The NIa-Pro protein of Turnip mosaic virus improves growth and reproduction of the aphid vector, Myzus persicae (green peach aphid)

Plant Journal

Volumn 77, Issue 4, 2014, Pages 653-663

  Casteel, Clare L ^a   Yang, Chunling ^b   Nanduri, Ananya C ^a   De Jong, Hannah N ^a   Whitham, Steven A ^b   Jander, Georg ^a  

^a United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

^b IOWA STATE UNIVERSITY   (United States)

Author keywords

aphid; Arabidopsis thaliana; mutualism; Myzus persicae; Nicotiana benthamiana; Pathogen; plant defense; plant insect interactions; Turnip mosaic virus; Vector

Indexed keywords

VIRUS PROTEIN;

ANIMAL; APHID; ARABIDOPSIS; ARABIDOPSIS THALIANA; ARTICLE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; METABOLISM; MYZUS PERSICAE; NICOTIANA BENTHAMIANA; PARASITOLOGY; PATHOGENESIS; PHLOEM; PHYSIOLOGY; PLANT DEFENSE; PLANT DISEASE; PLANT LEAF; PLANT-INSECT INTERACTIONS; POTYVIRUS; RAPESEED; REPRODUCTION; SYMBIOSIS; TOBACCO; TRANSGENIC PLANT; TURNIP MOSAIC VIRUS; VECTOR; VIROLOGY;

APHID; ARABIDOPSIS THALIANA; MUTUALISM; MYZUS PERSICAE; NICOTIANA BENTHAMIANA; PATHOGEN; PLANT DEFENSE; PLANT-INSECT INTERACTIONS; TURNIP MOSAIC VIRUS; VECTOR;

ANIMALS; APHIDS; ARABIDOPSIS; BRASSICA NAPUS; GENE EXPRESSION; GENE EXPRESSION REGULATION, PLANT; HOST-PARASITE INTERACTIONS; PHLOEM; PLANT DISEASES; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; POTYVIRUS; REPRODUCTION; TOBACCO; VIRAL PROTEINS;

EID: 84893864809     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12417     Document Type: Article

References (68)

1. Anindya, R., and, Savithri, H.S., (2004) Potyviral NIa proteinase, a proteinase with novel deoxyribonuclease activity. J. Biol. Chem. 279, 32159-32169. (Pubitemid 39014663)
2. Barth, C., and, Jander, G., (2006) Arabidopsis myrosinases TGG1 and TGG2 have redundant function in glucosinolate breakdown and insect defense. Plant J. 46, 549-562.
3. Beauchemin, C., Boutet, N., and, Laliberté, J.-F., (2007) Visualization of the interaction between the precursors of VPg, the viral protein linked to the genome of Turnip mosaic virus, and the translation eukaryotic initiation factor iso 4E in planta. J. Virol. 81, 775-782. (Pubitemid 46067903)
4. Belliure, B., Janssen, A., Maris, P.C., Peters, D., and, Sabelis, M.W., (2005) Herbivore arthropods benefit from vectoring plant viruses. Ecol. Lett. 8, 70-79. (Pubitemid 40172140)
5. Blanc, S., Uzest, M., and, Drucker, M., (2011) New research horizons in vector-transmission of plant viruses. Curr. Opin. Microbiol. 14, 483-491.
6. Bombarely, A., Rosli, H.G., Vrebalov, J., Moffett, P., Mueller, L.A., and, Martin, G.B., (2012) A draft genome sequence of Nicotiana benthamiana to enhance molecular plant-microbe biology research. Mol. Plant Microbe Interact. 25, 1523-1530.
7. Bosque-Perez, N.A., and, Eigenbrode, S.D., (2011) The influence of virus-induced changes in plants on aphid vectors: insights from luteovirus pathosystems. Virus Res. 159, 201-205.
8. Botha, C.E.J., and, Matsiliza, B., (2004) Reduction in transport in wheat (Triticum aestivum) is caused by sustained phloem feeding by the Russian wheat aphid (Diuraphis noxia). S. Afr. J. Bot. 70, 249-254. (Pubitemid 38995160)
9. Burgyan, J., and, Havelda, Z., (2011) Viral suppressors of RNA silencing. Trends Plant Sci. 16, 265-272.
10. Bush, J., Jander, G., and, Ausubel, F.M., (2006) Prevention and control of pests and diseases. In Arabidopsis Protocols, 2nd edn. (, Salinas, J., and, Sanchez-Serrano, J.J., eds). Totowa: Humana Press, pp. 13-25.
11. Chung, B.Y.-W., Miller, W.A., Atkins, J.F., and, Firth, A.E., (2008) An overlapping essential gene in the Potyviridae. Proc. Natl Acad. Sci. USA 105, 5897-5902. (Pubitemid 351758469)
12. Clay, N., Adio, A., Denoux, C., Jander, G., and, Ausubel, F., (2009) Glucosinolate metabolites required for an Arabidopsis innate immune response. Science, 323, 95-101.
13. Clough, S.J., and, Bent, A.F., (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
14. Csorba, T., Pantaleo, B., and, Burgyán, J., (2009) RNA silencing: an antiviral mechanism. In Advances in Virus Research (, Loebenstein, G., and, Carr, J.P., eds). The Netherlands: Elsevier, pp. 35-71.
15. Curtis, M.D., and, Grossniklaus, U., (2003) A Gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133, 462-469. (Pubitemid 37325657)
16. De Vos, M., and, Jander, G., (2009) Myzus persicae (green peach aphid) salivary components induce defence responses in Arabidopsis thaliana. Plant, Cell Environ. 32, 1548-1560.
17. Debarro, P.J., (1992) The role of temperature, photoperiod, crowding and plant-quality on the production of alate viviparous females of the bird cherry-oat aphid, Rhopalosiphum padi. Entomol. Exp. Appl. 65, 205-214.
18. Dreyer, D.L., and, Campbell, B.C., (1987) Chemical basis of host-plant resistance to aphids. Plant, Cell Environ. 10, 353-361.
19. Eigenbrode, S.D., Ding, H., Shiel, P., and, Berger, P.H., (2002) Volatiles from potato plants infected with potato leafroll virus attract and arrest the virus vector, Myzus persicae (Homoptera: Aphididae). Proc. R. Soc. Lond. B Biol. Sci. 269, 455-460. (Pubitemid 34264042)
20. Fraile, A., and, García-Arenal, F., (2010) The coevolution of plants and viruses: resistance and pathogenicity. In Advances in Virus Research (, Carr, J.P., and, Loebenstein, G., eds). The Netherlands: Elsevier, pp. 1-32.
21. Gray, S.M., and, Banerjee, N., (1999) Mechanisms of arthropod transmission of plant and animal viruses. Microbiol. Mol. Biol. Rev. 63, 128-148. (Pubitemid 29116089)
22. Hansen, A.K., and, Moran, N.A., (2011) Aphid genome expression reveals host-symbiont cooperation in the production of amino acids. Proc. Natl Acad. Sci. USA 108, 2849-2854.
23. Harvey, J.A., Witjes, L.M.A., Benkirane, M., Duyts, H., and, Wagenaar, R., (2007) Nutritional suitability and ecological relevance of Arabidopsis thaliana and Brassica oleracea as foodplants for the cabbage butterfly, Pieris rapae. Plant Ecol. 189, 117-126. (Pubitemid 46941003)
24. Hodge, S., and, Powell, G., (2008) Do plant viruses facilitate their aphid vectors by inducing symptoms that alter behavior and performance? Environ. Entomol. 37, 1573-1581.
25. Hodgson, C.J., (1981) Effects of infection with the cabbage black ringspot strain of turnip mosaic virus on turnip as a host to Myzus persicae and Brevicoryne brassicae. Ann. Appl. Biol. 98, 1-14.
26. Hoh, F., Uzest, M., Drucker, M., Plisson-Chastang, C., Bron, P., Blanc, S., and, Dumas, C., (2010) Structural insights into the molecular mechanisms of cauliflower mosaic virus transmission by its insect vector. J. Virol. 84, 4706-4713.
27. Hunt, E.J., Pritchard, J., Bennett, M.J., Zhu, X., Barrett, D.A., Allen, T., Bale, J., and, Newbury, H.J., (2006) The Arabidopsis thaliana/Myzus persicae model system demonstrates that a single gene can influence the interaction between a plant and a sap-feeding insect. Mol. Ecol. 15, 4203-4213. (Pubitemid 44607162)
28. Ingwell, L.L., Eigenbrode, S.D., and, Bosque-Perez, N.A., (2012) Plant viruses alter insect behavior to enhance their spread. Sci. Rep. 2, 578.
29. Kersch-Becker, M.F., and, Thaler, J.S., (2013) Virus strains differentially induce plant susceptibility to aphid vectors and chewing herbivores. Oecologia, DOI: 10.1007/s00442-013-2812-7. Epub ahead of print.
30. Kim, J.H., and, Jander, G., (2007) Myzus persicae (green peach aphid) feeding on Arabidopsis induces the formation of a deterrent indole glucosinolate. Plant J. 49, 1008-1019. (Pubitemid 46340693)
31. Koch, E., and, Slusarenko, A., (1990) Arabidopsis is susceptible to infection by a downy mildew fungus. Plant Cell, 2, 437-445. (Pubitemid 120029602)
32. Lam, H.M., Wong, P., Chan, H.K., Yam, K.M., Chen, L., Chow, C.M., and, Coruzzi, G.M., (2003) Overexpression of the ASN1 gene enhances nitrogen status in seeds of Arabidopsis. Plant Physiol. 132, 926-935. (Pubitemid 36715090)
33. Lellis, A.D., Kasschau, K.D., Whitham, S.A., and, Carrington, J.C., (2002) Loss-of-susceptibility mutants of Arabidopsis thaliana reveal an essential role for eIF(iso)4E during potyvirus infection. Curr. Biol. 12, 1046-1051. (Pubitemid 34703338)
34. Lemaitre, T., Gaufichon, L., Boutet-Mercey, S., Christ, A., and, Masclaux-Daubresse, C., (2008) Enzymatic and metabolic diagnostic of nitrogen deficiency in Arabidopsis thaliana Wassileskija accession. Plant Cell Physiol. 49, 1056-1065. (Pubitemid 351989692)
35. Lewsey, M.G., Murphy, A.M., Maclean, D., et al. (2010) Disruption of two defensive signaling pathways by a viral RNA silencing suppressor. Mol. Plant Microbe Interact. 23, 835-845.
36. Lohaus, G., Burba, M., and, Heldt, H.W., (1994) Comparison of the contents of sucrose and amino acids in the leaves, phloem sap and taproots of high and low sugar-producing hybrids of sugar beet (Beta vulgaris L.). J. Exp. Bot. 45, 1097-1101. (Pubitemid 2129281)
37. Macdonald, S.J., Lin, G.G., Russell, C.W., Thomas, G.H., and, Douglas, A.E., (2012) The central role of the host cell in symbiotic nitrogen metabolism. Proc. R. Soc. Lond. B Biol. Sci. 279, 2965-2973.
38. Martín Martín, A., Cabrera y Poch, H.L., Martínez Herrera, D., and, Ponz, F., (1999) Resistances to turnip mosaic potyvirus in Arabidopsis thaliana. Mol. Plant Microbe Interact. 12, 1016-1021. (Pubitemid 29506780)
39. Martiniere, A., Bak, A., Macia, J.L., et al. (2013) A virus responds instantly to the presence of the vector on the host and forms transmission morphs. eLife, 2, e00183.
40. Mauck, K.E., De Moraes, C.M., and, Mescher, M.C., (2010) Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts. Proc. Natl Acad. Sci. USA 107, 3600-3605.
41. Mauck, K., Bosque-Perez, N.A., Eigenbrode, S.D., De Moraes, C.M., and, Mescher, M.C., (2012) Transmission mechanisms shape pathogen effects on host-vector interactions: evidence from plant viruses. Funct. Ecol. 26, 1162-1175.
42. Mavankal, G., and, Rhoads, R.E., (1991) In vitro cleavage at or near the N-terminus of the helper component protein in the tobacco vein mottling virus polyprotein. Virology, 185, 721-731.
43. Meihls, L.N., Handrick, V., Glauser, G., et al. (2013) Natural variation in maize aphid resistance is associated with DIMBOA-Glc methyltransferase activity. Plant Cell, 25, 2341-2355.
44. Murashige, T., and, Skoog, F.A., (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15, 473-497.
45. Nakagawa, T., Suzuki, T., Murata, S., et al. (2007) Improved Gateway binary vectors: high-performance vectors for creation of fusion constructs in Transgenic analysis of plants. Biosci. Biotechnol. Biochem. 71, 2095-2100. (Pubitemid 350113146)
46. Ng, J.C.K., and, Perry, K.L., (2004) Transmission of plant viruses by aphid vectors. Mol. Plant Pathol. 5, 505-511. (Pubitemid 39219107)
47. Ngumbi, E., Eigenbrode, S.D., Bosque-Perez, N.A., Ding, H., and, Rodriguez, A., (2007) Myzus persicae is arrested more by blends than by individual compounds elevated in headspace of PLRV-infected potato. J. Chem. Ecol. 33, 1733-1747. (Pubitemid 47414538)
48. Pagan, I., Fraile, A., Fernandez-Fueyo, E., Montes, N., Alonso-Blanco, C., and, Garcia-Arenal, F., (2010) Arabidopsis thaliana as a model for the study of plant-virus co-evolution. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, 1983-1995.
49. Pfalz, M., Vogel, H., and, Kroymann, J., (2009) The gene controlling the indole glucosinolate modifier1 quantitative trait locus alters indole glucosinolate structures and aphid resistance in Arabidopsis. Plant Cell, 21, 985-999.
50. Pfalz, M., Mikkelsen, M.D., Bednarek, P., Olsen, C.E., Halkier, B.A., and, Kroymann, J., (2011) Metabolic engineering in Nicotiana benthamiana reveals key enzyme functions in Arabidopsis indole glucosinolate modification. Plant Cell, 23, 716-729.
51. Pruss, G.J., Lawrence, C.B., Bass, T., Li, Q.Q., Bowman, L.H., and, Vance, V., (2004) The potyviral suppressor of RNA silencing confers enhanced resistance to multiple pathogens. Virology, 320, 107-120. (Pubitemid 38296718)
52. Rajamäki, M.-L., and, Valkonen, J.P.T., (2009) Control of nuclear and nucleolar localization of nuclear inclusion protein a of picorna-like Potato virus A in Nicotiana Species. Plant Cell, 21, 2485-2502.
53. Riechmann, J.L., Laín, S., and, García, J.A., (1992) Highlights and prospects of potyvirus molecular biology. J. Gen. Virol. 73, 1-16.
54. Riens, B., Lohaus, G., Heineke, D., and, Heldt, H.W., (1991) Amino acid and sucrose content determined in the cytosolic, chloroplastic, and vacuolar compartments and in the phloem sap of spinach leaves. Plant Physiol. 97, 227-233. (Pubitemid 21914208)
55. Roth, B.M., Pruss, G.J., and, Vance, V.B., (2004) Plant viral suppressors of RNA silencing. Virus Res. 102, 97-108. (Pubitemid 38447254)
56. Sambrook, J., Fritsch, E.F., and, Maniatis, T., (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory.
57. Sanchez, F., Martinez-Herrera, D., Aguilar, I., and, Ponz, F., (1998) Infectivity of turnip mosaic potyvirus cDNA clones and transcripts on the systemic host Arabidopsis thaliana and local lesion hosts. Virus Res. 55, 207-219. (Pubitemid 28345175)
58. Schaad, M.C., Haldeman-Cahill, R., Cronin, S., and, Carrington, J.C., (1996) Analysis of the VPg-proteinase (NIa) encoded by tobacco etch potyvirus: effects of mutations on subcellular transport, proteolytic processing, and genome amplification. J. Virol. 70, 7039-7048. (Pubitemid 26307418)
59. Shattuck, V.I., (1992) The biology, epidemiology, and control of turnip mosaic virus. Horticult. Rev. 14, 199-238.
60. Sisterson, M.S., (2008) Effects of insect-vector preference for healthy or infected plants on pathogen spread: insights from a model. J. Econ. Entomol. 101, 1-8. (Pubitemid 351299670)
61. Tomlinson, J.A., (1987) Epidemiology and control of virus diseases of vegetables. Ann. Appl. Biol. 110, 661-681.
62. Verchot, J., Koonin, E.V., and, Carrington, J.C., (1991) The 35-kDa protein from the N-terminus of the potyviral polyprotein functions as a third virus-encoded proteinase. Virology, 185, 527-535.
63. Walling, L.L., (2000) The myriad plant responses to herbivores. J. Plant Growth Regul. 19, 195-216.
64. Walsh, J.A., and, Jenner, C.E., (2002) Turnip mosaic virus and the quest for durable resistance. Mol. Plant Pathol. 3, 289-300.
65. Werner, B.J., Mowry, T.M., Bosque-Perez, N.A., Ding, H., and, Eigenbrode, S.D., (2009) Changes in green peach aphid responses to potato leafroll virus-induced volatiles emitted during disease progression. Environ. Entomol. 38, 1429-1438.
66. Winter, H., Lohaus, G., and, Heldt, H.W., (1992) Phloem transport of amino acids in relation to their cytosolic levels in barley leaves. Plant Physiol. 99, 996-1004.
67. Zhang, T., Luan, J.B., Qi, J.F., Huang, C.J., Li, M., Zhou, X.P., and, Liu, S.S., (2012) Begomovirus-whitefly mutualism is achieved through repression of plant defences by a virus pathogenicity factor. Mol. Ecol. 21, 1294-1304.
68. Ziebell, H., Murphy, A.M., Groen, S.C., et al. (2011) Cucumber mosaic virus and its 2b RNA silencing suppressor modify plant-aphid interactions in tobacco. Sci. Rep. 1, 187.