AtFH1 formin mutation affects actin filament and microtubule dynamics in Arabidopsis thaliana
Language English Country Great Britain, England Media print-electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
23202131
PubMed Central
PMC3542049
DOI
10.1093/jxb/ers351
PII: ers351
Knihovny.cz E-resources
- MeSH
- Arabidopsis genetics growth & development metabolism MeSH
- Formins MeSH
- Plant Roots genetics growth & development metabolism MeSH
- Membrane Proteins genetics metabolism MeSH
- Actin Cytoskeleton genetics metabolism MeSH
- Microtubules genetics metabolism MeSH
- Mutation * MeSH
- Arabidopsis Proteins genetics metabolism MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- AFH1 protein, Arabidopsis MeSH Browser
- Formins MeSH
- Membrane Proteins MeSH
- Arabidopsis Proteins MeSH
Plant cell growth and morphogenesis depend on remodelling of both actin and microtubule cytoskeletons. AtFH1 (At5g25500), the main housekeeping Arabidopsis formin, is targeted to membranes and known to nucleate and bundle actin. The effect of mutations in AtFH1 on root development and cytoskeletal dynamics was examined. Consistent with primarily actin-related formin function, fh1 mutants showed increased sensitivity to the actin polymerization inhibitor latrunculin B (LatB). LatB-treated mutants had thicker, shorter roots than wild-type plants. Reduced cell elongation and morphological abnormalities were observed in both trichoblasts and atrichoblasts. Fluorescently tagged cytoskeletal markers were used to follow cytoskeletal dynamics in wild-type and mutant plants using confocal microscopy and VAEM (variable-angle epifluorescence microscopy). Mutants exhibited more abundant but less dynamic F-actin bundles and more dynamic microtubules than wild-type seedlings. Treatment of wild-type seedlings with a formin inhibitor, SMIFH2, mimicked the root growth and cell expansion phenotypes and cytoskeletal structure alterations observed in fh1 mutants. The results suggest that besides direct effects on actin organization, the in vivo role of AtFH1 also includes modulation of microtubule dynamics, possibly mediated by actin-microtubule cross-talk.
See more in PubMed
Abe T, Hashimoto T. 2005. Altered microtubule dynamics by expresion of modified alfa-tubulin protein causes right-handed helical growth in transgenic Arabidopsis plants. The Plant Journal 43, 191–204 PubMed
Abramoff MD, Magelhaes PJ, Ram SJ. 2004. Image processing with ImageJ. Biophotonics International 11, 36–42
Alonso J, Stepanova A, Leisse T, et al. 2003. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653–657 PubMed
Baluška F, Jasik J, Edelmann H, Salajova T, Volkmann D. 2001. Latrunculin B-induced plant dwarfism: plant cell elongation is F-actin-dependent. Developmental Biology 231, 113–124 PubMed
Bannigan A, Baskin T. 2005. Directional cell expansion—turning toward actin. Current Opinion in Plant Biology 8, 619–624 PubMed
Banno H, Chua N. 2000. Characterization of the Arabidopsis formin-like protein AFH1 and its interacting protein. Plant and Cell Physiology 41, 617–626 PubMed
Bartolini F, Gundersen G. 2010. Formins and microtubules. Biochimica et Biophysica Acta 1803, 164–173 PubMed PMC
Blanchoin L, Boujemaa-Paterski R, Henty J, Khurana P, Staiger C. 2010. Actin dynamics in plant cells: a team effort from multiple proteins orchestrates this very fast-paced game. Current Opinion in Plant Biology 13, 714–723 PubMed
Blanchoin L, Staiger C. 2010. Plant formins: diverse isoforms and unique molecular mechanism. Biochimica et Biophysica Acta 1803, 201–206 PubMed
Breuninger H, Lenhard M. 2010. Control of tissue and organ growth in plants. Current Topics in Developmental Biology 91, 185–220 PubMed
Chesarone M, DuPage A, Goode B. 2010. Unleashing formins to remodel the actin and microtubule cytoskeletons. Nature Reviews. Molecular Cell Biology 11, 62–74 PubMed
Cheung A, Niroomand S, Zou Y, Wu H. 2010. A transmembrane formin nucleates subapical actin assembly and controls tip-focused growth in pollen tubes. Proceedings of the National Academy of Sciences, USA 107, 16390–16395 PubMed PMC
Cheung A, Wu H. 2004. Overexpression of an Arabidopsis formin stimulates supernumerary actin cable formation from pollen tube cell membrane. The Plant Cell 16, 257–269 PubMed PMC
Cole R, Synek L, Žárský V, Fowler J. 2005. SEC8, a subunit of the putative Arabidopsis exocyst complex, facilitates pollen germination and competitive pollen tube growth. Plant Physiology 138, 2005–2018 PubMed PMC
Collings D, Lill A, Himmelspach R, Wasteneys G. 2006. Hypersensitivity to cytoskeletal antagonists demonstrates microtubule–microfilament cross-talk in the control of root elongation in Arabidopsis thaliana. New Phytologist 170, 275–290 PubMed
Copeland S, Green B, Burchat S, Papalia G, Banner D, Copeland J. 2007. The diaphanous inhibitory domain/diaphanous autoregulatory domain interaction is able to mediate heterodimerization between mDia1 and mDia2. Journal of Biological Chemistry 282, 30120–30130 PubMed
Cvrčková F. 2000. Are plant formins integral membrane proteins?. Genome Biology 1,, RESEARCH001 PubMed PMC
Cvrčková F, Grunt M, Žárský V. 2012. Expression of GFP–mTalin reveals an actin-related role for the arabidopsis class II formin AtFH12. Biologia Plantarum 3, 431–440
Deeks M, Cvrčková F, Machesky L, Mikitová V, Žárský V, Davies B, Hussey P. 2005. Arabidopsis group Ie formins localize to specific cell membrane domains, interact with actin-binding proteins and cause defects in cell expansion upon aberrant expression. New Phytologist 168, 529–540 PubMed
Deeks M, Fendrych M, Smertenko A, Bell K, Oparka K, Cvrčková F, Žárský V, Hussey P. 2010. The plant formin AtFH4 interacts with both actin and microtubules, and contains a newly identified microtubule-binding domain. Journal of Cell Science 123, 1209–1215 PubMed
Deeks M, Hussey P, Davies B. 2002. Formins: intermediates in signal-transduction cascades that affect cytoskeletal reorganization. Trends in Plant Science 7, 492–498 PubMed
Dvořáková L, Cvrčková F, Fischer L. 2007. Analysis of the hybrid proline-rich protein families from seven plant species suggests rapid diversification of their sequences and expression patterns. BMC Genomics 8, 412 PubMed PMC
Emons A, Hofte H, Mulder B. 2007. Microtubules and cellulose microfibrils: how intimate is their relationship?. Trends in Plant Science 12, 279–281 PubMed
Gilliland L, Kandasamy M, Pawloski L, Meagher R. 2002. Both vegetative and reproductive actin isovariants complement the stunted root hair phenotype of the Arabidopsis act2-1 mutation. Plant Physiology 130, 2199–2209 PubMed PMC
Gilliland L, Pawloski L, Kandasamy M, Meagher R. 2003. Arabidopsis actin gene ACT7 plays an essential role in germination and root growth. The Plant Journal 33, 319–328 PubMed
Granger CL, Cyr RJ. 2001. Spatiotemporal relationships between growth and microtubule orientation as revealed in living root cells of Arabidopsis thaliana transformed with green-fluorescent-protein gene construct GFP–MBD. Protoplasma 216, 201–214 PubMed
Grunt M, Žárský V, Cvrčková F. 2008. Roots of angiosperm formins: the evolutionary history of plant FH2 domain-containing protein. BMC Evolutionary Biology 8, 115 PubMed PMC
Harris E, Li F, Higgs H. 2004. The mouse formin, FRL, slows actin filament barbed end elongation, competes with capping protein, accelerates polymerization from monomers, and severs filaments. Journal of Biological Chemistry 279, 20076–20087 PubMed
Hashimoto T. 2002. Molecular genetic analysis of left-right handedness in plants. Philosophical Transactions of the Royal Society B: Biological Sciences 357, 799–808 PubMed PMC
Henty J, Bledsoe S, Khurana P, Meagher R, Day B, Blanchoin L, Staiger C. 2011. Arabidopsis actin depolymerizing factor 4 modulates the stochastic dynamic behavior of actin filaments in the cortical array of epidermal cells. The Plant Cell 23, 3711–3726 PubMed PMC
Higaki T, Kutsuna N, Sano T, Kondo N, Hasezawa S. 2010. Quantification and cluster analysis of actin cytoskeletal structures in plant cells: role of actin bundling in stomatal movement during diurnal cycles in Arabidopsis guard cells. The Plant Journal 61, 156–165 PubMed
Ingouff M, Fitz J, Guerin C, Robert H, Sorensen M, Van Damme D, Geelen D, Blanchoin L, Berger F. 2005. Plant formin AtFH5 is an evolutionarily conserved actin nucleator involved in cytokinesis. Nature Cell Biology 7, 374–380 PubMed
Ketelaar T, Allwood E, Anthony R, Voigt B, Menzel D, Hussey P. 2004. The actin-interacting protein AIP is essential for actin organization and plant development. Current Biology 14, 145–149 PubMed
Knezevic S, Streibig J, Ritz C. 2007. Utilizing R software package for dose–response studies: the concept and data analysis. Weed Technology 21, 840–848
Li Y, Shen Y, Cai C, Zhong C, Zhu L, Yuan M, Ren H. 2010. The type II Arabidopsis formin 14 interacts with microtubules and microfilaments to regulate cell division. The Plant Cell 22, 2710–2726 PubMed PMC
Marc J, Granger C, Brincat J, Fisher D, Kao T, McCubbin A, Cyr R. 1998. A GFP–MAP4 reporter gene for visualizing cortical microtubule rearrangements in living epidermal cells. The Plant Cell 10, 1927–1939 PubMed PMC
Martiniere A, Gayral P, Hawes C, Runions J. 2011. Building bridges: formin 1 of Arabidopsis forms a connection between the cell wall and the actin cytoskeleton. The Plant Journal 66, 354–365 PubMed
Michelot A, Derivery E, Paterski-Boujemma R, Guerin C, Huang S, Parcy F, Staiger C, Blanchoin L. 2006. A novel mechanism for the formation of actin-filament bundles by a nonprocessive formin. Current Biology 16, 1924–1930 PubMed
Michelot A, Guerin C, Huang S, Ingouff M, Richard S, Rodiuc N, Staiger C, Blanchoin L. 2005. The formin homology 1 domain modulates the actin nucleation and bundling activity of Arabidopsis Formin 1. The Plant Cell 17, 2296–2313 PubMed PMC
Nishimura T, Yokota E, Wada T, Shimmen T, Okada K. 2003. An Arabidopsis ACT2 dominant-negative mutation, which disturbs F-actin polimerization, reveals its distinctive function in root development. Plant and Cell Physiology 44, 1131–1140 PubMed
Peremyslov V, Prokhnevsky A, Dolja V. 2010. class XI myosins are required for development, cell expansion and F-actin organization in Arabidopsis. The Plant Cell 22, 1883–1897 PubMed PMC
Petrášek J, Schwarzerová K. 2009. Actin and microtubule cytoskeleton interactions. Current Opinion in Plant Biology 12, 728–734 PubMed
Rahman A, Bannigan A, Sulaman W, Pechter P, Blancaflor E, Baskin T. 2007. Auxin, actin and growth of the Arabidopsis thaliana primary root. The Plant Journal 50, 514–528 PubMed
Rizvi S, Neidt E, Cui J, Feiger Z, Skau C, Gardel M, Kozmin S, Kovar D. 2009. Identification and characterization of a small molecule inhibitor of formin-mediated actin assembly. Chemistry and Biology 16, 1158–1168 PubMed PMC
Sampathkumar A, Lindeboom J, Debolt S, Gutierrez R, Ehrhardt D, Ketelaar T, Persson S. 2011. Live cell imaging reveals structural associations between the actin and microtubule cytoskeleton in Arabidopsis. The Plant Cell 23, 2302–2313 PubMed PMC
Shaw S, Kamyar R, Ehrhardt D. 2003. Sustained microtubule treadmilling in Arabidopsis cortical arrays. Science 300, 1715–1718 PubMed
Smertenko A, Deeks M, Hussey P. 2010. Strategies of actin reorganisation in plant cells. Journal of Cell Science 123, 3019–3028 PubMed
Smith LG, Oppenheimer DG. 2005. Spatial control of cell expansion by the plant cytoskeleton. Annual Review of Cell and Developmental Biology 21, 271–295 PubMed
Sparkes I, Graumann K, Martiniere A, Schoberer J, Wang P, Osterrieder A. 2011. Bleach it, switch it, bounce it, pull it: using laser to reveal plant cell dynamics. Journal of Experimental Botany 62, 1–7 PubMed
Staiger C, Sheahan M, Khurana P, Wang X, McCurdy D, Blanchoin L. 2009. Actin filament dynamics are dominated by rapid growth and severing activity in the Arabidopsis cortical array. Journal of Cell Biology 182, 269–280 PubMed PMC
Szklarczyk D, Franceschini A, Kuhn M, et al. 2011. The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Research 39, D561–D568 PubMed PMC
Thitamadee S, Tuchihara K, Hashimoto T. 2002. Microtubule basis for left-handed helical growth in Arabidopsis. Nature 417, 193–196 PubMed
van der Honing H, Kieft H, Emons A, Ketelaar T. 2012. Arabidopsis VILLIN2 and VILLIN3 are required for the generation of thick actin filament bundles and for directional organ growth. Plant Physiology 58, 1426–1438 PubMed PMC
Vizcay-Barrena G, Webb S, Martin-Fernandez M, Wilson Z. 2011. Subcellular and single-molecule imaging of plant fluorescent proteins using total internal reflection fluorescent microscopy (TIRFM). Journal of Experimental Botany 62, 5419–5428 PubMed PMC
Wan Y, Ash W, Fan L, Hao H, Kim M, Lin J. 2011. Variable-angle total internal reflection fluorescence microscopy of intact cells of Arabidopsis thaliana. Plant Methods 7, 27 PubMed PMC
Wang J, Xue X, Ren H. 2012. New insights into the role of plant formins: regulating the organization of the actin and microtubule cytoskeleton. Protoplasma 249, Suppl. 2 S101–S107 PubMed
Xue X, Guo C, Du F, Lu Q, Zhang C, Ren H. 2011. AtFH8 is involved in root development under effect of low-dose latrunculin B in dividing cells. Molecular Plant 4, 264–278 PubMed
Yang W, Ren S, Zhang X, et al. 2011. BENT UPPERMOST INTERNODE1 encodes the class II Formin FH5 crucial for actin organization and rice development. The Plant Cell 23, 661–680 PubMed PMC
Ye J, Zheng Y, Yan A, Chen N, Wang Z, Huang S, Yang Z. 2009. Arabidopsis Formin3 directs the formation of actin cables and polarized growth in pollen tubes. The Plant Cell 21, 3868–3884 PubMed PMC
Yi K, Guo C, Chen D, Zhao B, Yang B, Ren H. 2005. Cloning and functional characterization of a formin-like protein (AtFH8) from Arabidopsis. Plant Physiology 138, 1071–1082 PubMed PMC
Zhang Y, He J, McCormick S. 2010. Interdependence of endomembrane trafficking and actin dynamics during polarized growth of arabidopsis pollen tubes. Plant Physiology 152, 2200–2210 PubMed PMC
Zhang Z, Zhang Y, Tan H, Wan Y, Li G, Liang W, Yuan Z, Hu J, Ren H, Zhang D. 2011. RICE MORPHOLOGY DETERMINANT encodes the type II formin FH5 and regulates rice morphogenesis. The Plant Cell 23, 681–700 PubMed PMC
Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W. 2004. GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiology 136, 2621–2632 PubMed PMC
Transmembrane formins as active cargoes of membrane trafficking
Bundling up the Role of the Actin Cytoskeleton in Primary Root Growth
Analysis of formin functions during cytokinesis using specific inhibitor SMIFH2
The Arabidopsis thaliana Class II Formin FH13 Modulates Pollen Tube Growth
Multifunctional Microtubule-Associated Proteins in Plants
Formins: linking cytoskeleton and endomembranes in plant cells
Formins and membranes: anchoring cortical actin to the cell wall and beyond