Abstract
Interactions between the actin cytoskeleton and myosin motor proteins are crucial for force generation, intracellular transport, and morphogenesis in eukaryotic cells. In plant cells, the rapid intracellular transport system—cytoplasmic streaming—is generated by the interaction between actin and the plant-specific myosin XI. Genomic analyses have revealed numerous actin and myosin genes (paralogues) in angiosperms, suggesting that the plant actin–myosin XI system is more complex than expected. Recent molecular biological and biochemical approaches have revealed the functional diversity of actins and myosins in vascular plants. Actin isoforms show various biochemical properties in vitro and form distinct filamentous structures in cells. Myosin XIs exhibit various enzymatic properties and velocities, and their classification based on velocities crudely correlates with their expression pattern in tissues. Myosin XI isoform numbers increase with the evolution of plants from algae to angiosperms, suggesting that diversity of the actin–myosin system is essential for higher plant systems, such as development, morphogenesis, fertilisation, and environmental response. In this review, we summarise recent advances in research into the plant actin–myosin system and discuss the diversity entwined with plant evolution, and then propose a new model for intracellular transport regulated by multiple actin–myosin isoforms.
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References
Avisar D, Prokhnevsky AI, Dolja VV (2008) Class VIII myosins are required for plasmodesmatal localization of a closterovirus Hsp70 homolog. J Virol 82:2836–2843. https://doi.org/10.1128/JVI.02246-07
Baluska F, Cvrckova F, Kendrick-Jones J, Volkmann D (2001) Sink plasmodesmata as gateways for phloem unloading. Myosin VIII and calreticulin as molecular determinants of sink strength? Plant Physiol 126:39–46
Cai G, Parrotta L, Cresti M (2015) Organelle trafficking, the cytoskeleton, and pollen tube growth. J Integr Plant Biol 57:63–78. https://doi.org/10.1111/jipb.12289
Duan Z, Tominaga M (2018) Actin-myosin XI: an intracellular control network in plants. Biochem Biophys Res Commun 506:403–408. https://doi.org/10.1016/j.bbrc.2017.12.169
El-Mezgueldi M, Bagshaw CR (2008) The myosin family: biochemical and kinetic properties. In: Myosins. Springer, Berlin, pp 55–93
Golomb L, Abu-Abied M, Belausov E, Sadot E (2008) Different subcellular localizations and functions of Arabidopsis myosin VIII. BMC Plant Biol 8:3. https://doi.org/10.1186/1471-2229-8-3
Gunning PW, Ghoshdastider U, Whitaker S, Popp D, Robinson RC (2015) The evolution of compositionally and functionally distinct actin filaments. J Cell Sci 128:2009–2019. https://doi.org/10.1242/jcs.165563
Haraguchi T, Tominaga M, Matsumoto R, Sato K, Nakano A, Yamamoto K, Ito K (2014) Molecular characterization and subcellular localization of Arabidopsis class VIII myosin, ATM1. J Biol Chem 289:12343–12355. https://doi.org/10.1074/jbc.M113.521716
Haraguchi T et al (2018) Functional diversity of class XI myosins in Arabidopsis thaliana. Plant Cell Physiol 59:2268–2277. https://doi.org/10.1093/pcp/pcy147
Ito K et al (2003) Recombinant motor domain constructs of Chara corallina myosin display fast motility and high ATPase activity. Biochem Biophys Res Commun 312:958–964
Kandasamy MK, McKinney EC, Meagher RB (2009) A single vegetative actin isovariant overexpressed under the control of multiple regulatory sequences is sufficient for normal Arabidopsis development. Plant Cell 21:701–718. https://doi.org/10.1105/tpc.108.061960
Kato T, Morita MT, Tasaka M (2010) Defects in dynamics and functions of actin filament in Arabidopsis caused by the dominant-negative actin fiz1-induced fragmentation of actin filament. Plant Cell Physiol 51:333–338. https://doi.org/10.1093/pcp/pcp189
Kijima ST, Hirose K, Kong SG, Wada M, Uyeda TQ (2016) Distinct biochemical properties of Arabidopsis thaliana actin isoforms. Plant Cell Physiol 57:46–56. https://doi.org/10.1093/pcp/pcv176
Kijima ST, Staiger CJ, Katoh K, Nagasaki A, Ito K, Uyeda TQP (2018) Arabidopsis vegetative actin isoforms, AtACT2 and AtACT7, generate distinct filament arrays in living plant cells. Sci Rep 8:4381. https://doi.org/10.1038/s41598-018-22707-w
Kollmar M, Muhlhausen S (2017) Myosin repertoire expansion coincides with eukaryotic diversification in the Mesoproterozoic era. BMC Evol Biol 17:211. https://doi.org/10.1186/s12862-017-1056-2
Lanza M et al (2012) Role of actin cytoskeleton in brassinosteroid signaling and in its integration with the auxin response in plants. Dev Cell 22:1275–1285. https://doi.org/10.1016/j.devcel.2012.04.008
Madison SL, Nebenführ A (2013) Understanding myosin functions in plants: are we there yet? Curr Opin Plant Biol 16(6):710–717. https://doi.org/10.1016/j.pbi.2013.10.004
Madison SL, Buchanan ML, Glass JD, McClain TF, Park E, Nebenfuhr A (2015) Class XI myosins move specific organelles in pollen tubes and are required for normal fertility and pollen tube growth in Arabidopsis. Plant Physiol 169:1946–1960. https://doi.org/10.1104/pp.15.01161
McDowell JM, Huang S, McKinney EC, An YQ, Meagher RB (1996) Structure and evolution of the actin gene family in Arabidopsis thaliana. Genetics 142:587–602
Meagher RB, McKinney EC, Vitale AV (1999) The evolution of new structures: clues from plant cytoskeletal genes. Trends Genet 15:278–284
Muhlhausen S, Kollmar M (2013) Whole-genome duplication events in plant evolution reconstructed and predicted using myosin motor proteins. BMC Evol Biol 13:202. https://doi.org/10.1186/1471-2148-13-202
Nishiyama T et al (2018) The Chara genome: secondary complexity and implications for plant terrestrialization. Cell 174:448–464.e24. https://doi.org/10.1016/j.cell.2018.06.033
Ojangu EL, Tanner K, Pata P, Jarve K, Holweg CL, Truve E, Paves H (2012) Myosins XI-K, XI-1, and XI-2 are required for development of pavement cells, trichomes, and stigmatic papillae in Arabidopsis. BMC Plant Biol 12:81. https://doi.org/10.1186/1471-2229-12-81
Okamoto K et al (2015) Regulation of organ straightening and plant posture by an actin-myosin XI cytoskeleton. Nat Plant 1:15031
Okuda S et al (2009) Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells. Nature 458:357–361. https://doi.org/10.1038/nature07882
Peremyslov VV, Prokhnevsky AI, Avisar D, Dolja VV (2008) Two class XI myosins function in organelle trafficking and root hair development in Arabidopsis. Plant Physiol 146:1109–1116. https://doi.org/10.1104/pp.107.113654
Peremyslov VV, Prokhnevsky AI, Dolja VV (2010) Class XI myosins are required for development, cell expansion, and F-actin organization in Arabidopsis. Plant Cell 22:1883–1897. https://doi.org/10.1105/tpc.110.076315
Prokhnevsky AI, Peremyslov VV, Dolja VV (2008) Overlapping functions of the four class XI myosins in Arabidopsis growth, root hair elongation, and organelle motility. Proc Natl Acad Sci USA 105:19744–19749. https://doi.org/10.1073/pnas.0810730105
Reddy ASN (2001) Molecular motors and their functions in plants. Int Rev Cytol 204:97–178
Reichelt S, Knight AE, Hodge TP, Baluska F, Samaj 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. Plant J 19:555–567
Rula S et al (2018) Measurement of enzymatic and motile activities of Arabidopsis myosins by using Arabidopsis actins. Biochem Biophys Res Commun 495:2145–2151. https://doi.org/10.1016/j.bbrc.2017.12.071
Sattarzadeh A, Franzen R, Schmelzer E (2008) The Arabidopsis class VIII myosin ATM2 is involved in endocytosis. Cell Motil Cytoskeleton 65:457–468. https://doi.org/10.1002/cm.20271
Shimmen T, Yokota E (2004) Cytoplasmic streaming in plants. Curr Opin Cell Biol 16:68–72. https://doi.org/10.1016/j.ceb.2003.11.009
Slajcherova K, Fiserova J, Fischer L, Schwarzerova K (2012) Multiple actin isotypes in plants: diverse genes for diverse roles? Front Plant Sci 3:226. https://doi.org/10.3389/fpls.2012.00226
Takeuchi H, Higashiyama T (2016) Tip-localized receptors control pollen tube growth and LURE sensing in Arabidopsis. Nature 531:245–248. https://doi.org/10.1038/nature17413
Tamura K et al (2013) Myosin XI-i links the nuclear membrane to the cytoskeleton to control nuclear movement and shape in Arabidopsis. Curr Biol 23:1776–1781. https://doi.org/10.1016/j.cub.2013.07.035
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Tominaga M, Ito K (2015) The molecular mechanism and physiological role of cytoplasmic streaming. Curr Opin Plant Biol 27:104–110. https://doi.org/10.1016/j.pbi.2015.06.017
Tominaga M, Nakano A (2012) Plant-specific myosin XI, a molecular perspective. Front Plant Sci 3:211. https://doi.org/10.3389/fpls.2012.00211
Tominaga M et al (2003) Higher plant myosin XI moves processively on actin with 35 nm steps at high velocity. EMBO J 22:1263–1272. https://doi.org/10.1093/emboj/cdg130
Tominaga M, Kojima H, Yokota E, Nakamori R, Anson M, Shimmen T, Oiwa K (2012) The calcium-induced mechanical change in the neck domain alters the activity of plant myosin XI. J Biol Chem 287:30711–30718
Tominaga M et al (2013) Cytoplasmic streaming velocity as a plant size determinant. Dev Cell 27:345–352. https://doi.org/10.1016/j.devcel.2013.10.005
Ueda H et al (2010) Myosin-dependent endoplasmic reticulum motility and F-actin organization in plant cells. Proc Natl Acad Sci USA 107:6894–6899. https://doi.org/10.1073/pnas.0911482107
Yamamoto K, Kikuyama M, Sutoh-Yamamoto N, Kamitsubo E (1994) Purification of actin based motor protein from Chara corallina. Proc Jpn Acad 70:175–180
Yamamoto K, Hamada S, Kashiyama T (1999) Myosins from plants. Cell Mol Life Sci 56:227–232
Yang L, Qin L, Liu G, Peremyslov VV, Dolja VV, Wei Y (2014) Myosins XI modulate host cellular responses and penetration resistance to fungal pathogens. Proc Natl Acad Sci USA 111:13996–14001. https://doi.org/10.1073/pnas.1405292111
Yokota E, Shimmen T (1994) Isolation and characterization of plant myosin from pollen tubes of lily. Protoplasma 177:153–162
Acknowledgements
The authors would like to thank the Japan Society for the Promotion of Science [KAKENHI 24658002, 26440131, and 15H01309 (to K.I.), 20001009, 23770060, and 25221103 (to M.T.)] and the Japan Science and Technology Agency, ALCA, [JPMJAL1401 (to K.I., T.H., Z.D., and M.T.)] for support.
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Haraguchi, T., Duan, Z., Tamanaha, M., Ito, K., Tominaga, M. (2019). Diversity of Plant Actin–Myosin Systems. In: Sahi, V., Baluška, F. (eds) The Cytoskeleton. Plant Cell Monographs, vol 24. Springer, Cham. https://doi.org/10.1007/978-3-030-33528-1_4
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