Skip to main content

Interactions Between the Actin Cytoskeleton and an Auxin Transport Protein

  • Chapter
Book cover Actin: A Dynamic Framework for Multiple Plant Cell Functions

Part of the book series: Developments in Plant and Soil Sciences ((DPSS,volume 89))

Abstract

In shoots, polar auxin transport is basipetal (i.e., from the shoot apex toward the base), and is driven by the basal localization of the auxin efflux carrier complex. One mechanism by which this efflux carrier complex could be localized to the basal membrane is through attachment to the actin cytoskeleton. The efflux carrier protein complex is believed to consist of several polypeptides, including a regulatory subunit that binds auxin transport inhibitors such as naphthylphthalamic acid (NPA). Several lines of experimentation have been used to determine whether the NPA-binding protein interacts with actin filaments. The NPA-binding protein has been shown to partition with the actin cytoskeleton during detergent extraction. Agents that specifically alter the polymerization state of the actin cytoskeleton also change the amount of NPA-binding protein and actin recovered in these cytoskeletal pellets. Actin affinity columns were prepared with polymers of actin purified from zucchini hypocotyl tissue. NPA-binding activity was eluted in a single peak from the actin filament column. Cytochalasin D, which fragments the actin cytoskeleton, was shown to reduce polar auxin transport in zucchini hypocotyls. The interaction of the NPA-binding protein with the actin cytoskeleton may localize it in one plane of the plasma membrane, and thereby control the polarity of auxin transport.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
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

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Alessa L and Kropf DL (1999) F-actin marks the rhizoid pole in living Pelvetia compressa zygotes. Development 126: 201–209

    PubMed  CAS  Google Scholar 

  • Andersland JM, Jagendorf AT and Parthasarathy MV (1992) The isolation of actin from pea roots by DNase I affinity chromatography. Plant Physiol 100: 1716–1723

    Article  PubMed  CAS  Google Scholar 

  • Apel ED and Merlie JP (1995) Assembly of the postsynaptic apparatus. Curr Opin Neurobiol 5: 62–67

    Article  PubMed  CAS  Google Scholar 

  • Ayscough KR and Drubin DG (1996) Actin: general principles from studies in yeast. Annu Rev Cell Dev Biol 12: 129–160

    Article  PubMed  CAS  Google Scholar 

  • Bernasconi P, Bhavesh CP, Reagan JD and Subramanian MV (1996) The N-1-naphthylphthalamic acid-binding protein is an integral membrane protein. Plant Physiol 111:427–432

    PubMed  CAS  Google Scholar 

  • Butler JH, Hu S, Brady SR, Dixon MW and Muday GK (1998) In vitro and in vivo evidence for actin association of the naphthylphthalamic acid-binding protein from zucchini hypocotyls. Plant J 13: 291–301

    Article  PubMed  CAS  Google Scholar 

  • Calvert CM, Gant SJ and Bowles DJ (1996) Tomato annexins p34 and p35 bind to F-actin and display nucleotide phosphodiesterase activity inhibited by phospholipid binding. Plant Cell 8: 333–342

    PubMed  CAS  Google Scholar 

  • Cande WZ, Goldsmith MHM and Ray PM (1973) Polar auxin transport and auxin-induced elongation in the absence of cytoplasmic streaming. Planta 111: 279–296

    Article  CAS  Google Scholar 

  • Carraway C (1992) Association of cytoskeletal proteins with membranes. In: Carraway K, Carraway C (eds) The Cytoskeleton: A Practical Approach. Oxford: IRL Press, pp 123–150

    Google Scholar 

  • Chant J (1999) Cell polarity in yeast. Annu Rev Cell Dev Biol 15: 365–391

    Article  PubMed  CAS  Google Scholar 

  • Chen R, Hilson P, Sedbrook J, Rosen E, Caspar T and Masson PH (1998) The Arabidopsis thaliana AGRAVITROPIC1 gene encodes a component of the polar-auxin-transport efflux carrier. Proc Natl Acad Sci USA 95: 15112–15117

    Article  PubMed  CAS  Google Scholar 

  • Chen R, Rosen E and Masson PH (1999) Gravitropism in higher plants. Plant Physiol 120: 343–350

    Article  PubMed  CAS  Google Scholar 

  • Cox DN and Muday GK (1994) NPA binding activity is peripheral to the plasma membrane and is associated with the cytoskeleton. Plant Cell 6: 1941–1953

    PubMed  CAS  Google Scholar 

  • Dixon MW, Jacobson JA, Cady CT and Muday GK (1996) Cytoplasmic orientation of the naphthylphthalamic acid-binding protein in zucchini plasma membrane vesicles. Plant Physiol 112: 421–432

    PubMed  CAS  Google Scholar 

  • Drubin DG and Nelson WJ (1996) Origins of cell polarity. Cell 84: 335–344

    Article  PubMed  CAS  Google Scholar 

  • Ebenezer C (1997) Regulation of auxin transport through changes in the cytoskeletal association of the NPA binding protein. MS Thesis. Wake Forest University, Winston-Salem, NC

    Google Scholar 

  • Fischer C and Neuhaus G (1996) Influence of auxin on the establishment of bilateral symmetry in monocots. Plant J 9: 659–669

    Article  CAS  Google Scholar 

  • Froehner SC (1993) Regulation of ion channel distribution at synapses. Annu Rev Neurosci 16: 347–368

    Article  PubMed  CAS  Google Scholar 

  • Gälweiler L, Guan C, Müller A, Wisman E, Mendgen K, Yephremov A and Palme K (1998) Regulation of polar auxin transport by AtPINl in Arabidopsis vascular tissue. Science 282: 2226–2230

    Article  PubMed  Google Scholar 

  • Gautam M, Noakes PG, Mudd J, Nichol M, Chu GC, Sanes JR and Merlie JP (1995) Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice. Nature 377: 232–236

    Article  PubMed  CAS  Google Scholar 

  • Goldsmith MHM (1977) The polar transport of auxin. Annu Rev Plant Physiol 28: 439–478.

    Article  CAS  Google Scholar 

  • Goodner B and Quantrano RS (1993) Fucus embryogenesis: a model to study the establishment of polarity. Plant Cell 5: 1471–1481

    PubMed  Google Scholar 

  • Hadfi K, Speth V and Neuhaus G (1998) Auxin-induced developmental patterns in Brassica juncea embryos. Development 125: 879–887

    PubMed  CAS  Google Scholar 

  • Hertel R, Lomax TL and Briggs WR (1983) Auxin transport in membrane vesicles from Cucurbita pepo L. Planta 157: 193–201

    Article  CAS  Google Scholar 

  • Hu S, Brady SR, Kovar D, Staiger CJ, Clarke GB, Roux SJ and Muday G (2000) Identification of plant F-actin-binding proteins by F-actin chromatography. Plant J, In review

    Google Scholar 

  • Jacobs M and Gilbert SF (1983) Basal localization of the presumptive auxin transport carrier in pea stem cells. Science 220: 1297–1300

    Article  PubMed  CAS  Google Scholar 

  • Kandasamy M, McKinney E and Meagher R (1999) The late pollen-specific actins in angiosperms. Plant J 18: 681–691

    Article  PubMed  CAS  Google Scholar 

  • Kropf DL, Berge SK and Quatrano RS (1989) Actin localization during Fucus embryogenesis. Plant Cell 1: 191–200

    PubMed  CAS  Google Scholar 

  • Li R, Zheng Y and Drubin DG (1995) Regulation of cortical actin cytoskeleton assembly during polarized cell growth in budding yeast. J Cell Biol 128: 599–615

    Article  PubMed  CAS  Google Scholar 

  • Liu C-M, Xu Z-H and Chua N-H (1993) Auxin polar transport is essential for the establishment of bilateral symmetry during early plant embryogenesis. Plant Cell 5: 621–630

    PubMed  CAS  Google Scholar 

  • Liu X and Yen L-F (1992) Purification and characterization of actin from maize pollen. Plant Physiol 99: 1151–1155

    Article  PubMed  CAS  Google Scholar 

  • Lomax TL, Muday GK and Rubery P (1995) Auxin transport. In: Davies PJ (ed) Plant Hormones: Physiology, Biochemistry, and Molecular Biology. Norwell: Kluwer Academic Press, pp 509–530

    Google Scholar 

  • Morris DA and Johnson CF (1990) The role of auxin efflux carriers in the reversible loss of polar auxin transport in the pea (Pisum sativum L.) stem. Planta 181: 117–124

    Article  CAS  Google Scholar 

  • Morris DA and Robinson JS (1998) Targeting of auxin carriers to the plasma membrane: differential effects of brefeldin A on the traffic of auxin uptake and efflux carriers. Planta 205: 606–612

    Article  CAS  Google Scholar 

  • Morris DA, Rubery PH, Jarman J and Sabater M (1991) Effects of inhibitors of protein synthesis on transmembrane auxin transport in Cucurbita pepo L. hypocotyl segments. J Exp Bot 42: 773–783

    Article  CAS  Google Scholar 

  • Muday GK, Brunn SA, Haworth P and Subramanian M (1993) Evidence for a single naphthylphthalamic acid binding site on the zucchini plasma membrane. Plant Physiol 103: 449–456

    PubMed  CAS  Google Scholar 

  • Müller A, Guan C, Gälweiler L, Tanzler P, Huijser P, Marchant A, Parry G, Bennett M, Wisman E and Palme K (1998) AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J 17: 6903–6911

    Article  PubMed  Google Scholar 

  • Nelson WJ and Hammerton RW (1989) A membrane-cytoskeletal complex containing Na+,K+-ATPase, ankyrin, and fodrin in Madin-Darby canine kidney (MDCK) cells: implications for the biogenesis of epithelial cell polarity. J Cell Biol 108: 893–902

    Article  PubMed  CAS  Google Scholar 

  • Okada K, Ueda J, Komaki MK, Bell CJ and Shimura Y (1991) Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3: 677–684

    PubMed  CAS  Google Scholar 

  • Ortuno A, Sanchez-Bravo J, Moral JR, Acosta M and Sabater F (1990) Changes in the concentration of indole-3-acetic acid during the growth of etiolated lupin hypocotyls. Physiol Plant 78: 211–217

    Article  CAS  Google Scholar 

  • Pinder JC, Sleep JA, Bennett PM and Gratzer WB (1995) Concentrated Tris solutions for the preparation, depolymerization, and assay of actin; application to erythroid actin. Anal Biochem 225: 291–295

    Article  PubMed  CAS  Google Scholar 

  • Rashotte A, Brady S, Reed R, Ante S and Muday G (2000) Basipetal auxin transport is required for gravitropism in roots of Arabidopsis. Plant Physiol 122:481–490

    Article  PubMed  CAS  Google Scholar 

  • Ren H, Gibbon BC, Ashworth SL, Sherman DM, Yuan M and Staiger CJ (1997) Actin purified from maize pollen functions in living plant cells. Plant Cell 9: 1445–1457

    PubMed  CAS  Google Scholar 

  • Rubery PH and Sheldrake AR (1974) Carrier-mediated auxin transport. Planta 118:101–121

    Article  CAS  Google Scholar 

  • Schiavone FM and Cooke TJ (1987) Unusual patterns of somatic embryogenesis in the domesticated carrot: developmental effects of exogenous auxins and auxin transport inhibitors. Cell Differ 21: 53–62

    Article  PubMed  CAS  Google Scholar 

  • Shaw SL and Quatrano RS (1996) Polar localization of a dihydropyridine receptor on living Fucus zygotes. J Cell Sci 109: 335–342

    PubMed  CAS  Google Scholar 

  • Sheterline P, Clayton J and Sparrow JC (1998) Actin. Protein Profile 4: 1–272

    Google Scholar 

  • Steinmann T, Geldner N, Grebe M, Mangold S, Jackson C, Paris S, Gälweiler L, Palme K and Jurgens G (1999) Coordinated polar localization of auxin efflux carrier PINI by GNOM ARF GEF. Science 268: 316–318

    Article  Google Scholar 

  • Sussman MR and Gardner G (1980) Solubilization of the receptor for N-1-napthylphthalamic acid. Plant Physiol 66: 1074–1078

    Article  PubMed  CAS  Google Scholar 

  • Suttle JC (1988) Effect of ethylene treatment on polar IAA transport, net IAA uptake and specific binding of N-l-naphthylphthalamic acid in tissues and microsomes isolated from etiolated pea epicotyls. Plant Physiol 88: 795–799

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson S and Morris DA (1994) Targeting of auxin carriers to the plasma membrane: effects of monensin on transmembrane auxin transport in Cucurbita pepo L. tissue. Planta 193: 194–202

    Article  CAS  Google Scholar 

  • Zechel K (1980) Isolation of polymerization-competent cytoplasmic actin by affinity chromatography on immobilized DNase I using formamide as eluant. Eur J Biochem 110: 343–348

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

C. J. Staiger F. Baluška D. Volkmann P. W. Barlow

Rights and permissions

Reprints and permissions

Copyright information

© 2000 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Muday, G.K. (2000). Interactions Between the Actin Cytoskeleton and an Auxin Transport Protein. In: Staiger, C.J., Baluška, F., Volkmann, D., Barlow, P.W. (eds) Actin: A Dynamic Framework for Multiple Plant Cell Functions. Developments in Plant and Soil Sciences, vol 89. Springer, Dordrecht. https://doi.org/10.1007/978-94-015-9460-8_30

Download citation

  • DOI: https://doi.org/10.1007/978-94-015-9460-8_30

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-90-481-5504-0

  • Online ISBN: 978-94-015-9460-8

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics