Skip to main content
Log in

Tissue-specific subcellular immunolocalization of a myosin-like protein in maize root apices

  • Published:
Protoplasma Aims and scope Submit manuscript

Summary

Using a heterologous myosin antibody raised against the whole molecule of bovine muscle myosin, we have identified a myosin-like protein in maize. Immunoblots of subcellular fractions isolated from roots identified one distinct band at about 210 kDa in the microsomal protein fraction and one band at about 180 kDa in the soluble protein fraction. Indirect immunofluorescence was performed using maize root apex sections to reveal endocellular distributions of the myosin-like protein. Both diffuse and particulate labelling patterns were observed throughout the cytoplasm of all root cells. In mitotic cells, myosin-like protein was excluded from spindle regions. Amyloplast surfaces were labelled prominently in cells of the root cap statenchyma and in all root cortex cells. On the other hand, myosin-like protein was prominently enriched at cellular peripheries in cells of the pericycle and outer stele in the form of continuous peripheral labelling. From all root apex tissues, phloem elements showed the most abundant presence of myosinlike protein.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

AFs:

actin filaments

MTs:

microtubules

References

  • Asada T, Collings D (1997) Molecular motors in higher plants. Trends Plant Sci 2: 29–37

    Google Scholar 

  • Bähler M (1996) Myosins on the move to signal transduction. Curr Opin Cell Biol 8: 18–22

    PubMed  Google Scholar 

  • Baluška F, Hasenstein KH (1997) Root cytoskeleton: its role in perception of and response to gravity. Planta 203: S69-S78

    PubMed  Google Scholar 

  • —, Parker JS, Barlow PW (1992) Specific patterns of cortical and endoplasmic microtubules associated with cell growth and tissue differentiation in roots of maize (Zea mays L.). J Cell Sci 103: 191–200

    Google Scholar 

  • —, Vitha S, Barlow PW, Volkmann D (1997a) Re-arrangements of F-actin arrays in growing cells of intact maize root apex tissue: a major developmental switch occurs in the postmitotic transition region. Eur J Cell Biol 72: 113–121

    PubMed  Google Scholar 

  • —, Kreibaum A, Vitha S, Parker JS, Barlow PW, Sievers A (1997b) Central root cap cells are depleted of endoplasmic microtubules and actin microfilament bundles: implications for their role as gravity-sensing statocytes. Protoplasma 196: 212–223

    PubMed  Google Scholar 

  • —, Lichtscheidl IK, Volkmann D, Barlow PW (1998) The plant cell body: a cytoskeletal tool for cellular development and morphogenesis. Protoplasma 202: 1–10

    Google Scholar 

  • —, Samaj J, Napier R, Volkmann D (1999) Maize calreticulin localizes preferentially to plasmodesmata. Plant J 19: 481–488

    PubMed  Google Scholar 

  • - Volkmann D, Barlow PW (2000a) Actin-based domains of “cell periphery complex” and their associations with polarized “cell bodies” in higher plants. Plant Biol 2 (in press)

  • —, Barlow PW, Volkmann D (2000b) Actin and myosin VIII in developing root cells. In: Staiger CJ, Baluška F, Volkmann D, Barlow PW (eds) Actin: a dynamic framework for multiple plant cell functions. Kluwer, Dordrecht, pp 457–476

    Google Scholar 

  • Barlow PW, Parker JS (1997) Microtubular cytoskeleton and root morphogenesis. Plant Soil 187: 23–36

    Google Scholar 

  • Berrios M, Fisher PA (1986) A myosin heavy chain-like polypeptide is associated with the nuclear envelope in higher eukaryotic cells. J Cell Biol 103: 711–724

    PubMed  Google Scholar 

  • — —, Matz EC (1991) Localization of a myosin heavy chain-like polypeptide toDrosophila nuclear pore complexes. Proc Natl Acad Sci USA 88: 219–223

    PubMed  Google Scholar 

  • Blackman LM, Overall RL (1998) Immunolocalisation of the cytoskeleton to plasmodesmata ofChara corallina. Plant J 14: 733–741

    Google Scholar 

  • Boevink P, Oparka K, Santa Cruz S, Martin B, Betteridge A, Hawes C (1998) Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J 15: 441–447

    PubMed  Google Scholar 

  • Braun M (1996) Immunolocalization of myosin in rhizoids ofChara globularis Thuill. Protoplasma 191: 1–8

    Google Scholar 

  • Brown SS (1997) Myosins in yeast. Curr Opin Cell Biol 9: 44–48

    PubMed  Google Scholar 

  • Cleary AL, Mathesius U (1996) Rearrangements of F-actin during stomatogenesis visualized by confocal microscopy in fixed and permeabilisedTradescantia leaf cells. Bot Acta 109: 15–24

    Google Scholar 

  • Cole NB, Lippincott-Schwartz J (1995) Organization of organelles and membrane traffic by microtubules. Curr Opin Cell Biol 7: 55–65

    Google Scholar 

  • Cope MJTV, Whisstock J, Rayment I, Kendrick-Jones J (1996) Conservation within the myosin motor domain: implications for structure and function. Structure 4: 969–987

    PubMed  Google Scholar 

  • Ding B, Kwon M-O, Warnberg L (1996) Evidence that actin filaments are involved in controlling the permeability of plasmodesmata in tobacco mesophyll. Plant J 10: 157–164

    Google Scholar 

  • Frankel S, Sigel EA, Craig C, Elgin SCR, Mooseker MS, Artavanis-Tsakonas S (1997) An actin-related protein inDrosophila colocalizes with heterochromatin protein 1 in pericentric heterochromatin. J Cell Sci 110: 1999–2012

    PubMed  Google Scholar 

  • Giddings TH, Staehelin LA (1988) Spatial relationship between microtubules and plasma membrane rosettes during the deposition of primary wall microfibrils inClosterium sp. Planta 173: 22–30

    Google Scholar 

  • Gonsior SM, Platz S, Buchmeier S, Scheer U, Jockusch BM (1999) Conformational difference between nuclear and cytoplasmic actin as detected by a monoclonal antibody. J Cell Sci 112: 797–809

    PubMed  Google Scholar 

  • Grolig F, Williamson RE, Parke J, Miller C, Anderton BH (1988) Myosin and Ca2+-sensitive streaming in the algaChara: detection of two polypeptides reacting with a monoclonal anti-myosin and their localization in the streaming endoplasm. Eur J Cell Biol 47: 22–31

    Google Scholar 

  • —, Schröder J, Sawitzky H, Lange U (1996) Partial characterization of putative 110 kDa myosin from the green algaChara corallina by in vitro binding of fluorescent F-actin. Cell Biol Int 20: 365–373

    PubMed  Google Scholar 

  • Heidemann SR, Kaech S, Buxbaum RE, Malus A (1999) Direct observations of the mechanical behaviors of the cytoskeleton in living fibroblasts. J Cell Biol 145: 109–122

    PubMed  Google Scholar 

  • Herrmann C, Wray J, Travers F, Barman T (1992) Effect of 2,3-butanedione monoxime on myosin and myofibrillar ATPases: an example of an uncompetitive inhibitor. Biochemistry 31: 12227–12232

    PubMed  Google Scholar 

  • Heslop-Harrison J, Heslop-Harrison Y (1989a) Actomyosin and movement in the angiosperm pollen tube: an interpretation of some recent results. Sex Plant Reprod 2: 199–207

    Google Scholar 

  • — — (1989b) Myosin associated with the surfaces of organelles, vegetative nuclei and generative cells in angiosperm pollen grains and tubes. J Cell Sci 94: 319–325

    Google Scholar 

  • Holzbaur ELF, Vallee RB (1994) DYNEIN: molecular structure and cellular function. Annu Rev Cell Biol 10: 339–372

    PubMed  Google Scholar 

  • Ikonen E, de Almeid JB, Fath KR, Burgess DR, Ashman K, Simons K, Stow JL (1997) Myosin II is associated with Golgi membranes: identification of p200 as nonmuscle myosin II on Golgi-derived vesicles. J Cell Sci 110: 2155–2164

    PubMed  Google Scholar 

  • Kinkema M, Wang H, Schiefelbein J (1994) Molecular analysis of myosin gene family inAmbidopsis thaliana. Plant Mol Biol 26: 1139–1153

    PubMed  Google Scholar 

  • Knight A, Kendrick-Jones J (1993) A myosin-like protein from a higher plant. J Mol Biol 231: 148–154

    PubMed  Google Scholar 

  • Kuroda K (1990) Cytoplasmic streaming in plant cells. Int Rev Cytol 121: 267–307

    Google Scholar 

  • —, Kamiya N (1975) Active movement of Nitella chloroplasts in vitro. Proc Jpn Acad 42: 507–511

    Google Scholar 

  • La Claire JW II (1991) Immunolocalization of myosin in intact and wounded cells of green algaErnodesmis erticillata (Küntzing) Borgesen. Planta 184: 209–217

    Google Scholar 

  • Lichtscheidl IK, Lancelle SA, Hepler PK (1990) Actin-endoplasmic reticulum complexes inDrosera: their structural relationship with the plasmalemma, nucleus, and organelles in cells prepared by high pressure freezing. Protoplasma 155: 116–126

    Google Scholar 

  • Liebe S, Menzel D (1995) Actomyosin-based motility of endoplasmic reticulum and chloroplasts in Vallisneria mesophyll cells. Biol Cell 85: 207–222

    PubMed  Google Scholar 

  • Maupin P, Phillips CL, Adalstein RS, Pollard TD (1994) Differential localization of myosin-II isozymes in human cultured cells and blood cells. J Cell Sci 107: 3077–3090

    PubMed  Google Scholar 

  • May KM, Watts FZ, Jones N, Hyams JS (1997) Type II myosin involved in cytokinesis in the fission yeast,Schizosaccharomyces pombe. Cell Motil Cytoskeleton 38: 385–396

    PubMed  Google Scholar 

  • Menzel D, Elsner-Menzel C (1989) Actin-based chloroplast rearrangements in the cortex of the giant coenocytic green algaCaulerpa. Protoplasma 150: 1–8

    Google Scholar 

  • Mermall V, Post PL, Mooseker MS (1998) Unconventional myosins in cell movement, membrane traffic, and signal transduction. Science 279: 527–533

    PubMed  Google Scholar 

  • Milankov K, De Boni U (1993) Cytochemical localization of actin and myosin aggregates within interphase nuclei in situ. Exp Cell Res 209: 189–199

    PubMed  Google Scholar 

  • Miller DD, Scordilis SP, Hepler PK (1995) Identification and localization of three classes of myosins in pollen tubes ofLilium longiflorum andNicotiana alata. J Cell Sci 108: 2549–2653

    PubMed  Google Scholar 

  • Mineyuki Y, Gunning BES (1988) Streak time-lapse video microscopy: analysis of protoplasmic motility and cell division inTradescantia stamen hair cells. J Microsc 150: 41–55

    Google Scholar 

  • —, Takagi M, Furuya M (1984) Changes in organelle movement in the nuclear region during the cell cycle of Adiantum protonema. Plant Cell Physiol 25: 297–308

    Google Scholar 

  • Moepps B, Conrad S, Schraudolf H (1993) PCR-dependent amplification and sequence characterization of partial cDNAs encoding myosin-like proteins inAnemia phyllitidis (L.) Sw. andArabidopsis thaliana (L.). Plant Mol Biol 21: 1077–1083

    PubMed  Google Scholar 

  • Moore JD, Endow SA (1996) Kinesin proteins: a phylum of motors for microtubule based motility. BioEssays 18: 207–219

    PubMed  Google Scholar 

  • Mooseker MS, Cheney RE (1995) Unconventional myosins. Annu Rev Cell Dev Biol 11: 633–675

    PubMed  Google Scholar 

  • Nebenführ A, Gallagher LA, Dunahay TG, Frohlick JA, Mazurkiewicz AM, Meehl JB, Staehelin LA (1999) Stop-and-go movements of plant golgi stacks are mediated by the acto-myosin system. Plant Physiol 121: 1127–1141

    PubMed  Google Scholar 

  • Nowak G, Pestic-Dragovich L, Hozák P, Philimonenko A, Simerly C, Schatten G, de Lanerolle P (1997) Evidence for the presence of myosin I in the nucleus. J Biol Chem 272: 17176–17181

    PubMed  Google Scholar 

  • Overall RL, Blackman LM (1996) A model of the macromolecular structure of plasmodesmata. Trends Plant Sci 9: 307–311

    Google Scholar 

  • Parke J, Miller C, Anderton BH (1986) Higher plant myosin heavychain identified using a monoclonal antibody. Eur J Cell Biol 41: 9–13

    Google Scholar 

  • Plazinski J, Elliott J, Hurley UA, Burch J, Arioli T, Williamson RE (1997) Myosins from angiosperms, ferns, and algae: amplification of gene fragments with versatile PRC primers and detection of protein products with a monoclonal antibody to a conserved head epitope. Protoplasma 196: 78–86

    Google Scholar 

  • Qiao L, Grolig F, Jablonsky PP, Williamson RE (1989) Myosin heavy chains: detection by immunoblotting in higher plants and localization by immunofluorescence in the algaChara. Cell Biol Int Rep 13: 107–117

    Google Scholar 

  • —, Jablonsky PP, Elliott J, Williamson RE (1994) A 170 kDa polypeptide from mung bean shares multiple epitopes with rabbit skeletal myosin and binds ADP-agarose. Cell Biol Int Rep 18: 1035–1047

    Google Scholar 

  • Quader H, Hofmann A, Schnepf E (1987) Shape and movement of the endoplasmic reticulum in onion bulb epidermis cells: possible involvement of actin. Eur J Cell Biol 44: 17–26

    Google Scholar 

  • Radford JE, White RG (1998) Localization of a myosin-like protein to plasmodesmata. Plant J 14: 743–750

    PubMed  Google Scholar 

  • Reichelt S, Kendrick-Jones J (2000) Myosins. In: Staiger CJ, Baluška F, Volkmann D, Barlow PW (eds) Actin: a dynamic framework for multiple plant cell functions. Kluwer, Dordrecht, pp 29–44

    Google Scholar 

  • —, Knight AE, Hodge TP, Baluška F, Šamaj J, Volkmann D, Kendrick-Jones J (1999) Characterization of the unconventional myosin VIII in plant cells and its localization at the postcytokinetic cell wall. Plant J 19: 555–569

    PubMed  Google Scholar 

  • Rimm DL, Pollard TD (1989) Purification and characterization of an Acanthamoeba nuclear actin-binding protein. J Cell Biol 109: 585–591

    PubMed  Google Scholar 

  • Sack FD (1997) Plastids and gravitropic sensing. Planta 203: S63-S68

    PubMed  Google Scholar 

  • —, Suyemoto M, Leopold AC (1986) Amyloplast sedimentation and organelle saltation in living corn columella cells. Am J Bot 73: 1692–1698

    PubMed  Google Scholar 

  • 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 (in press)

  • Satiat-Jeunemaitre B, Steele C, Hawes C (1996) Golgi-membrane dynamics are cytoskeleton dependent: a study on Golgi stack movement induced by brefeldin A. Protoplasma 191: 21–33

    Google Scholar 

  • Sato Y, Kadota A, Wada M (1999) Mechanically induced avoidance response of chloroplasts in fern protonemal cells. Plant Physiol 121: 37–44

    PubMed  Google Scholar 

  • Sauman I, Berry SJ (1994) An actin infrastructure is associated with eukaryotic chromosomes: structural and functional significance. Eur J Cell Biol 64: 348–356

    PubMed  Google Scholar 

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

    Google Scholar 

  • Shimmen T, Yano M (1984) Active sliding movement of latex beads coated with skeletal muscle myosin on Chara actin bundles. Protoplasma 121: 132–137

    Google Scholar 

  • —, Yokota E (1994) Physiological and biochemical aspects of cytoplasmic streaming. Int Rev Cytol 155: 97–139

    Google Scholar 

  • Smith JD, Todd P, Staehelin LA (1997) Modulation of statolith mass and grouping in white clover (Trifolium repens) grown in 1-g, microgravity and on the clinostat. Plant J 12: 1361–1373

    PubMed  Google Scholar 

  • Spudich A (1994) Myosin reorganization in activated RBL cells correlates temporally with stimulated secretion. Cell Motil Cytoskeleton 29: 345–353

    PubMed  Google Scholar 

  • Staiger CJ (2000) Signaling to the actin cytoskeleton in plants. Annu Rev Plant Physiol Plant Mol Biol 51: 257–288

    PubMed  Google Scholar 

  • Tang X, Hepler PK, Scordilis SP (1989) Immunochemical and immunocytochemical identification of a myosin heavy chain polypeptide inNicotiana pollen tubes. J Cell Sci 92: 569–574

    PubMed  Google Scholar 

  • Tirlapur UK, Cai G, Faleri C, Moscatelli A, Scali M, Del Casino C, Tiezzi A, Cresti M (1995) Confocal imaging and immunogold electron microscopy of changes in distribution of myosin during pollen hydration, germination and pollen tube growth inNicotiana tabacum L. Eur J Cell Biol 67: 209–217

    PubMed  Google Scholar 

  • Tischendorf G, Sawitzky D, Werz G (1987) Antibodies specific for vertebrate actin, myosin, or vinculin recognize epitopes in the giant nucleus of the marine green algaAcetabularia. Cell Motil Cytoskeleton 7: 78–86

    Google Scholar 

  • Tonini R, Grohovaz F, Laporta CAM, Mazzanti M (1999) Gating mechanism of the nuclear pore complex channel in isolated neonatal and adult mouse liver nuclei. FASEB J 13: 1395–1403

    PubMed  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

    Google Scholar 

  • Uyeda TQP (1996) Ultra-fastChara myosin: a test case for the swinging lever arm model for force production by myosin. J Plant Res 109: 231–239

    Google Scholar 

  • Volkmann D, Baluška F (1999) The actin cytoskeleton in plants: from transport networks to signaling networks. Microsc Res Tech 47: 135–154

    PubMed  Google Scholar 

  • — —, Lichtscheidl IK, Driss-Ecole D, Perbal G (1999) Statoliths motions in gravity-perceiving plant cells: does actomyosin counteract gravity? FASEB J 13: S143-S147

    PubMed  Google Scholar 

  • Wang A, Liang Y, Fridell RA, Probst FJ, Wilcox ER, Touchman JW, Morton CC, Morell RJ, Noben-Trauth K, Camper SA, Friedman TB (1998) Association of unconventional myosinMYO15 mutations with human nonsyndromic deafnessDFNB3. Science 280: 1447–1451

    PubMed  Google Scholar 

  • Weber V, Harata M, Hauser H, Wintersberger U (1995) The actinrelated protein Act3p ofSaccharomyces cere isiae is located in the nucleus. Mol Biol Cell 6: 1263–1270

    PubMed  Google Scholar 

  • Wunsch C, Wada M (1996) Recovery of interphase nuclei from extreme structural alterations in centrifuged fern protonemal cells. Eur J Cell Biol 71: 414–422

    PubMed  Google Scholar 

  • —, Kurachi M, Kikumoto M, Tashiro H, Wada M (1998) Detection of intranuclear forces by the use of laser optics during the recovery process of elongated interphase nuclei in centrifuged protonemal cells ofAdiantum capillus-eneris. J Plant Res 111: 399–405

    Google Scholar 

  • Yonemura S, Pollard TD (1992) The localization of myosin I and myosin II inAcanthamoeba by fluorescence microscopy. J Cell Sci 102: 629–642

    PubMed  Google Scholar 

  • Yumura S (1996) Rapid redistribution of myosin II in livingDictyostelium amoebae, as revealed by fluorescent probes introduced by electroporation. Protoplasma 192: 217–222

    Google Scholar 

  • Zhao K, Wang W, Rando OJ, Xue Y, Swiderek K, Kuo A, Crabtree GR (1998) Rapid and phosphoinositol-dependent binding of the SWI/SNF-like BAF complex to chromatin after T lymphocyte receptor signaling. Cell 95: 627–636

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Dedicated to Professor Walter Gustav Url on the occasion of his 70th birthday

Rights and permissions

Reprints and permissions

About this article

Cite this article

Baluška, F., Polsakiewicz, M., Peters, M. et al. Tissue-specific subcellular immunolocalization of a myosin-like protein in maize root apices. Protoplasma 212, 137–145 (2000). https://doi.org/10.1007/BF01282915

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01282915

Keywords

Navigation