Armet is an effector protein mediating aphid-plant interactions

FASEB Journal

Volumn 29, Issue 5, 2015, Pages 2032-2045

  Wang, Wei ^a,b   Dai, Huaien ^c   Zhang, Yi ^d   Chandrasekar, Raman ^c   Luo, Lan ^a   Hiromasa, Yasuaki ^c   Sheng, Changzhong ^c   Peng, Gongxin ^d   Chen, Shaoliang ^b   Tomich, John M ^c   Reese, John ^c   Edwards, Owain ^e   Kang, Le ^a   Reeck, Gerald ^c   Cui, Feng ^a,c  

^a INSTITUTE OF ZOOLOGY   (China)

^b BEIJING FORESTRY UNIVERSITY   (China)

^c KANSAS STATE UNIVERSITY   (United States)

^d HEBEI UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^e CSIRO   (Australia)

Author keywords

Calcium binding; Feeding behavior; MANF; Saliva protein; Salivary gland

Indexed keywords

INSECT PROTEIN; PROTEIN ARMET; UNCLASSIFIED DRUG; IMMUNOGLOBULIN G; MESSENGER RNA; SALIVA PROTEIN;

ARTICLE; ARTIFICIAL DIET; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; FEEDING BEHAVIOR; LIFESPAN; MOLECULAR EVOLUTION; NONHUMAN; PEA APHID; PHLOEM; PLANT INSECT INTERACTION; PRIORITY JOURNAL; PROTEIN SECRETION; RNA INTERFERENCE; SALIVARY GLAND; TOBACCO; VICIA FABA; AMINO ACID SEQUENCE; ANIMAL; APHID; CHEMISTRY; CIRCULAR DICHROISM; EATING; ENZYME IMMUNOASSAY; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; MASS SPECTROMETRY; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PARASITOLOGY; PHYSIOLOGY; RABBIT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SALIVA; SECRETION (PROCESS); WESTERN BLOTTING;

ACYRTHOSIPHON PISUM; APHIDIDAE; MAMMALIA; NICOTIANA TABACUM; VICIA FABA;

AMINO ACID SEQUENCE; ANIMALS; APHIDS; BASE SEQUENCE; BLOTTING, WESTERN; CIRCULAR DICHROISM; CLONING, MOLECULAR; EATING; ENDOPLASMIC RETICULUM STRESS; EVOLUTION, MOLECULAR; HOST-PATHOGEN INTERACTIONS; IMMUNOENZYME TECHNIQUES; IMMUNOGLOBULIN G; INSECT PROTEINS; MOLECULAR SEQUENCE DATA; RABBITS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SALIVA; SALIVARY PROTEINS AND PEPTIDES; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; VICIA FABA;

EID: 84924723291     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-266023     Document Type: Article

References (43)

1. Blackman, R. L., and Eastop, V. F. (1984) Aphids on the World's Crops: An Identification and Information Guide, John Wiley & Sons, New York
2. Tjallingii, W. F., and Esch, T. H. (1993) Fine structure of the stylet route in plant tissues by some aphids. Physiol. Entomol. 18, 317-328
3. Cherqui, A., and Tjallingii, W. F. (2000) Salivary proteins of aphids, a pilot study on identification, separation and immunolocalisation. J. Insect Physiol. 46, 1177-1186
4. Miles, P. W. (1999) Aphid saliva. Biol. Rev. Camb. Philos. Soc. 74, 41-85
5. Tjallingii, W. F. (2006) Salivary secretions by aphids interacting with proteins of phloem wound responses. J. Exp. Bot. 57, 739-745
6. 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
7. Jones, J. D. G., and Dangl, J. L. (2006) The plant immune system. Nature 444, 323-329
8. Hogenhout, S. A., Van Der Hoorn, R. A. L., Terauchi, R., and Kamoun, S. (2009) Emerging concepts in effector biology of plant-associated organisms. Mol. Plant Microbe Interact. 22, 115-122
9. Harmel, N., Létocart, 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
10. 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
11. Rao, S. A. K., Carolan, J. C., and Wilkinson, T. L. (2013) Proteomic profiling of cereal aphid saliva reveals both ubiquitous and adaptive secreted proteins. PLoS ONE 8, e57413
12. Cooper, W. R., Dillwith, J. W., and Puterka, G. J. (2010) Salivary proteins of Russian wheat aphid (Hemiptera: Aphididae). Environ. Entomol. 39, 223-231
13. 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. USA 105, 9965-9969
14. 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
15. 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
16. Pitino, M., Coleman, A. D., Maffei, M. E., Ridout, C. J., and Hogenhout, S. A. (2011) Silencing of aphid genes by dsRNA feeding from plants. PLoS ONE 6, e25709
17. 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
18. Guo, K., Wang, W., Luo, L., Chen, J., Guo, Y., and Cui, F. (2014) Characterization of an aphid-specific, cysteine-rich protein enriched in salivary glands. Biophys. Chem. 189, 25-32
19. Mizobuchi, N., Hoseki, J., Kubota, H., Toyokuni, S., Nozaki, J., Naitoh, M., Koizumi, A., and Nagata, K. (2007) ARMET is a soluble ER protein induced by the unfolded protein response via ERSE-II element. Cell Struct. Funct. 32, 41-50
20. Apostolou, A., Shen, Y., Liang, Y., Luo, J., and Fang, S. (2008) Armet, a UPR-upregulated protein, inhibits cell proliferation and ER stress-induced cell death. Exp. Cell Res. 314, 2454-2467
21. Petrova, P., Raibekas, A., Pevsner, J., Vigo, N., Anafi, M., Moore, M. K., Peaire, A. E., Shridhar, V., Smith, D. I., Kelly, J., Durocher, Y., and Commissiong, J. W. (2003) MANF: a new mesencephalic, astrocyte-derived neurotrophic factor with selectivity for dopaminergic neurons. J. Mol. Neurosci. 20, 173-188
22. Palgi, M., Lindström, R., Peränen, J., Piepponen, T. P., Saarma, M., and Heino, T. I. (2009) Evidence that DmMANF is an invertebrate neurotrophic factor supporting dopaminergic neurons. Proc. Natl. Acad. Sci. USA 106, 2429-2434
23. Lindholm, P., Voutilainen, M. H., Laurén, J., Peränen, J., Leppänen, V. M., Andressoo, J. O., Lindahl, M., Janhunen, S., Kalkkinen, N., Timmusk, T., Tuominen, R. K., and Saarma, M. (2007) Novel neurotrophic factor CDNF protects and rescues midbrain dopamine neurons in vivo. Nature 448, 73-77
24. Lindholm, P., Peränen, J., Andressoo, J. O., Kalkkinen, N., Kokaia, Z., Lindvall, O., Timmusk, T., and Saarma, M. (2008) MANF is widely expressed in mammalian tissues and differently regulated after ischemic and epileptic insults in rodent brain. Mol. Cell. Neurosci. 39, 356-371
25. Palgi, M., Greco, D., Lindström, R., Auvinen, P., and Heino, T. I. (2012) Gene expression analysis of Drosophila Manf mutants reveals perturbations in membrane traffic and major metabolic changes. BMC Genomics 13, 134
26. Will, T., Tjallingii, W. F., Thönnessen, A., and Van Bel, A. J. (2007) Molecular sabotage of plant defense by aphid saliva. Proc. Natl. Acad. Sci. USA 104, 10536-10541
27. Will, T., Kornemann, S. R., Furch, A. C., Tjallingii, W. F., and Van Bel, A. J. (2009) Aphid watery saliva counteracts sieve-tube occlusion: a universal phenomenon? J. Exp. Biol. 212, 3305-3312
28. Medina-Ortega, K. J., and Walker, G. P. (2013) Does aphid salivation affect phloem sieve element occlusion in vivo? J. Exp. Bot. 64, 5525-5535
29. Mutti, N. S., Park, Y., Reese, J. C., and Reeck, G. R. (2006) RNAi knockdown of a salivary transcript leading to lethality in the pea aphid, Acyrthosiphon pisum. J. Insect Sci. 6, 38
30. Akey, D. H., and Beck, S. D. (1971) Continuous rearing of the pea aphid, Acyrthosiphon pisum, on a holidic diet. Ann. Entomol. Soc. Am. 64, 353-356
31. Will, T., Steckbauer, K., Hardt, M., and Van Bel, A. J. E. (2012) Aphid gel saliva: sheath structure, protein composition and secretory dependence on stylet-tip milieu. PLoS ONE 7, e46903
32. Yoshida, H., Haze, K., Yanagi, H., Yura, T., and Mori, K. (1998) Identification of the cis-acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose-regulated proteins. Involvement of basic leucine zipper transcription factors. J. Biol. Chem. 273, 33741-33749
33. Hellens, R. P., Allan, A. C., Friel, E. N., Bolitho, K., Grafton, K., Templeton, M. D., Karunairetnam, S., Gleave, A. P., and Laing, W. A. (2005) Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods 1, 13
34. 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
35. Cao, H. H., Wang, S. H., and Liu, T. X. (2014) Jasmonate- and salicylate-induced defenses in wheat affect host preference and probing behavior but not performance of the grain aphid, Sitobion avenae. Insect Sci. 21, 47-55
36. Louis, J., and Shah, J. (2013) Arabidopsis thaliana-Myzus persicae interaction: shaping the understanding of plant defense against phloem-feeding aphids. Front. Plant Sci. 4, 213
37. Cooper, W. C., Jia, L., and Goggin, F. L. (2004) Acquired and R-gene-mediated resistance against the potato aphid in tomato. J. Chem. Ecol. 30, 2527-2542
38. Gao, L. L., Kamphuis, L. G., Kakar, K., Edwards, O. R., Udvardi, M. K., and Singh, K. B. (2010) Identification of potential early regulators of aphid resistance in Medicago truncatula via transcription factor analysis. New Phytol. 186, 980-994
39. 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
40. Giordanengo, P., Brunissen, L., Rusterucci, C., Vincent, C., Van Bel, A., Dinant, S., Girousse, C., Faucher, M., and Bonnemain, J.-L. (2010) Compatible plant-aphid interactions: how aphids manipulate plant responses. C. R. Biol. 333, 516-523
41. Parkash, V., Lindholm, P., Peränen, J., Kalkkinen, N., Oksanen, E., Saarma, M., Leppänen, V. M., and Goldman, A. (2009) The structure of the conserved neurotrophic factors MANF and CDNF explains why they are bifunctional. Protein Eng. Des. Sel. 22, 233-241
42. Hellman, M., Arumäe, U., Yu, L. Y., Lindholm, P., Peränen, J., Saarma, M., and Permi, P. (2011) Mesencephalic astrocytederived neurotrophic factor (MANF) has a unique mechanism to rescue apoptotic neurons. J. Biol. Chem. 286, 2675-2680
43. Hoseki, J., Sasakawa, H., Yamaguchi, Y., Maeda, M., Kubota, H., Kato, K., and Nagata, K. (2010) Solution structure and dynamics of mouse ARMET. FEBS Lett. 584, 1536-1542