Viruses are parasites that require the host cell machinery for their propagation within and between cells. Myosins are molecular motors involved in the trafficking of cargos along actin filaments. Plant viruses have evolved to borrow this transport mechanism to aid their infection and spread within the plant. However, little is known about which of the many plant myosins are essential and at which specific steps they act to support virus infection. Here we investigated the role of different N. benthamiana myosins during the infection by Tobacco mosaic virus (TMV). Our results show that class XI myosins play specific roles in the reproduction and intracellular movement of TMV in association with the dynamic endoplasmic reticulum network, whereas class VIII myosins support the specific targeting of the viral movement protein to plasmodesmata and thus the cell-to-cell movement of the virus. Together these results indicate that TMV interacts with distinct myosins during specific infection steps.
Vyšlo v časopise: Myosins VIII and XI Play Distinct Roles in Reproduction and Transport of. PLoS Pathog 10(10): e32767. doi:10.1371/journal.ppat.1004448 Kategorie: Research Article prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004448
1. Burch-SmithTM, ZambryskiPC (2012) Plasmodesmata paradigm shift: regulation from without versus within. Annu Rev Plant Biol 63 : 239–260.
2. MauleA, FaulknerC, Benitez-AlfonsoY (2012) Plasmodesmata "in Communicado". Front Plant Sci 3 : 30.
3. NiehlA, HeinleinM (2011) Cellular pathways for viral transport through plasmodesmata. Protoplasma 248 : 75–99.
4. AmariK, BoutantE, HofmannC, Schmitt-KeichingerC, Fernandez-CalvinoL, et al. (2010) A family of plasmodesmal proteins with receptor-like properties for plant viral movement proteins. PloS Pathog 6: e1001119.
5. AmariK, LerichA, Schmitt-KeichingerC, DoljaVV, RitzenthalerC (2011) Tubule-guided cell-to-cell movement of a plant virus requires class XI myosin motors. PLoS Pathog 7: e1002327.
6. HirashimaK, WatanabeY (2001) Tobamovirus replicase coding region is involved in cell-to-cell movement. J Virol 75 : 8831–8836.
7. HirashimaK, WatanabeY (2003) RNA helicase domain of tobamovirus replicase executes cell-to-cell movement possibly through collaboration with its nonconserved region. J Virol 77 : 12357–12362.
8. Guenoune-GelbartD, ElbaumM, SagiG, LevyA, EpelBL (2008) Tobacco mosaic virus (TMV) replicase and movement protein function synergistically in facilitating TMV spread by lateral diffusion in the plasmodesmal desmotubule of Nicotiana benthamiana. Mol Plant Microbe Interact 21 : 335–345.
9. PeiroA, Martinez-GilL, TamboreroS, PallasV, Sanchez-NavarroJA, et al. (2014) The Tobacco mosaic virus movement protein associates with but does not integrate into biological membranes. J Virol 88 : 3016–3026.
10. PenaEJ, HeinleinM (2013) Cortical microtubule-associated ER sites: organization centers of cell polarity and communication. Curr Opin Plant Biol 16 : 764–773.
11. KawakamiS, WatanabeY, BeachyRN (2004) Tobacco mosaic virus infection spreads cell to cell as intact replication complexes. Proc Natl Acad Sci U S A 101 : 6291–6296.
12. LiuJZ, BlancaflorEB, NelsonRS (2005) The Tobacco mosaic virus 126-kilodalton protein, a constituent of the virus replication complex, alone or within the complex aligns with and traffics along microfilaments. Plant Physiol 138 : 1853–1865.
13. HofmannC, NiehlA, SambadeA, SteinmetzA, HeinleinM (2009) Inhibition of Tobacco mosaic virus movement by expression of an actin-binding protein. Plant Physiol 149 : 1810–1823.
14. WrightKM, WoodNT, RobertsAG, ChapmanS, BoevinkP, et al. (2007) Targeting of TMV movement protein to plasmodesmata requires the actin/ER network: evidence from FRAP. Traffic 8 : 21–31.
15. PeremyslovVV, MocklerTC, FilichkinSA, FoxSE, JaiswalP, et al. (2011) Expression, splicing, and evolution of the myosin gene family in plants. Plant Physiol 155 : 1191–1204.
16. WuSZ, RitchieJA, PanAH, QuatranoRS, BezanillaM (2011) Myosin VIII regulates protonemal patterning and developmental timing in the moss Physcomitrella patens. Mol Plant 4 : 909–921.
17. BaluskaF, CvrckovaF, Kendrick-JonesJ, VolkmannD (2001) Sink plasmodesmata as gateways for phloem unloading. Myosin VIII and calreticulin as molecular determinants of sink strength? Plant Physiol 126 : 39–46.
18. ReicheltS, KnightAE, HodgeTP, BaluskaF, SamajJ, et al. (1999) Characterization of the unconventional myosin VIII in plant cells and its localization at the post-cytokinetic cell wall. Plant J 19 : 555–567.
19. GolombL, Abu-AbiedM, BelausovE, SadotE (2008) Different subcellular localizations and functions of Arabidopsis myosin VIII. BMC Plant Biol 8 : 3.
20. SattarzadehA, FranzenR, SchmelzerE (2008) The Arabidopsis class VIII myosin ATM2 is involved in endocytosis. Cell Motil Cytoskeleton 65 : 457–468.
21. HaraguchiT, TominagaM, MatsumotoR, SatoK, NakanoA, et al. (2014) Molecular characterization and subcellular localization of Arabidopsis class VIII myosin, ATM1. J Biol Chem: doi 10.1074/jbc.M1113.521716
22. OjanguEL, JarveK, PavesH, TruveE (2007) Arabidopsis thaliana myosin XIK is involved in root hair as well as trichome morphogenesis on stems and leaves. Protoplasma 230 : 193–202.
23. PeremyslovVV, ProkhnevskyAI, AvisarD, DoljaVV (2008) Two class XI myosins function in organelle trafficking and root hair development in Arabidopsis. Plant Physiol 146 : 1109–1116.
24. ProkhnevskyAI, PeremyslovVV, DoljaVV (2008) Overlapping functions of the four class XI myosins in Arabidopsis growth, root hair elongation, and organelle motility. Proc Natl Acad Sci U S A 105 : 19744–19749.
25. VidaliL, BurkartGM, AugustineRC, KerdavidE, TuzelE, et al. (2010) Myosin XI is essential for tip growth in Physcomitrella patens. Plant Cell 22 : 1868–1882.
26. PeremyslovVV, ProkhnevskyAI, DoljaVV (2010) Class XI myosins are required for development, cell expansion, and F-Actin organization in Arabidopsis. Plant Cell 22 : 1883–1897.
27. TominagaM, KimuraA, YokotaE, HaraguchiT, ShimmenT, et al. (2013) Cytoplasmic streaming velocity as a plant size determinant. Dev Cell 27 : 345–352.
28. AvisarD, ProkhnevskyAI, MakarovaKS, KooninEV, DoljaVV (2008) Myosin XI-K Is required for rapid trafficking of Golgi stacks, peroxisomes, and mitochondria in leaf cells of Nicotiana benthamiana. Plant Physiol 146 : 1098–1108.
29. AvisarD, Abu-AbiedM, BelausovE, SadotE, HawesC, et al. (2009) A comparative study of the involvement of 17 Arabidopsis myosin family members on the motility of Golgi and other organelles. Plant Physiol 150 : 700–709.
30. UedaH, YokotaE, KutsunaN, ShimadaT, TamuraK, et al. (2010) Myosin-dependent endoplasmic reticulum motility and F-actin organization in plant cells. Proc Natl Acad Sci U S A 107 : 6894–6899.
31. TamuraK, IwabuchiK, FukaoY, KondoM, OkamotoK, 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.
32. PeremyslovVV, KlockoAL, FowlerJE, DoljaVV (2012) Arabidopsis myosin XI-K localizes to the motile endomembrane vesicles associated with F-actin. Front Plant Sci 3 : 184.
33. PeremyslovVV, MorgunEA, KurthEG, MakarovaKS, KooninEV, et al. (2013) Identification of myosin XI receptors in Arabidopsis defines a distinct class of transport vesicles. Plant Cell 25 : 3022–3038.
34. AvisarD, ProkhnevskyAI, DoljaVV (2008) Class VIII myosins are required for plasmodesmatal localization of a closterovirus Hsp70 homolog. J Virol 82 : 2836–2843.
35. YuanZJ, ChenHY, ChenQ, OmuraT, XieLH, et al. (2011) The early secretory pathway and an actin-myosin VIII motility system are required for plasmodesmatal localization of the NSvc4 protein of Rice stripe virus. Virus Res 159 : 62–68.
36. AgbeciM, GrangeonR, NelsonRS, ZhengH, LaliberteJF (2013) Contribution of host intracellular transport machineries to intercellular movement of Turnip mosaic virus. PLoS Pathog 9: e1003683.
37. FengZ, ChenX, BaoY, DongJ, ZhangZ, et al. (2013) Nucleocapsid of Tomato spotted wilt tospovirus forms mobile particles that traffic on an actin/endoplasmic reticulum network driven by myosin XI-K. New Phytol 200 : 1212–1224.
38. SunZ, ZhangS, XieL, ZhuQ, TanZ, et al. (2012) The secretory pathway and the actomyosin motility system are required for plasmodesmatal localization of the P7-1 of Rice black-streaked dwarf virus. Arch Virol 158 : 1055–1064.
39. HarriesPA, ParkJW, SasakiN, BallardKD, MauleAJ, et al. (2009) Differing requirements for actin and myosin by plant viruses for sustained intercellular movement. Proc Natl Acad Sci U S A 106 : 17594–17599.
40. OjanguEL, TannerK, PataP, JarveK, HolwegCL, et al. (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.
41. HeinleinM, EpelBL, PadgettHS, BeachyRN (1995) Interaction of tobamovirus movement proteins with the plant cytoskeleton. Science 270 : 1983–1985.
42. LindboJA (2007) High-efficiency protein expression in plants from agroinfection-compatible Tobacco mosaic virus expression vectors. BMC Biotechnol 7 : 52.
43. RaffaeleS, BayerE, LafargeD, CluzetS, RetanaSG, et al. (2009) Remorin, a solanaceae protein resident in membrane rafts and plasmodesmata, impairs Potato virus X movement. Plant Cell 21 : 1541–1555.
44. TilsnerJ, AmariK, TorranceL (2011) Plasmodesmata viewed as specialised membrane adhesion sites. Protoplasma 248 : 39–60.
45. LewandowskiDJ, DawsonWO (2000) Functions of the 126-and 183-kDa proteins of Tobacco mosaic virus. Virology 271 : 90–98.
46. DingXS, LiuJZ, ChengNH, FolimonovA, HouYM, et al. (2004) The Tobacco mosaic virus 126-kDa protein associated with virus replication and movement suppresses RNA silencing. Mol Plant Microbe Interact 17 : 583–592.
47. VoglerH, AkbergenovR, ShivaprasadPV, DangV, FaslerM, et al. (2007) Modification of small RNAs associated with suppression of RNA silencing by tobamovirus replicase protein. J Virol 81 : 10379–10388.
48. HarriesPA, SchoelzJE, NelsonRS (2010) Intracellular transport of viruses and their components: utilizing the cytoskeleton and membrane highways. Mol Plant Microbe Interact 23 : 1381–1393.
49. SattentauQ (2008) Avoiding the void: cell-to-cell spread of human viruses. Nat Rev Microbiol 6 : 815–826.
50. SattentauQJ (2011) The direct passage of animal viruses between cells. Curr Opin Virol 1 : 396–402.
51. RobertsKL, BainesJD (2011) Actin in herpesvirus infection. Viruses 3 : 336–346.
52. AvisarD, Abu-AbiedM, BelausovE, SadotE (2012) Myosin XIK is a major player in cytoplasm dynamics and is regulated by two amino acids in its tail. J Exp Bot 63 : 241–249.
53. RodrigoG, ZwartMP, ElenaSF (2014) Onset of virus systemic infection in plants is determined by speed of cell-to-cell movement and number of primary infection foci. J R Soc Interface 11.
54. LiuC, NelsonRS (2013) The cell biology of Tobacco mosaic virus replication and movement. Front Plant Sci 4 : 12.
55. dos Reis FigueiraA, GolemS, GoregaokerSP, CulverJN (2002) A nuclear localization signal and a membrane association domain contribute to the cellular localization of the Tobacco mosaic virus 126-kDa replicase protein. Virology 301 : 81–89.
56. LewisJD, LazarowitzSG (2010) Arabidopsis synaptotagmin SYTA regulates endocytosis and virus movement protein cell-to-cell transport. Proc Natl Acad Sci U S A 107 : 2491–2496.
57. YamazakiT, TakataN, UemuraM, KawamuraY (2010) Arabidopsis synaptotagmin SYT1, a type I signal-anchor protein, requires tandem C2 domains for delivery to the plasma membrane. J Biol Chem 285 : 23165–23176.
58. RuizMT, VoinnetO, BaulcombeDC (1998) Initiation and maintenance of virus-induced gene silencing. Plant Cell 10 : 937–946.
59. BrandnerK, SambadeA, BoutantE, DidierP, MelyY, et al. (2008) Tobacco mosaic virus movement protein interacts with green fluorescent protein-tagged microtubule end-binding protein 1. Plant Physiol 147 : 611–623.
60. BoutantE, DidierP, NiehlA, MelyY, RitzenthalerC, et al. (2010) Fluorescent protein recruitment assay for demonstration and analysis of in vivo protein interactions in plant cells and its application to Tobacco mosaic virus movement protein. Plant J 62 : 171–177.
61. KarimiM, InzeD, DepickerA (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7 : 193–195.
62. NiehlA, PasquierA, FerriolI, MelyY, HeinleinM (2014) Comparison of the Oilseed rape mosaic virus and Tobacco mosaic virus movement proteins (MP) reveals common and dissimilar MP functions for tobamovirus spread. Virology 456–457 : 43–54.
63. MansillaC, SanchezF, PadgettHS, PogueGP, PonzF (2009) Chimeras between Oilseed rape mosaic virus and Tobacco mosaic virus highlight the relevant role of the tobamoviral RdRp as pathogenicity determinant in several hosts. Mol Plant Pathol 10 : 59–68.
64. ThevenazP, RuttimannUE, UnserM (1998) A pyramid approach to subpixel registration based on intensity. IEEE Trans Image Process 7 : 27–41.
Zvýšte si kvalifikáciu online z pohodlia domova
Nemáte účet? Registrujte sa
Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
