Actin-dependent fluid-phase endocytosis in inner cortex cells of maize root apices

Journal of Experimental Botany

Volumn 55, Issue 396, 2004, Pages 463-473

  Baluska F ^a,b   Samaj J ^a,c   Hlavacka, A ^a   Kendrick Jones, J ^d   Volkmann, D ^a  

^a UNIVERSITY OF BONN   (Germany)

^b INSTITUTE OF BOTANY   (Slovakia)

^c INSTITUTE OF CHEMISTRY   (Slovakia)

^d MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Actin; Endocytosis; Myosin; Pit fields; Plasmodesmata; Root cortex

Indexed keywords

BIOLOGICAL MEMBRANES; BIOMARKERS; CELLS; DYES; ELECTROLYSIS; FLUORESCENCE; PLASMAS; POLYMERIZATION; TISSUE;

CORTEX CELLS; FLUID-PHASE ENDOCYTOSIS; PLANT ROOTS;

CROPS;

ACTIN; CYCLOPEPTIDE; DEPSIPEPTIDE; FLUORESCENT DYE; FUSED HETEROCYCLIC RINGS; ISOQUINOLINE DERIVATIVE; JASPAMIDE; LATRUNCULIN B; LUCIFER YELLOW; MYOSIN; THIAZOLE DERIVATIVE; THIAZOLIDINE DERIVATIVE;

ARTICLE; DRUG ANTAGONISM; DRUG EFFECT; ENDOCYTOSIS; HISTOLOGY; IMMUNOELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; MAIZE; METABOLISM; PHYSIOLOGY; PLANT ROOT; ULTRASTRUCTURE;

ACTINS; BICYCLO COMPOUNDS, HETEROCYCLIC; DEPSIPEPTIDES; ENDOCYTOSIS; FLUORESCENT DYES; IMMUNOHISTOCHEMISTRY; ISOQUINOLINES; MICROSCOPY, IMMUNOELECTRON; MYOSINS; PEPTIDES, CYCLIC; PLANT ROOTS; THIAZOLES; THIAZOLIDINES; ZEA MAYS;

ZEA MAYS;

EID: 17944396324     PISSN: 00220957     EISSN: None     Source Type: Journal    
DOI: 10.1093/jxb/erh042     Document Type: Article

References (70)

1. Bahaji A, Cornejo MJ, Ortiz-Zapater E, Contreras I, Aniento F. 2001. Uptake of endocytic markers by rice cells: variations related to the growth phase. European Journal of Cell Biology 80, 178-186.
2. Baluška F, Barlow PW, Hauskrecht M, Kubica Š, Parker JS, Volkmann D. 1995. Microtubule arrays in maize root cells. Interplay between the cytoskeleton, nuclear organization, and post-mitotic cellular growth patterns. New Phytologist 130, 177-192.
3. Baluška F, Barlow PW, Volkmann D. 2000. 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. Dordrecht, The Netherlands: Kluwer Academic Publishers, 457-476.
4. Baluška F, Brailsford RW, Hauskrecht M, Jackson MB, Barlow PW. 1993b. Cellular dimorphism in the maize root cortex: involvement of microtubules, ethylene and gibberellin in the behavior in post-mitotic growth zones. Botanica Acta 106, 394-403.
5. Baluška F, Cvrcková F, Kendrick-Jones J, Volkmann D. 2001b. Sink plasmodesmata as gateways for phloem unloading. Myosin VIII and calreticulin as molecular determinants of sink strength? Plant Physiology 126, 39-46.
6. Baluška F, Hlavacka A, Šamaj J, Palme K, Robinson DG, Matoh T, McCurdy DW, Menzel D, Volkmann D. 2002. F-actin-dependent endocytosis of cell wall pectins in meristematic root cells: insights from brefeldin A-induced compartments. Plant Physiology 130, 422-431.
7. Baluška F, Jásik J, Edelmann HG, Salajová T, Volkmann D. 2001a. Latrunculin B induced plant dwarfism: plant cell elongation is F-actin dependent. Developmental Biology 231, 113-124.
8. Baluška F, 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.). Journal of Cell Science 103, 91-200.
9. Baluška F, Parker JS, Barlow PW. 1993a. The microtubular cytoskeleton in cells of cold-treated roots of maize (Zea mays L.) shows tissue-specific responses. Protoplasma 172, 84-96.
10. Baluška F, Vitha S, Barlow PW, Volkmann D. 1997. Rearrangements of F-actin arrays in growing cells of intact maize root apex tissue: a major developmental switch occurs in the postmitotic transition region. European Journal of Cell Biology 72, 113-121.
11. Baluška F, Volkmann D, Barlow PW. 2001c. A polarity crossroad in the transition growth zone of maize root apices: cytoskeletal and developmental implications. Journal of Plant Growth Regulation 20, 170-181.
12. Basrai MA, Naider F, Becker JM. 1990. Internalization of Lucifer Yellow in Candida albicans by fluid phase endocytosis. Journal of General Microbiology 136, 1059-1065.
13. Bret-Harte MS, Silk WK. 1994. Non-vascular, symplasmic diffusion of sucrose cannot satisfy the carbon demands of growth in the primary root tip of Zea mays L. Plant Physiology 105, 19-33.
14. Chaffey NJ, Barlow PW. 2001. The cytoskeleton facilitates a three-dimensional symplasmic continuum in the long-lived ray and axial parenchyma cells of angiosperm trees. Planta 213, 811-823.
15. Chaffey NJ, Barlow PW. 2002. Myosin, microtubules, and microfilaments: co-operation between cytoskeletal components during cambial cell division and secondary vascular differentiation in trees. Planta 214, 526-536.
16. Chaffey NJ, Harris N. 1985. Plasmatubules: fact or artefact? Planta 165, 185-190.
17. Cholewa E, Peterson CA. 2001. Detecting exodermal Casparian bands in vivo and fluid-phase endocytosis in onion (Allium cepa L.) roots. Canadian Journal of Botany 79, 30-37.
18. Čiamporová M, Dekánková K, Hanáčková Z, Ovečka M, Baluška F. 2003. Structural aspects of root hair initiation in Vicia sativa roots treated with F-actin polymerization inhibitor latrunculin B. Plant and Soil 255, 1-7.
19. Coetzee J, Fineran BA. 1989. Translocation of lysine from the host Melicope simplex to the parasitic dwarf mistletoe Korthalsella lindsayi (Viscaceae). New Phytologist 112, 377-381.
20. Cram WJ. 1980. Pinocytosis in plants. New Phytologist 84, 1-17.
21. Derksen J, Knuiman B, Hoedemaekers K, Guyon A, Bonhomme S, Pierson ES. 2002. Growth and cellular organization of Arabidopsis pollen tubes in vitro. Sexual Plant Reproduction 15, 133-139.
22. Evert RF, Eschrich W, Neuberger DS, Eichhorn SE. 1977a. Tubular extension of the plasmalemma in leaf cells of Zea mays L. Planta 135, 203-205.
23. Evert RF, Eschrich W, Heyser W. 1977b. Distribution and structure of the plasmodesmata in mesophyll and bundle-sheath cells of Zea mays L. Planta 136, 77-89.
24. 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.
25. Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Muller P, Delbarre A, Ueda T, Nakano A, Jürgens G. 2003. The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112, 219-230.
26. Gradmann D, Robinson DG. 1989. Does turgor prevent endocytosis in plants? Plant, Cell and Environment 12, 151-154.
27. Harris N, Chaffey NJ. 1986. Plasmatubules - real modifications of the plasmalemma. Nordisk Journal of Botany 6, 599-607.
28. Hawes C, Crooks K, Coleman J, Satiat-Jeunematrie B. 1995. Endocytosis in plants: fact or artefact? Plant, Cell and Environment 18, 1245-1252.
29. Hillmer S, Hedrich R, Robert-Nicoud M, Robinson DG. 1990. Uptake of Lucifer Yellow CH in leaves of Commelina communis is mediated by endocytosis. Protoplasma 158, 142-148.
30. Hillmer S, Quader H, Robert-Nicoud M, Robinson DG. 1989. Lucifer Yellow uptake in cells and protoplasts of Daucus carota visualized by laser scanning microscopy. Journal of Experimental Botany 40, 417-423.
31. Holstein SEH. 2002. Clathrin and plant endocytosis. Traffic 3, 614-620.
32. +-ATPase in the root apex: evidence for strong expression in xylem parenchyma and asymmetric localization within cortical and epidermal cells. Physiologia Plantarum 104, 311-316.
33. Jin M, Snider MD. 1993. Role of microtubules in transferrin receptor transport from the cell surface to endosomes of the Golgi complex. Journal of Biological Chemistry 268, 18390-18397.
34. Jitsuyama Y, Suzuki T, Harada T, Fujikawa S. 2001. Loading process of sugars into cabbage petiole and asparagus shoot apex cells by incubation with hypertonic sugar solutions. Protoplasma 217, 205-216.
35. Jürgens G, Geldner N. 2002. Protein secretion in plants: from the trans-Golgi network to the outer space. Traffic 3, 605-613.
36. Kandasamy MK, Kappler R, Kristen U. 1988. Plasmatubules in the pollen tubes of Nicotiana sylvestris. Planta 173, 35-41.
37. Kazmierczak A, Maszewski J. 1997. Uptake of fluorescent-labelled BSA into root cells: Endocytosis? Acta Societatis botanicorum Poloniae 66, 319-324.
38. Knight A, Kendrick-Jones J. 1993. A myosin-like protein from a higher plant. Journal of Molecular Biology 231, 148-154.
39. Low PS, Chandra S. 1994. Endocytosis in plants. Annual Review of Plant Physiology and Plant Molecular Biology 45, 609-631.
40. McCurdy DW. 1999. Is 2,3 butanedione monoxime an effective inhibitor of myosin-based activities in plant cells? Protoplasma 209, 120-125.
41. Morris SM, Arden SD, Roberts RC, Kendrick-Jones J, Cooper JA, Luzio JP, Buss F. 2002. Myosin VI binds to and localizes with Dab2, potentially linking receptor-mediated endocytosis and the actin cytoskeleton. Traffic 3, 331-341.
42. Munn AL. 2001. Molecular requirements for the internalization step of endocytosis: insights from yeast. Biochimica et Biophysica Acta 1535, 236-257.
43. Nishizawa N, Mori S. 1977. Invagination of plasmalemma: its role in the absorption of macromolecules in rice roots. Plant and Cell Physiology 18, 767-782.
44. Oparka KJ, Murant EA, Wright KM, Prior DAM, Harris N. 1991. The drug probenecid inhibits the vacuolar accumulation of fluorescent anions in onion epidermal cells. Journal of Cell Science 99, 557-563.
45. Oparka KJ, Robinson D, Prior DAM, Derrick P, Wright KM. 1988. Uptake of Lucifer Yellow CH into intact barley roots: evidence for fluid-phase endocytosis. Planta 176, 541-547.
46. Oparka KJ, Wright KM, Murant EA, Allan EJ. 1993. Fluid-phase endocytosis: do plants need it? Journal of Experimental Botany 44, 247-255.
47. Ou GS, Chen ZL, Yuan M. 2002. Jasplakinolide reversibly disrupts actin filaments in suspension-cultured tobacco BY-2 cells. Protoplasma 219, 168-175.
48. Owen TP, Platt-Aloia KA, Thomson WW. 1991. Ultrastructural localization of Lucifer Yellow and endocytosis in plant cells. Protoplasma 160, 115-120.
49. Palevitz BA, Hepler PK. 1985. Changes in dye coupling of stomatal cells of Allium and Commelina demonstrated by microinjection of Lucifer Yellow. Planta 164, 473-479.
50. 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. Dordrecht, Netherlands: Kluwer Academic Publishers, 29-44.
51. Reichelt S, 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 post-cytokinetic cell wall. The Plant Journal 19, 555-569.
52. Riezman H. 1985. Endocytosis in yeast: several of the yeast secretory mutants are defective in endocytosis. Cell 40, 1001-1009.
53. Robertson JG, Lyttleton P. 1982. Coated and smooth vesicles in the biogenesis of cell walls, plasma membranes, infection threads and peribacteroid membranes in root hairs and nodules of white clover. Journal of Cell Science 58, 63-78.
54. Robinson DG, Hinz G, Holstein SEH. 1998. The molecular characterization of transport vesicles. Plant Molecular Biology 38, 49-76.
55. Roszak R, Rambour S. 1997. Uptake of Lucifer Yellow by plant cells in the presence of endocytotic inhibitors. Protoplasma 199, 198-207.
56. 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 Physiology 41, 571-582.
57. Šamaj J, Ovecka M, Hlavacka A, et al. 2002. Involvement of the mitogen-activated protein kinase SIMK in regulation of root hair tip-growth. EMBO Journal 21, 3296-3306.
58. Sawitzky H, Liebe S, Willingale-Theune J, Menzel D. 1999. The anti-proliferative agent jasplakinolide rearranges the actin cytoskeleton of plant cells. European Journal of Cell Biology 78, 424-433.
59. Schulz A. 1994. Phloem transport and differential unloading in pea seedlings after source and sink manipulations. Planta 192, 239-248.
60. Shurety W, Stewart NL, Stow JL. 1998. Fluid-phase markers in the basolateral endocytic pathway accumulate in response to the actin assembly-promoting drug jasplakinolide. Molecular Biology of the Cell 9, 957-975.
61. Spector I, Braet F, Shochet NR, Bubb MR. 1999. New anti-actin drugs in the study of the organization and function of the actin cytoskeleton. Microscope Research Techniques 47, 18-37.
62. Stark-Urnau M, Mendgen K. 1995. Sequential deposition of plant glycoproteins and polysaccharides at the host-parasite interface of Uromyces vignae and Vigna sinensis. Evidence for endocytosis and secretion. Protoplasma 186, 1-11.
63. Stewart WW. 1981. Lucifer dyes - highly fluorescent dyes for biological tracing. Nature 292, 17-21.
64. Subtil A, Dautry-Varsat A. 1997. Microtubule depolymerization inhibits clathrin coated-pit internalization in non-adherent cell lines while interleukin 2 endocytosis is not affected. Journal of Cell Science 110, 2441-2447.
65. Swanson JA, Yirinec BD, Silverstein SC. 1985. Phorbol esters and horseradish peroxidase stimulate pinocytosis and redirect the flow of pinocytosed fluid in macrophages. Journal of Cell Science 100, 851-859.
66. Tominaga M, Yokota E, Sonobe S, Shimmen T. 2000. Mechanism of inhibition of cytoplasmic streaming by a myosin inhibitor, 2,3-butanedione monoxime. Protoplasma 213, 46-54.
67. Uemura M, Steponkus PL. 2003. Modification of the intracellular sugar content alters the incidence of freeze-induced membrane lesions of protoplasts isolated from Arabidopsis thaliana leaves. Plant, Cell and Environment 26, 1083-1096.
68. Warmbrodt RD. 1985. Studies on the root of Hordeum vulgare L. - ultrastructure of the seminal root with special reference to the phloem. American Journal of Botany 72, 414-432.
69. Wiederkehr A, Meier KD, Riezman H. 2001. Identification and characterization of Saccharomyces cerevisiae mutants defective in fluid-phase endocytosis. Yeast 18, 759-773.
70. Wright KM, Oparka KJ. 1989. Uptake of Lucifer Yellow CH into plant cell protoplasts: a quantitative assessment of fluid-phase endocytosis. Planta 179, 257-264.