Agrobacterium-delivered virulence protein VirE2 is trafficked inside host cells via a myosin XI-K-powered ER/actin network

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 11, 2017, Pages 2982-2987

  Yang, Qinghua ^a   Li, Xiaoyang ^a   Tu, Haitao ^a   Pan, Shen Q ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Actin filaments; Endoplasmic reticulum; Myosin; Protein trafficking; VirE2

Indexed keywords

F ACTIN; MYOSIN; PROTEIN; UNCLASSIFIED DRUG; VIRULENCE PROTEIN E2; ACTIN; BACTERIAL PROTEIN; BREFELDIN A; CYTOCHALASIN D; DNA BINDING PROTEIN; ION CHANNEL; VIRE2 PROTEIN, AGROBACTERIUM; VIRULENCE FACTOR;

AGROBACTERIUM TUMEFACIENS; ARTICLE; BACTERIAL VIRULENCE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; HOST CELL; NONHUMAN; PLANT CELL; PRIORITY JOURNAL; GENETICS; INTRACELLULAR SPACE; METABOLISM; PROTEIN TRANSPORT; VIRULENCE;

ACTINS; AGROBACTERIUM TUMEFACIENS; BACTERIAL PROTEINS; BREFELDIN A; CYTOCHALASIN D; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM; INTRACELLULAR SPACE; ION CHANNELS; PLANT CELLS; PROTEIN TRANSPORT; VIRULENCE; VIRULENCE FACTORS;

EID: 85015451290     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1612098114     Document Type: Article

References (52)

1. Chilton MD, et al. (1977) Stable incorporation of plasmid DNA into higher plant cells: The molecular basis of crown gall tumorigenesis. Cell 11(2):263-271.
2. Zambryski P, et al. (1980) Tumor DNA structure in plant cells transformed by A. tumefaciens. Science 209(4463):1385-1391.
3. Albright LM, Yanofsky MF, Leroux B, Ma DQ, Nester EW (1987) Processing of the T-DNA of Agrobacterium tumefaciens generates border nicks and linear, singlestranded T-DNA. J Bacteriol 169(3):1046-1055.
4. Fronzes R, Christie PJ, Waksman G (2009) The structural biology of type IV secretion systems. Nat Rev Microbiol 7(10):703-714.
5. Bundock P, den Dulk-Ras A, Beijersbergen A, Hooykaas PJ (1995) Trans-kingdom T-DNA transfer from Agrobacterium tumefaciens to Saccharomyces cerevisiae. EMBO J 14(13):3206-3214.
6. Piers KL, Heath JD, Liang X, Stephens KM, Nester EW (1996) Agrobacterium tumefaciens- mediated transformation of yeast. Proc Natl Acad Sci USA 93(4):1613-1618.
7. de Groot MJ, Bundock P, Hooykaas PJ, Beijersbergen AG (1998) Agrobacterium tumefaciens- mediated transformation of filamentous fungi. Nat Biotechnol 16(9):839-842.
8. Kathiresan S, Chandrashekar A, Ravishankar GA, Sarada R (2009) Agrobacteriummediated transformation in the green alga Haematococcus pluvialis (Chlorophyceae, Volvocales). J Phycol 45(3):642-649.
9. Wang K, Herrera-Estrella L, Van Montagu M, Zambryski P (1984) Right 25 bp terminus sequence of the nopaline T-DNA is essential for and determines direction of DNA transfer from agrobacterium to the plant genome. Cell 38(2):455-462.
10. Yanofsky MF, et al. (1986) ThevirD operon of Agrobacterium tumefaciens encodes a site-specific endonuclease. Cell 47(3):471-477.
11. Herrera-Estrella A, Chen ZM, Van Montagu M, Wang K (1988) VirD proteins of Agrobacterium tumefaciens are required for the formation of a covalent DNA-protein complex at the 5' terminus of T-strand molecules. EMBO J 7(13):4055-4062.
12. Vergunst AC, et al. (2000) VirB/D4-dependent protein translocation from Agrobacterium into plant cells. Science 290(5493):979-982.
13. Schrammeijer B, den Dulk-Ras A, Vergunst AC, Jurado Jácome E, Hooykaas PJ (2003) Analysis of Vir protein translocation from Agrobacterium tumefaciens using Saccharomyces cerevisiae as a model: Evidence for transport of a novel effector protein VirE3. Nucleic Acids Res 31(3):860-868.
14. Vergunst AC, et al. (2005) Positive charge is an important feature of the C-terminal transport signal of the VirB/D4-translocated proteins of Agrobacterium. Proc Natl Acad Sci USA 102(3):832-837.
15. Engström P, Zambryski P, Van Montagu M, Stachel S (1987) Characterization of Agrobacterium tumefaciens virulence proteins induced by the plant factor acetosyringone. J Mol Biol 197(4):635-645.
16. Citovsky V, DE Vos G, Zambryski P (1988) Single-stranded DNA binding protein encoded by the virE locus of Agrobacterium tumefaciens. Science 240(4851):501-504.
17. Sen P, Pazour GJ, Anderson D, Das A (1989) Cooperative binding of Agrobacterium tumefaciens VirE2 protein to single-stranded DNA. J Bacteriol 171(5):2573-2580.
18. Citovsky V, Wong ML, Zambryski P (1989) Cooperative interaction of Agrobacterium VirE2 protein with single-stranded DNA: Implications for the T-DNA transfer process. Proc Natl Acad Sci USA 86(4):1193-1197.
19. Dym O, et al. (2008) Crystal structure of the Agrobacterium virulence complex VirE1- VirE2 reveals a flexible protein that can accommodate different partners. Proc Natl Acad Sci USA 105(32):11170-11175.
20. Citovsky V, Warnick D, Zambryski P (1994) Nuclear import of Agrobacterium VirD2 and VirE2 proteins in maize and tobacco. Proc Natl Acad Sci USA 91(8):3210-3214.
21. Citovsky V, Zupan J, Warnick D, Zambryski P (1992) Nuclear localization of Agrobacterium VirE2 protein in plant cells. Science 256(5065):1802-1805.
22. Gelvin SB (1998) Agrobacterium VirE2 proteins can form a complex with T strands in the plant cytoplasm. J Bacteriol 180(16):4300-4302.
23. Shi Y, Lee LY, Gelvin SB (2014) Is VIP1 important for Agrobacterium-mediated transformation? Plant J 79(5):848-860.
24. Li X, Yang Q, Tu H, Lim Z, Pan SQ (2014) Direct visualization of Agrobacteriumdelivered VirE2 in recipient cells. Plant J 77(3):487-495.
25. Luby-Phelps K (2000) Cytoarchitecture and physical properties of cytoplasm: Volume, viscosity, diffusion, intracellular surface area. Int Rev Cytol 192:189-221.
26. Tzfira T (2006) On tracks and locomotives: The long route of DNA to the nucleus. Trends Microbiol 14(2):61-63.
27. Tzfira T, Vaidya M, Citovsky V (2001) VIP1, an Arabidopsis protein that interacts with Agrobacterium VirE2, is involved in VirE2 nuclear import and Agrobacterium infectivity. EMBO J 20(13):3596-3607.
28. Djamei A, Pitzschke A, Nakagami H, Rajh I, Hirt H (2007) Trojan horse strategy in Agrobacterium transformation: Abusing MAPK defense signaling. Science 318(5849):453-456.
29. Salman H, et al. (2005) Nuclear localization signal peptides induce molecular delivery along microtubules. Biophys J 89(3):2134-2145.
30. Sakalis PA, van Heusden GP, Hooykaas PJ (2014) Visualization of VirE2 protein translocation by the Agrobacterium type IV secretion system into host cells. Microbiology Open 3(1):104-117.
31. Lawrence CJ, Morris NR, Meagher RB, Dawe RK (2001) Dyneins have run their course in plant lineage. Traffic 2(5):362-363.
32. Wasteneys GO (2002) Microtubule organization in the green kingdom: Chaos or selforder? J Cell Sci 115(pt 7):1345-1354.
33. Krucker T, Siggins GR, Halpain S (2000) Dynamic actin filaments are required for stable long-term potentiation (LTP) in area CA1 of the hippocampus. Proc Natl Acad Sci USA 97(12):6856-6861.
34. Misumi Y, et al. (1986) Novel blockade by Brefeldin A of intracellular transport of secretory proteins in cultured rat hepatocytes. J Biol Chem 261(24):11398-11403.
35. Skoufias DA, Wilson L (1992) Mechanism of inhibition of microtubule polymerization by colchicine: Inhibitory potencies of unliganded colchicine and tubulin-colchicine complexes. Biochemistry 31(3):738-746.
36. Nelson BK, Cai X, Nebenführ A (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 51(6):1126-1136.
37. Nakano RT, et al. (2009) GNOM-LIKE1/ERMO1 and SEC24a/ERMO2 are required for maintenance of endoplasmic reticulum morphology in Arabidopsis thaliana. Plant Cell 21(11):3672-3685.
38. Ueda H, et al. (2010) Myosin-dependent endoplasmic reticulum motility and F-actin organization in plant cells. Proc Natl Acad Sci USA 107(15):6894-6899.
39. Saitoh M, Ishikawa T, Matsushima S, Naka M, Hidaka H (1987) Selective inhibition of catalytic activity of smooth muscle myosin light chain kinase. J Biol Chem 262(16):7796-7801.
40. Avisar D, Prokhnevsky AI, Makarova KS, Koonin EV, Dolja VV (2008) Myosin XI-K is required for rapid trafficking of Golgi stacks, peroxisomes, and mitochondria in leaf cells of Nicotiana benthamiana. Plant Physiol 146(3):1098-1108.
41. Ward DV, Zambrysk iPC (2001) The six functions of Agrobacterium VirE2. Proc Natl Acad Sci USA 98(2):385-386.
42. Yokota E, Yukawa C, Muto S, Sonobe S, Shimmen T (1999) Biochemical and immunocytochemical characterization of two types of myosins in cultured tobacco bright yellow-2 cells. Plant Physiol 121(2):525-534.
43. Li JF, Nebenführ A (2007) Organelle targeting of myosin XI ismediated by two globular tail subdomains with separate cargo binding sites. J Biol Chem 282(28):20593-20602.
44. Peremyslov VV, et al. (2011) Expression, splicing, and evolution of the myosin gene family in plants. Plant Physiol 155(3):1191-1204.
45. Dumas F, Duckely M, Pelczar P, Van Gelder P, Hohn B (2001) An Agrobacterium VirE2 channel for transferred-DNA transport into plant cells. Proc Natl Acad Sci USA 98(2):485-490.
46. Lee LY, et al. (2012) Screening a cDNA library for protein-protein interactions directly in planta. Plant Cell 24(5):1746-1759.
47. Hwang HH, Gelvin SB (2004) Plant proteins that interact with VirB2, the Agrobacterium tumefaciens pilin protein, mediate plant transformation. Plant Cell 16(11):3148-3167.
48. Hood EE, Gelvin SB, Melchers LS, Hoekema A (1993) New Agrobacterium helper plasmids for gene transfer to plants. Transgenic Res 2(4):208-218.
49. Knauf VC, Nester EW (1982) Wide host range cloning vectors: A cosmid clone bank of an Agrobacterium Ti plasmid. Plasmid 8(1):45-54.
50. Xiang C, Han P, Lutziger I, Wang K, Oliver DJ (1999) A mini binary vector series for plant transformation. Plant Mol Biol 40(4):711-717.
51. Van Damme D, et al. (2004) In vivo dynamics and differential microtubule-binding activities of MAP65 proteins. Plant Physiol 136(4):3956-3967.
52. Chen PY, Wang CK, Soong SC, To KY (2003) Complete sequence of the binary vector pBI121 and its application in cloning T-DNA insertion from transgenic plants. Mol Breed 11(4):287-293.