Mp10 and Mp42 from the aphid species myzus persicae trigger plant defenses in nicotiana benthamiana through different activities

Molecular Plant-Microbe Interactions

Volumn 27, Issue 1, 2014, Pages 30-39

  Rodriguez, Patricia A ^a,b   Stam, Remco ^a,b,c   Warbroek, Tim ^a,b   Bos, Jorunn I B ^a,b  

^a Cell and Molecular Sciences   (United Kingdom)

^b SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; INSECT PROTEIN;

AGROBACTERIUM; ANIMAL; APHID; ARTICLE; CONFOCAL MICROSCOPY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETIC MARKER; GENETIC TRANSCRIPTION; GENETICS; HOST PARASITE INTERACTION; IMMUNOLOGY; METABOLISM; PARASITOLOGY; PHYSIOLOGY; PLANT DISEASE; PLANT IMMUNITY; PLANT LEAF; REAL TIME POLYMERASE CHAIN REACTION; TOBACCO;

AGROBACTERIUM; ANIMALS; APHIDS; GENE EXPRESSION REGULATION, PLANT; GENETIC MARKERS; HOST-PARASITE INTERACTIONS; INSECT PROTEINS; MICROSCOPY, CONFOCAL; PLANT DISEASES; PLANT IMMUNITY; PLANT LEAVES; REAL-TIME POLYMERASE CHAIN REACTION; RECOMBINANT FUSION PROTEINS; TOBACCO; TRANSCRIPTION, GENETIC;

EID: 84890500695     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-05-13-0156-R     Document Type: Article

References (43)

1. Alvarez, A. E., Broglia, V. G., Alberti D'Amato, A. M., Wouters, D., van der Vossen, E., Garzo, E., Tjallingii, W. F., Dicke, M., and Vosman, B. 2012. Comparative analysis of Solanum stoloniferum responses to probing by the green peach aphid Myzus persicae and the potato aphid Macrosiphum euphorbiae. Insect Sci. 00:1-21.
2. Atamian, H. S., Chaudhary, R., Cin, V. D., Bao, E., Girke, T., and Kaloshian, I. 2013. In planta expression or delivery of potato aphid Macrosiphum euphorbiae effectors Me10 and Me23 enhances aphid fecundity. Mol. Plant-Microbe Interact. 26:67-74.
3. Blackman, R. L., and Eastop, V. F. 2006. Aphids on the World's Herbaceous Plants and Shrubs. John Wiley & Sons, New York.
4. Bos, J. I. B., 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.
5. Caillaud, M. C., Piquerez, S. J. M., and Jones, J. D. G. 2012. Characterization of the membrane-associated HaRxL17 Hpa effector candidate. Plant Signal. Behav. 7:145-149.
6. Carolan, J. C., Fitzroy, C. I. J., 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.
7. 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.
8. Cooper, W. C., Jia, L., and Goggin, F. L. 2004. Acquired and R-genemediated resistance against the potato aphid in tomato. J. Chem. Ecol. 30:2527-2542.
9. Cunnac, S., Lindeberg, M., and Collmer, A. 2009. Pseudomonas syringae type III secretion system effectors: repertoires in search of functions. Curr. Opin. Microbiol. 12:53-60.
10. Denecke, J., De Rycke, R., and Botterman, J. 1992. Plant and mammalian sorting signals for protein retention in the endoplasmic reticulum contain a conserved epitope. EMBO (Eur. Mol. Biol. Organ.) J. 11:2345-2355.
11. 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.
12. de Vos, M., Van Oosten, V. R., Van Poecke, R. M., Van Pelt, J. A., Pozo, M. J., Mueller, M. J., Buchala, A. J., Métraux, J. P., Van Loon, L. C., Dicke, M., Pieterse, C. M. 2005. Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol. Plant-Microbe Interact. 18:923-937.
13. de Vos, M., Kim, J. H., and Jander, G. 2007. Biochemistry and molecular biology of Arabidopsis-aphid interactions. Bioessays 29:871-883.
14. Ellis, C., Karafyllidis, I., and Turner, J. G. 2002. Constitutive activation of jasmonate signaling in an Arabidopsis mutant correlates with enhanced resistance to Erysiphe cichoracearum, Pseudomonas syringae, and Myzus persicae. Mol. Plant-Microbe Interact. 15:1025-1030.
15. Giska, F., Lichocka, M., Piechocki, M., Dadlez, M., Schmelzer, E., Hennig, J., and Krzymowska, M. 2013. Phosphorylation of HopQ1, a type III effector from Pseudomonas syringae, creates a binding site for host 14-3-3 proteins. Plant Physiol. 161:2049-2061.
16. Hogenhout, S. A., and Bos, J. I. B. 2011. Effector proteins that modulate plant-insect interactions. Curr. Opin. Plant Biol. 14:422-428.
17. The International Aphid Genomics Consortium. 2010. Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biol. 8:e1000313. Published online.
18. Jones, J. D. G., and Dangl, J. L. 2006. The plant immune system. Nature 444:323-329.
19. Karimi, M., Inzé, D., and Depicker, A. 2002. GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7:193-195.
20. Kerchev, P. I., Karpinska, B., Morris, J. A., Hussain, A., Verrall, S. R., Hedley, P. E., Fenton, B., Foyer, C. H., and Hancock, R. D. 2013. Vitamin C and the abscisic acid-insensitive 4 (ABI4) transcription factor are important determinants of aphid resistance in Arabidopsis. Antiox. Redox Signal. 18:2091-2105.
21. Maimbo, M., Ohnishi, K., Hikichi, Y., Yoshioka, H., and Kiba, A. 2010. S-glycoprotein-like protein regulates defense responses in Nicotiana plants against Ralstonia solanacearum. Plant Physiol. 152:2023-2035.
22. Mewis, I., Appel, H. M., Hom, A., Raina, R., and Schultz, J. C. 2005. Major signaling pathways modulate Arabidopsis glucosinolate accumulation and response to both phloem-feeding and chewing insects. Plant Physiol. 138:1149-1162.
23. Milling, A., Babujee, L., and Allen, C., 2011. Ralstonia solanacearum extracellular polysaccharide is a specific elicitor of defense responses in wilt-resistant tomato plants. PLoS One 6:e15853. Published online.
24. Moran, P. J., and Thompson, G. A. 2001. Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiol. 125:1074-1085.
25. 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.SA. 105:9965-9969.
26. Nakagawa, T., Kurose, T., Hino, T., Tanaka, K., Kawamukai, M., Niwa, Y., Toyooka, K., Matsuoka, K., Jinbo, T., and Kimura, T. 2007. Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J. Biosci. Bioeng. 104:34-41.
27. Nicholson, S. J., Hartson, S. D., and Puterka, G. J. 2012. Proteomic analysis of secreted saliva from Russian Wheat Aphid (Diuraphis noxia Kurd.) biotypes that differ in virulence to wheat. J. Proteom. 75:2252-2268.
28. Pegadaraju, V., Knepper, C., Reese, J., and Shah, J. 2005. Premature leaf senescence modulated by the Arabidopsis PHYTOALEXIN DEFICIENT4 gene is associated with defense against the phloem-feeding green peach aphid. Plant Physiol. 139:1927-1934.
29. Pegadaraju, V., Louis, J., Singh, V., Reese, J. C., Bautor, J., Feys, B. J., Cook, G., Parker, J. E., and Shah, J. 2007. Phloem-based resistance to green peach aphid is controlled by Arabidopsis PHYTOALEXIN DEFI CIENT4 without its signaling partner ENHANCED DISEASE SUSCEPTIBILITY1. Plant J. 52:332-341.
30. Pieterse, C. M. J., Leon-Reyes, A., Van der Ent, S., and Van Wees, S. C. M. 2009. Networking by small-molecule hormones in plant immunity. Nat. Chem. Biol. 5:308-316.
31. Pitino, M., and Hogenhout, S. A. 2013. Aphid protein effectors promote aphid colonization in a plant species-specific manner. Mol. Plant-Microbe Interact. 26:130-139.
32. Ramsey, J. S., Wilson, A. C. C., de Vos, M., Sun, Q., Tamborindeguy, C., Winfield, A., Malloch, G., Smith, D. M., Fenton, B., Gray, S. M., and Jander, G. 2007. Genomic resources for Myzus persicae: EST sequencing, SNP identification, and microarray design. BMC Genomics 8:423.
33. Rico, A., Bennett, M. H., Forcat, S., Huang, W. E., and Preston, G. M. 2010. Agroinfiltration reduces ABA levels and suppresses Pseudomonas syringae-elicited salicylic acid production in Nicotiana tabacum. PLoS One 5:e8977. Published online. Rodriguez, P. A., and Bos, J. I. B. 2013. Toward understanding the role of aphid effectors in plant infestation. Mol. Plant-Microbe Interact. 26:25-30.
34. Stam, R., Jupe, J., Howden, A. J. M., Morris, J. A., Boevink, P. C., Hedley, P. E., and Huitema, E. 2013. Identification and characterisation of CRN effectors in Phytophthora capsici shows modularity and functional diversity. PLoS One 8:e59517. Published online.
35. Tjallingii, W. F. 2006. Salivary secretions by aphids interacting with proteins of phloem wound responses. J. Exp. Bot. 57:739-745.
36. Tsuda, K., Sato, M., Glazebrook, J., Cohen, J. D., and Katagiri, F. 2008. Interplay between MAMP-triggered and SA-mediated defense responses. Plant J. 53:763-775.
37. Tsuda, K., Sato, M., Stoddard, T., Glazebrook, J., and Katagiri, F. 2009. Network properties of robust immunity in plants. PLoS Genet. 5:e1000772. Published online.
38. Van Damme, M., Bozkurt, T. O., Cakir, C., Schornack, S., Sklenar, J., Jones, A. M. E., and Kamoun, S. 2012. The Irish potato famine pathogen Phytophthora infestans translocates the CRN8 kinase into host plant cells. PLoS Pathog. 8:e1002875. Published online.
39. Vida, T. A., and Emr, S. D. 1995. A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J. Cell Biol. 128:779-792.
40. Will, T., Tjallingii, W. F., Thönnessen, A., and Van Bel, A. J. E. 2007. Molecular sabotage of plant defense by aphid saliva. Proc. Natl. Acad. Sci. U.SA. 104:10536-10541.
41. Yoon, J., Chung, W. I., and Doi, D. 2009. NbHB1, Nicotiana benthamiana homeobox 1, is a jasmonic acid-dependent positive regulator of pathogen-induced plant cell death. New Phytol. 184:71-84.
42. Yu, X., Tang, J., Wang, Q., Ye, W., Tao, K., Duan, S., Lu, C., Yang, X., Dong, S., Zheng, X., and Wang, Y. 2012. The RxLR effector Avh241 from Phytophthora sojae requires plasma membrane localization to induce plant cell death. New Phytol. 196:247-260.
43. Zipfel, C., Robatzek, S., Navarro, L., Oakeley, E. J., Jones, J. D. G., Felix, G., and Boller, T. 2004. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764-767.