In planta expression or delivery of potato aphid macrosiphum euphorbiae effectors Me10 and Me23 enhances aphid fecundity

Molecular Plant-Microbe Interactions

Volumn 26, Issue 1, 2013, Pages 67-74

  Atamian, Hagop S ^a,b   Chaudhary, Ritu ^a,b   Cin, Valeriano Dal ^b   Bao, Ergude ^c   Girke, Thomas ^a,b   Kaloshian, Isgouhi ^a,b,d  

^a Genomics and Bioinformatics   (United States)

^b Department of Nematology ^*  (United States)

^c University of California Riverside   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INSECT PROTEIN; SIGNAL PEPTIDE; TRANSCRIPTOME;

AMINO ACID SEQUENCE; ANIMAL; ANTIBODY SPECIFICITY; APHID; ARTICLE; BIOASSAY; CHEMISTRY; FERTILITY; GENE EXPRESSION REGULATION; GENE LIBRARY; GENETICS; HIGH THROUGHPUT SEQUENCING; HOST PARASITE INTERACTION; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; NYMPH; PARASITOLOGY; PHYSIOLOGY; PLANT DISEASE; POTATO; PSEUDOMONAS SYRINGAE; SALIVARY GLAND; SEQUENCE ALIGNMENT; TOBACCO; TOMATO;

AMINO ACID SEQUENCE; ANIMALS; APHIDS; BIOLOGICAL ASSAY; CONSERVED SEQUENCE; FERTILITY; GENE EXPRESSION REGULATION; GENE LIBRARY; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HOST-PARASITE INTERACTIONS; INSECT PROTEINS; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; NYMPH; ORGAN SPECIFICITY; PLANT DISEASES; PROTEIN SORTING SIGNALS; PSEUDOMONAS SYRINGAE; SALIVARY GLANDS; SEQUENCE ALIGNMENT; SOLANUM TUBEROSUM; TOBACCO; TRANSCRIPTOME;

AGROBACTERIUM TUMEFACIENS; APHIDIDAE; LYCOPERSICON ESCULENTUM; MACROSIPHUM EUPHORBIAE; NICOTIANA BENTHAMIANA; PSEUDOMONAS SYRINGAE; SOLANUM TUBEROSUM;

EID: 84870974383     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-06-12-0144-FI     Document Type: Article

References (67)

1. Abramovitch, R. B., Anderson, J. C., and Martin, G. B. 2006. Bacterial elicitation and evasion of plant innate immunity. Nature Rev. Mol. Cell Biol. 7:601-611.
2. Atamian, H. S., and Kaloshian, I. 2012. Construction of RNA-Seq libraries from large and microscopic tissues for the Illumina sequencing platform. in: RNA Abundance Analysis, H. Jin and W. Gassmann, eds. Humana Press, Totowa. NJ, U.S.A.
3. Bao, E., Jiang, T., Kaloshian, I., and Girke, T. 2011. SEED: Efficient clustering of next-generation sequences. Bioinformatics 27:2502-2509p
4. BenMamoun, M. 2006. FPRANK: Stata module to compute Two-Sample Fligner-Policello Robust Rank Order Test. Statistical Software Components, S456739 Department of Economics, Boston College, Chestnut Hill, MA, U.S.A.
5. Bhattarai, K. K., Xie, Q.-G., Pourshalimi, D., Younglove, T., and Kaloshian, I. 2007. Coi1-dependent signaling pathway is not required for Mi-1-mediated potato aphid resistance. Mol. Plant-Microbe Interact. 20:276-282.
6. Birch, P. R., Rehmany, A. P., Pritchard, L., Kamoun, S., and Beynon, J. L. 2006. Trafficking arms: Oomycete effectors enter host plant cells. Trends Microbiol. 14:8-11.
7. Blackman, R. L., and Eastop, V. F. 2000. Aphids on the World's Crops. Wiley-Interscience, Chichester, U.K.
8. Bos, J. I., Prince, D., Pitino, M., Maffei, M. E., Win, J., and Hogenhout, S. A. 2010. A functional genomics approach identifies candidate effectors from the aphid species Myzus persicae (green peach aphid). PLoS Genet. 6:e1001216. Published online.
9. Buttner, D., and He, S. Y. 2009. Type III protein secretion in plant pathogenic bacteria. Plant Physiol. 150:1656-1664.
10. Carolan, J. C., Fitzroy, C. I., Ashton, P. D., Douglas, A. E., and Wilkinson, T. L. 2009. The secreted salivary proteome of the pea aphid Acyrthosiphon pisum characterised by mass spectrometry. Proteomics 9:2457-2467.
11. Carolan, J. C., Caragea, D., Reardon, K. T., Mutti, N. S., Dittmer, N., Pappan, K., Cui, F., Castaneto, M., Poulain, J., Dossat, C., Tagu, D., Reese, J. C., Reeck, G. R., Wilkinson, T. L., and Edwards, O. R. 2011. Predicted effector molecules in the salivary secretome of the pea aphid (Acyrthosiphon pisum): A dual transcriptomic/proteomic approach. J. Proteome Res. 10:1505-1518.
12. Cerato, C., Rongai, D., Borgatti, S., and Tamba, M. L. 1994. Study of the aphid populations and virus diseases on seed potato crops. Inf. Agrag. 50:67-72.
13. Chan, C. K., Forbes, A. R., and Raworth, D. A. 1991. Aphid-transmitted viruses and their vectors of the world. Agric. Can. Tech. Bull. 3E:1-216.
14. Cornelis, G. R., and Van Gijsegem, F. 2000. Assembly and function of type III secretory systems. Annu. Rev. Microbiol. 54:735-774.
15. Davis, E. L., Hussey, R. S., Mitchum, M. G., and Baum, T. J. 2008. Parasitism proteins in nematode-plant interactions. Curr. Opin. Plant Biol. 11:360-366.
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. De Vos, M., Van Oosten, V. R., Van Poecke, R. M. P., Van Pelt, J. A., Pozo, M. J., Mueller, M. J., Buchala, A. J., Metraux, J.-P., Van Loon, L. C., Dicke, M., and Pieterse, C. M. J. 2005. Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol. Plant-Microbe Interact. 18:923-937.
18. Earley, K. W., Haag, J. R., Pontes, O., Opper, K., Juehne, T., Song, K., and Pikaard, C. S. 2006. Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45:616-629p
19. Emanuelsson, O., Nielsen, H., Brunak, S., and von H eijne, G. 2000. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300:1005-1016.
20. Giordanengo, P., Brunissen, L., Rusterucci, C., Vincent, C., van Bel, A., Dinant, S., Girousse, C., Faucher, M., Bonnemain, J. L. 2010. Compatible plant-aphid interactions: How do aphids manipulate plant responses. C. R. Biol. 333:516-523.
21. Goodin, M. M., Zaitlin, D., Naidu, R. A., and Lommel, S. A. 2008. Nicotiana benthamiana: Its history and future as a model for plant-pathogen interactions. Mol. Plant-Microbe Interact. 21:1015-1026.
22. Gosset, V., Harmel, N., Gobel, C., Francis, F., Haubruge, E., Wathelet, J. P., du Jardin, P., Feussner, I., and Fauconnier, M. L. 2009. Attacks by a piercing-sucking insect (Myzus persicae Sultzer) or a chewing insect (Leptinotarsa decemlineata Say) on potato plants (Solanum tuberosum L.) induce differential changes in volatile compound release and oxylipin synthesis. J. Exp. Bot. 60:1231-1240.
23. Guttman, D. S., and Greenberg, J. T. 2001. Functional analysis of the Type III effectors AvrRpt2 and AvrRpm1 of Pseudomonas syringae with the use of a single-copy genomic integration system. Mol. Plant-Microbe Interact. 14:145-155.
24. Harmel, N., Letocart, E., Cherqui, A., Giordanengo, P., Mazzucchelli, G., Guillonneau, F., De Pauw, E., Haubruge, E., and Francis, F. 2008. Identification of aphid salivary proteins: A proteomic investigation of Myzus persicae. Insect Mol. Biol. 17:165-174.
25. Harris, M. O., Stuart, J. J., Mohan, M., Nair, S., Lamb, R. J., and Rohfritsch, O. 2003. Grasses and gall midges: Plant defense and insect adaptation. Annu. Rev. Entomol. 48:549-577.
26. Hogenhout, S. A., and Bos, J. I. 2011. Effector proteins that modulate plant-insect interactions. Curr. Opin. Plant Biol. 14:422-428.
27. Horne, I., Haritos, V. S., and Oakeshott, J. G. 2009. Comparative and functional genomics of lipases in holometabolous insects. Insect Biochem. Mol. Biol. 39:547-567.
28. International Aphid Genomics Consortium. 2010. Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biol. 8:e1000313. Published online.
29. Jones, J. D., and Dangl, J. L. 2006. The plant immune system. Nature 444:323-329p
30. Kaloshian, I., and Walling, L. L. 2005. Hemipterans as plant pathogens. Annu. Rev. Phytopathol. 43:491-521.
31. Kamoun, S. 2006. A catalogue of the effector secretome of plant pathogenic oomycetes. Annu. Rev. Phytopathol. 44:41-60.
32. Kempema, L. A., Cui, X., Holzer, F. M., and Walling, L. L. 2007. Arabidopsis transcriptome changes in response to phloem-feeding silverleaf whitefly nymphs. Similarities and distinctions in responses to aphids. Plant Physiol. 143:849-865.
33. 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. 49:1008-1019p
34. Lamb, C., and Dixon, R. A. 1997. The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:251-275.
35. Mantelin, S., Peng, H. C., Li, B., Atamian, H. S., Takken, F. L., and Kaloshian, I. 2011. The receptor-like kinase SlSERK1 is required for Mi-1-mediated resistance to potato aphids in tomato. Plant J. 67:459-471.
36. Margaritopoulos, J. T., Kasprowicz, L., Malloch, G. L., and Fenton, B. 2009. Tracking the global dispersal of a cosmopolitan insect pest, the peach potato aphid. BMC Ecol. 9:13.
37. Martinez de Ilarduya, O., Xie, Q., and Kaloshian, I. 2003. Aphid-induced defense responses in Mi-1-mediated compatible and incompatible tomato interactions. Mol. Plant-Microbe Interact. 16:699-708.
38. Miles, P. 1999. Aphid saliva. Biol. Rev. 74:41-85.
39. Moeller, F. W. 1973. The host plants of the potato aphid Macrosiphum euphorbiae and of closely related species. Wiss. Z. Univ. Rostock Math. Naturwiss. Reihe 22:1179-1184.
40. Moran, N. A. 1992. The evolution of aphid life cycles. Annu. Rev. Entomol. 37:321-348.
41. Moran, P. J., Cheng, Y., Cassell, J. L., and Thompson, G. A. 2002. Gene expression profiling of Arabidopsis thaliana in compatible plant-aphid interactions. Arch. Insect Biochem. Physiol. 51:182-203.
42. Mutti, N. S., Louis, J., Pappan, L. K., Pappan, K., Begum, K., Chen, M. S., Park, Y., Dittmer, N., Marshall, J., Reese, J. C., and Reeck, G. R. 2008. A protein from the salivary glands of the pea aphid, Acyrthosiphon pisum, is essential in feeding on a host plant. Proc. Natl. Acad. Sci. U.S.A. 105:9965-9969p
43. Nguyen, H. P., Chakravarthy, S., Velasquez, A. C., McLane, H. L., Zeng, L., Nakayashiki, H., Park, D.-H., Collmer, A., and Martin, G. B. 2010. Methods to study PAMP-triggered immunity using tomato and Nicotiana benthamiana. Mol. Plant-Microbe Interact. 23:991-999p
44. Petersen, T. N., Brunak, S., von Heijne, G., and Nielsen, H. 2011. SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nat. Methods 8:785-786.
45. Pollard, D. G. 1973. Plant penetration by feeding aphids (Hemiptera, Aphidoidea): A review. Bull. Entomol. Res. 62:631-714.
46. Ponsen, M. B. 1972. The site of potato leafroll virus multiplication in its vector, Myzus persicae: An anatomical study. Mededelingen Landbouwhogeschool Wageningen 72:1-147.
47. Price, D. R., Karley, A. J., Ashford, D. A., Isaacs, H. V., Pownall, M. E., Wilkinson, H. S., Gatehouse, J. A., and Douglas, A. E. 2007. Molecular characterisation of a candidate gut sucrase in the pea aphid, Acyrthosiphon pisum. Insect Biochem. Mol. Biol. 37:307-317.
48. Radcliffe, E. B., and Ragsdale, D. W. 2002. Aphid-transmitted Potato viruses: The Importance of Understanding Vector Biology. Am. J. Potato Res. 79:353-386.
49. Rentel, M. C., Leonelli, L., Dahlbeck, D., Zhao, B., and Staskawicz, B. J. 2008. Recognition of the Hyaloperonospora parasitica effector ATR13 triggers resistance against oomycete, bacterial, and viral pathogens. Proc. Natl. Acad. Sci. U.S.A. 105:1091-1096.
50. Rodriguez-Saona, C. R., Musser, R. O., Vogel, H., Hum-Musser, S. M., and Thaler, J. S. 2010. Molecular, biochemical, and organismal analyses of tomato plants simultaneously attacked by herbivores from two feeding guilds. J. Chem. Ecol. 36:1043-1057.
51. Rossi, M., Goggin, F. L., Milligan, S. B., Kaloshian, I., Ullman, D. E., and Williamson, V. M. 1998. The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc. Natl. Acad. Sci. U.S.A. 95:9750-9754.
52. Schulz, M. H., Zerbino, D. R., Vingron, M., and Birney, E. 2012. Oases: Robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics 28:1086-1092.
53. Segonzac, C., and Zipfel, C. 2011. Activation of plant pattern-recognition receptors by bacteria. Curr. Opin. Microbiol. 14:54-61.
54. Singh, R. P., and Boiteau, G. 1986. Reevaluation of the potato aphid, Macrosiphum euphorbiae (Thomas), as vector of potato virus Y. Am. Potato J. 63:335-340.
55. Singh, V., Louis, J., Ayre, B. G., Reese, J. C., Pegadaraju, V., and Shah, J. 2011. TREHALOSE PHOSPHATE SYNTHASE11-dependent trehalose metabolism promotes Arabidopsis thaliana defense against the phloemfeeding insect Myzus persicae. Plant J. 67:94-104.
56. Sohn, K. H., Lei, R., Nemri, A., and Jones, J. D. 2007. The downy mildew effector proteins ATR1 and ATR13 promote disease susceptibility in Arabidopsis thaliana. Plant Cell 19:4077-4090.
57. Thompson, G. A., and Goggin, F. L. 2006. Transcriptomics and functional genomics of plant defence induction by phloem-feeding insects. J. Exp. Bot. 57:755-766.
58. Tjallingii, W. F. 2006. Salivary secretions by aphids interacting with proteins of phloem wound responses. J. Exp. Bot. 57:739-745.
59. Tjallingii, W. F., and Hogen Esch, T. 1993. Fine structure of aphid stylet routes in plant tissues in correlation with EPG signals. Physiol. Entomol. 18:317-328.
60. van der Hoorn, R. A. 2008. Plant proteases: From phenotypes to molecular mechanisms. Annu. Rev. Plant Biol. 59:191-223.
61. Van Emden, H. F., and Harrington, R. 2007. Aphids As Crop Pests. Eds. CABI, Wallingford, U.K.
62. Von Dohlen, C. D., Rowe, C. A., and Heie, O. E. 2006. A test of morphological hypotheses for tribal and subtribal relationships of Aphidinae (Insecta: Hemiptera: Aphididae) using DNA sequences. Mol. Phylogenet. Evol. 38:316-329p
63. Weidemann, H. L. 1968. Zur morohologie der hauptspeicheldruse von Myzus persicae (Sulz.). Entomol. Exp. Appl. 11:450-454.
64. Will, T., Tjallingii, W. F., Thonnessen, A., and van Bel, A. J. 2007. Molecular sabotage of plant defense by aphid saliva. Proc. Natl. Acad. Sci. U.S.A. 104:10536-10541.
65. Wilson, A. C., Sternberg, L. S. L., and Hurley, K. B. 2011. Aphids alter host-plant nitrogen isotope fractionation. Proc. Natl. Acad. Sci. U.S.A. 108:10220-10224.
66. Zarate, S. I., Kempema, L. A., and Walling, L. L. 2007. Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol. 143:866-875.
67. Zhang, P., Zhu, X., Huang, F., Liu, Y., Zhang, J., Lu, Y., and Ruan, Y. 2011. Suppression of jasmonic acid-dependent defense in cotton plant by the mealybug Phenacoccus solenopsis. PLoS One 6:e22378. Published online.