Truncated Myosin XI Tail Fusions Inhibit Peroxisome, Golgi, and Mitochondrial Movement in Tobacco Leaf Epidermal Cells: a Genetic Tool for the Next Generation

Overview

Journal J Exp Bot

Publisher Oxford University Press

Specialty Biology

Date 2008 May 27

PMID 18503043

Citations 65

Authors

Imogen A Sparkes

Nicholas A Teanby

Chris Hawes

Affiliations

Soon will be listed here.

Abstract

Although organelle movement in higher plants is predominantly actin-based, potential roles for the 17 predicted Arabidopsis myosins in motility are only just emerging. It is shown here that two Arabidopsis myosins from class XI, XIE, and XIK, are involved in Golgi, peroxisome, and mitochondrial movement. Expression of dominant negative forms of the myosin lacking the actin binding domain at the amino terminus perturb organelle motility, but do not completely inhibit movement. Latrunculin B, an actin destabilizing drug, inhibits organelle movement to a greater extent compared to the effects of AtXIE-T/XIK-T expression. Amino terminal YFP fusions to XIE-T and XIK-T are dispersed throughout the cytosol and do not completely decorate the organelles whose motility they affect. XIE-T and XIK-T do not affect the global actin architecture, but their movement and location is actin-dependent. The potential role of these truncated myosins as genetically encoded inhibitors of organelle movement is discussed.

Citing Articles

Functional-metabolic coupling in distinct renal cell types coordinates organ-wide physiology and delays premature ageing.

Holcombe J, Weavers H Nat Commun. 2023; 14(1):8405.

PMID: 38110414 PMC: 10728150. DOI: 10.1038/s41467-023-44098-x.

Actomyosin and CSI1/POM2 cooperate to deliver cellulose synthase from Golgi to cortical microtubules in Arabidopsis.

Liu L, Wang T, Bai Y, Yan P, Dai L, Du P Nat Commun. 2023; 14(1):7442.

PMID: 37978293 PMC: 10656550. DOI: 10.1038/s41467-023-43325-9.

Visualizing the dynamics of plant energy organelles.

Koenig A, Liu B, Hu J Biochem Soc Trans. 2023; 51(6):2029-2040.

PMID: 37975429 PMC: 10754284. DOI: 10.1042/BST20221093.

The OPAQUE1/DISCORDIA2 myosin XI is required for phragmoplast guidance during asymmetric cell division in maize.

Nan Q, Liang H, Mendoza J, Liu L, Fulzele A, Wright A Plant Cell. 2023; 35(7):2678-2693.

PMID: 37017144 PMC: 10291028. DOI: 10.1093/plcell/koad099.

Hitchhiking Across Kingdoms: Cotransport of Cargos in Fungal, Animal, and Plant Cells.

Christensen J, Reck-Peterson S Annu Rev Cell Dev Biol. 2022; 38:155-178.

PMID: 35905769 PMC: 10967659. DOI: 10.1146/annurev-cellbio-120420-104341.

References

Li J, Nebenfuhr A . Organelle targeting of myosin XI is mediated by two globular tail subdomains with separate cargo binding sites. J Biol Chem. 2007; 282(28):20593-602. DOI: 10.1074/jbc.M700645200. View

Tyska M, Mackey A, Huang J, Copeland N, Jenkins N, Mooseker M . Myosin-1a is critical for normal brush border structure and composition. Mol Biol Cell. 2005; 16(5):2443-57. PMC: 1087248. DOI: 10.1091/mbc.e04-12-1116. View

Hashimoto K, Igarashi H, Mano S, Nishimura M, Shimmen T, Yokota E . Peroxisomal localization of a myosin XI isoform in Arabidopsis thaliana. Plant Cell Physiol. 2005; 46(5):782-9. DOI: 10.1093/pcp/pci085. View

Wang F, Thirumurugan K, Stafford W, Hammer 3rd J, Knight P, Sellers J . Regulated conformation of myosin V. J Biol Chem. 2003; 279(4):2333-6. DOI: 10.1074/jbc.C300488200. View

Golomb L, Abu-Abied M, Belausov E, Sadot E . Different subcellular localizations and functions of Arabidopsis myosin VIII. BMC Plant Biol. 2008; 8:3. PMC: 2275265. DOI: 10.1186/1471-2229-8-3. View

Li X, Mabuchi K, Ikebe R, Ikebe M . Ca2+-induced activation of ATPase activity of myosin Va is accompanied with a large conformational change. Biochem Biophys Res Commun. 2004; 315(3):538-45. DOI: 10.1016/j.bbrc.2004.01.084. View

Reichelt S, Knight A, Hodge T, Baluska F, Samaj J, Volkmann D . Characterization of the unconventional myosin VIII in plant cells and its localization at the post-cytokinetic cell wall. Plant J. 1999; 19(5):555-67. DOI: 10.1046/j.1365-313x.1999.00553.x. View

Allan V, Thompson H, McNiven M . Motoring around the Golgi. Nat Cell Biol. 2002; 4(10):E236-42. DOI: 10.1038/ncb1002-e236. View

Sparkes I, Runions J, Kearns A, Hawes C . Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat Protoc. 2007; 1(4):2019-25. DOI: 10.1038/nprot.2006.286. View

10.

Wu X, Rao K, Zhang H, Wang F, Sellers J, Matesic L . Identification of an organelle receptor for myosin-Va. Nat Cell Biol. 2002; 4(4):271-8. DOI: 10.1038/ncb760. View

11.

Miller D, Scordilis S, Hepler P . Identification and localization of three classes of myosins in pollen tubes of Lilium longiflorum and Nicotiana alata. J Cell Sci. 1995; 108 ( Pt 7):2549-63. DOI: 10.1242/jcs.108.7.2549. View

12.

Hofgen R, Willmitzer L . Storage of competent cells for Agrobacterium transformation. Nucleic Acids Res. 1988; 16(20):9877. PMC: 338805. DOI: 10.1093/nar/16.20.9877. View

13.

Ketelaar T, Allwood E, Anthony R, Voigt B, Menzel D, Hussey P . The actin-interacting protein AIP1 is essential for actin organization and plant development. Curr Biol. 2004; 14(2):145-9. DOI: 10.1016/j.cub.2004.01.004. View

14.

Romagnoli S, Cai G, Faleri C, Yokota E, Shimmen T, Cresti M . Microtubule- and actin filament-dependent motors are distributed on pollen tube mitochondria and contribute differently to their movement. Plant Cell Physiol. 2007; 48(2):345-61. DOI: 10.1093/pcp/pcm001. View

15.

Peremyslov V, Prokhnevsky A, Avisar D, Dolja V . Two class XI myosins function in organelle trafficking and root hair development in Arabidopsis. Plant Physiol. 2008; 146(3):1109-16. PMC: 2259062. DOI: 10.1104/pp.107.113654. View

16.

Rodriguez O, Cheney R . Human myosin-Vc is a novel class V myosin expressed in epithelial cells. J Cell Sci. 2002; 115(Pt 5):991-1004. DOI: 10.1242/jcs.115.5.991. View

17.

daSilva L, Snapp E, Denecke J, Lippincott-Schwartz J, Hawes C, Brandizzi F . Endoplasmic reticulum export sites and Golgi bodies behave as single mobile secretory units in plant cells. Plant Cell. 2004; 16(7):1753-71. PMC: 514159. DOI: 10.1105/tpc.022673. View

18.

Reisen D, Hanson M . Association of six YFP-myosin XI-tail fusions with mobile plant cell organelles. BMC Plant Biol. 2007; 7:6. PMC: 1802837. DOI: 10.1186/1471-2229-7-6. View

19.

Mano S, Nakamori C, Hayashi M, Kato A, Kondo M, Nishimura M . Distribution and characterization of peroxisomes in Arabidopsis by visualization with GFP: dynamic morphology and actin-dependent movement. Plant Cell Physiol. 2002; 43(3):331-41. DOI: 10.1093/pcp/pcf037. View

20.

Wu X, Wang F, Rao K, Sellers J, Hammer 3rd J . Rab27a is an essential component of melanosome receptor for myosin Va. Mol Biol Cell. 2002; 13(5):1735-49. PMC: 111140. DOI: 10.1091/mbc.01-12-0595. View