Abstract
Fimbrins are a class of conserved actin-binding proteins with a modular organization consisting of two tandemly repeated actin-binding domains and an N-terminal calcium-binding headpiece. The tandem arrangement of the two actin-binding domains enables fimbrins to cross-link actin filaments into tightly packed bundles that are typical of those seen in microvilli and other surface structures, such as microspikes. Fimbrin homologues have been identified in Arabidopsis thaliana and show the same general domain organization as non-plant fimbrins. AtFim1 binds to and cross-links pollen F-actin in a calcium-independent manner, and protects actin filaments from profilin-induced depolymerization both in vitro and in living stamen hair cells. The possible role of fimbrins in organizing the supramolecular architecture of the actin cytoskeleton in plant cells is discussed in light of the large size of the actin gene family and the presence of other actin-bundling proteins.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Adams AEM, Botstein D and Drubin DG (1991) Requirement of yeast fimbrin for actin organization and morphogenesis in vivo. Nature 354: 404–408
Adams AEM, Shen W, Lin C-S, Leavitt J and Matsudaira P (1995) Isoform-specific complementation of the yeast sac6 null mutation by human fimbrin. Mol Cell Biol 15: 69–75
Arpin M, Friederich E, Algrain M, Vernel F and Louvard D (1994) Functional differences between L- and T-plastin isoforms. J Cell Biol 127: 1995–2008
Blancaflor EB, Jones DL and Gilroy S (1998) Alterations in the cytoskeleton accompany aluminum-induced growth inhibition and morphological changes in primary roots of maize. Plant Physiol 118: 159–172
Bretscher A (1981) Fimbrin is a cytoskeletal protein that crosslinks F-actin in vitro. Proc Natl Acad Sci USA 78: 6849–6853
Bretscher A and Weber K (1980) Fimbrin, a new microfilament-associated protein present in microvilli and other cell surface structures. J Cell Biol 86: 335–340
Brower SM, Honts JE and Adams AEM (1995) Genetic analysis of the fimbrin-actin binding interaction in Saccharomyces cerevisiae. Genetics 140: 91–101
Castresana J and Saraste M (1995) Does vav bind to F-actin through a CH domain? FEBS Lett 374: 149–151
Christensen HEM, Mathur J and Chua N-H (1997) Cloning and characterization of the fimbrin gene family in Arabidopsis thaliana. 5th Int Congr Plant Mol Biol, Singapore, Abstr 278
Correia I, Chu D, Chou Y-H, Goldman RD and Matsudaira P (1999) Integrating the actin and vimentin cytoskeletons: adhesion-dependent formation of fimbrin-vimentin complexes in macrophages. J Cell Biol 146: 831–842
Cruz-Ortega, R, Cushman JC and Ownby JD (1997) cDNA clones encoding 1,3-β-glucanase and a fimbrin-like cytoskeletal protein are induced by A1 toxicity in wheat roots. Plant Physiol 114: 1453–1460
de Arruda MV, Watson S, Lin C-S, Leavitt J and Matsudaira P (1990) Fimbrin is a homologue of the cytoplasmic phosphoprotein plastin and has domains homologous with calmodulin and actin gelation proteins. J Cell Biol 111: 1069–1079
Drubin DG, Miller KG and Botstein D (1988) Yeast actin-binding proteins: evidence for a role in morphogenesis. J Cell Biol 107: 2551–2561
Gilliland LU, McKinney EC and Meagher RB (1999) Analysis of vegetative mutants in the conserved actin gene family of Arabidopsis. Mol Biol Cell 10 (Suppl): 22a
Gilliland LU, McKinney EC, Asmussen MA and Meagher RB (1998) Detection of deleterious genotypes in multigenerational studies. I. Disruptions in individual Arabidopsis actin genes. Genetics 149: 717–725
Gimona M and Winder SJ (1998) Single calponin homology domains are not actin-binding domains. Curr Biol 8: R674–R675
Glenney JR Jr, Kaulfus P, Matsudaira P and Weber K (1981) F-actin binding and bundling properties of fimbrin, a major cytoskeletal protein of microvillus core filaments. J Biol Chem 256: 9283–9288
Goldsmith SC, Pokala N, Shen W, Fedorov AA, Matsudaira P and Almo S (1997) The structure of an actin-cross-linking domain from human fimbrin. Nature Struct Biol 4: 708–712
Goldstein D, Djeu J, Latter G, Burbeck S and Leavitt J (1985) Abundant synthesis of the transformation-induced protein of neoplastic human fibroblasts, plastin, in normal lymphocytes. Cancer Res 45: 5643–5647
Grabski S and Schindler M (1995) Aluminum induces rigor within the actin network of soybean cells. Plant Physiol 108: 897–901
Hanein D, Volkmann N, Goldsmith S, Michon A-M, Lehman W, Craig R, DeRosier D, Almo S and Matsudaira P (1998) An atomic model of fimbrin binding to F-actin and its implications for filament cross-linking and regulation. Nature Struct Biol 9: 787–792
Honts JE, Sandrock TS, Brower SM, O’Dell JL and Adams AEM (1994) Actin mutations that show suppression with fimbrin mutations identify a likely fimbrin-binding site on actin. J Cell Biol 126: 413–422
Klahre U, Friederich E, Kost B, Louvard D and Chua N-H (2000) Villin-like actin-binding proteins are expressed ubiquitously in Arabidopsis. Plant Physiol 122: 35–47
Kobayashi I, Kobayashi Y and Hardham AR (1994) Dynamic reorganization of microtubules and microfilaments in flax cells during the resistance response to flax rust infection. Planta 195: 237–247
Kovar DR, Staiger CJ, Weaver EA and McCurdy DW (2000) Functional characterization of AtFim1, an actin filament cross-linking protein from Arabidopsis thaliana. Submitted
Kübier E and Riezman H (1993) Actin and fimbrin are required for the internalization step of endocytosis in yeast. EMBO J 12: 2855–2862
Lin C-S, Shen W, Chen ZP, Tu Y-H and Matsudaira P (1994) Identification of I-plastin, a human isoform expressed in intestine and kidney. Mol Cell Biol 14: 2457–2467
Lorenz M, Popp D and Holmes KC (1993) Refinement of the F-actin model against X-ray fiber diffraction data by the use of a directed mutation algorithm. J Mol Biol 234: 826–836
Matsudaira P (1991) Modular organization of actin cross-linking proteins. Trends Biochem Sci 16: 87–92
Matsudaira P, Mandelkow E, Renner W, Hesterburg LK and Weber K (1983) Role of fimbrin and villin in determining the interfilament distances of actin bundles. Nature 301: 209–214
McCurdy DW and 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 Cytoskel 15: 76–87
McCurdy DW and Kim M (1998) Molecular cloning of a novel fimbrin-like cDNA from Arabidopsis thaliana. Plant Mol Biol 36: 23–31
McKinney EC, Ali N, Traut A, Feldmann KA, Belostotsky DA, McDowell JM and Meagher RB (1995) Sequence-based identification of T-DNA insertion mutations in Arabidopsis: actin mutants act2–1 and act4–1. Plant J 8: 613–622.
Meagher RB, McKinney EC and Kandasamy MK (1999) Isovariant dynamics expands and buffers the responses of complex systems: the diverse plant actin gene family. Plant Cell 11:1–12
Namba Y, Ito M, Zu Y, Shigesada K and Maruyama K (1992) Human T cell L-plastin bundles actin filaments in a calcium-dependent manner. J Biochem 112: 503–507
Prassler J, Stocker S, Marriott G, Heidecker M, Kellermann and Gerisch G (1997) Interaction of a Dictyostelium member of the plastin/fimbrin family with actin filaments and actin-myosin complexes. Mol Biol Cell 8: 83–95
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
Sonobe S and Shibaoka H (1989) Cortical fine actin filaments in higher plant cells visualized by rhodamine-phalloidin after pretreatment with m-maleimidobenzoyl N-hydroxysuccinimide ester. Protoplasma 148: 80–86
Staiger CJ (2000) Signaling to the actin cytoskeleton in plant cells. Annu Rev Plant Physiol Plant Mol Biol 51: 257–288
Staiger CJ, Gibbon BC, Kovar DR and Zonia LE (1997) Profilin and actin depolymerizing factor: modulators of actin organization in plants. Trends Plant Sci 2: 275–281
Stradal T, Kranewitter W, Winder S J and Gimona M (1998) CH domains revisited. FEBS Lett 431: 134–137
Traas JA, Doonan JH, Rawlins DJ, Shaw PJ, Watts J and Lloyd CW (1987) An actin network is present throughout the cell cycle of carrot cells and associates with the dividing nucleus. J Cell Biol 105: 387–395
Vidali L, Yokota E, Cheung A, Shimmen T and Hepler PK (1999) The 135 kDa actin-bundling protein from Lilium longiflorum pollen is the plant homologue of villin. Protoplasma 209: 283–291
Waller F and Nick P (1997) Response of actin microfilaments during phytochrome-controlled growth of maize seedlings. Protoplasma 200: 154–162
Way M, Pope B and Weeds AG (1992) Evidence for functional homology in the F-actin binding domains of gelsolin and a-actinin: Implications for the requirements of severing and capping. J Cell Biol 119: 835–842
Winder SJ, Hemmings L, Maciver SK, Bolton SJ, Tinsley JM, Davies KE, Critchley DR and Kendrick-Jones J (1995) Utrophin actin binding domain: analysis of actin binding and cellular targeting. J Cell Sci 108: 63–71
Yokota E, Takahara K and Shimmen T (1998) Actin-bundling protein isolated from pollen tubes of lily. Biochemical and immunocytochemical characterization. Plant Physiol 116: 1421–1429
Author information
Authors and Affiliations
Editor information
Rights and permissions
Copyright information
© 2000 Springer Science+Business Media Dordrecht
About this chapter
Cite this chapter
McCurdy, D.W., Staiger, C.J. (2000). Fimbrin. 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_5
Download citation
DOI: https://doi.org/10.1007/978-94-015-9460-8_5
Publisher Name: Springer, Dordrecht
Print ISBN: 978-90-481-5504-0
Online ISBN: 978-94-015-9460-8
eBook Packages: Springer Book Archive