptin-like protein TPLATE and clathrin recruitment during plant somatic cytokinesis occurs via two distinct pathways. Proc Natl Acad Sci USA 108:615–620

    Article  PubMed  CAS  Google Scholar 

  • van Gisbergen PA, Li M, Wu SZ, 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • van Oostende-Triplet C, Guillet D, Triplet T, Pandzic E, Wiseman PW, Geitmann A (2017) Vesicle dynamics during plant cell cytokinesis reveals distinct developmental phases. Plant Physiol 174:1544–1558

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vanstraelen M, Van Damme D, De Rycke R, Mylle E, Inze D, Geelen D (2006) Cell cycle-dependent targeting of a kinesin at the plasma membrane demarcates the division site in plant cells. Curr Biol 16:308–314

    Article  CAS  PubMed  Google Scholar 

  • Vaskebova L, Samaj 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

    CAS  PubMed  Google Scholar 

  • Voigt B, Timmers AC, Samaj J, Muller 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

    Article  CAS  PubMed  Google Scholar 

  • Wang YS, Yoo CM, Blancaflor EB (2008) Improved imaging of actin filaments in transgenic Arabidopsis plants expressing a green fluorescent protein fusion to the C- and N-termini of the fimbrin actin-binding domain 2. New Phytol 177:525–536

    CAS  PubMed  Google Scholar 

  • Wasteneys GO (2002) Microtubule organization in the green kingdom: chaos or self-order? J Cell Sci 115:1345–1354

    CAS  PubMed  Google Scholar 

  • Wu SZ, Bezanilla M (2014) Myosin VIII associates with microtubule ends and together with actin plays a role in guiding plant cell division. elife 3:e03498

    Article  PubMed Central  CAS  Google Scholar 

  • Wu SZ, Yamada M, Mallett DR, Bezanilla M (2018) Cytoskeletal discoveries in the plant lineage using the moss Physcomitrella patens. Biophys Rev 10:1683–1693

    Article  PubMed  PubMed Central  Google Scholar 

  • Yokota E, Ueda S, Tamura K, Orii H, Uchi S, Sonobe S, Hara-Nishimura I, Shimmen T (2009) An isoform of myosin XI is responsible for the translocation of endoplasmic reticulum in tobacco cultured BY-2 cells. J Exp Bot 60:197–212

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Zhang W, Baluska F, Menzel D, Ren H (2009) Dynamics and roles of phragmoplast microfilaments in cell plate formation during cytokinesis of tobacco BY-2 cells. Chin Sci Bull 54:2051–2061

    Article  CAS  Google Scholar 

Download references

Acknowledgment

Research on the plant cytoskeleton in the authors’ laboratories is supported by the National Aeronautics and Space Administration (NASA grant numbers 80NSSC18K1462 and 80NSSC19KO129) to EBB and BSF Binational Science Foundation (grant number 2013084) to ES.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Einat Sadot .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Sadot, E., Blancaflor, E.B. (2019). The Actomyosin System in Plant Cell Division: Lessons Learned from Microscopy and Pharmacology. In: Sahi, V., Baluška, F. (eds) The Cytoskeleton. Plant Cell Monographs, vol 24. Springer, Cham. https://doi.org/10.1007/978-3-030-33528-1_6

Download citation

Publish with us

Policies and ethics