ATP hydrolyzing salivary enzymes of caterpillars suppress plant defenses

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Wu, Shuang ^a,b   Peiffer, Michelle ^a   Luthe, Dawn S ^a   Felton, Gary W ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b SOUTHWEST UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

5' NUCLEOTIDASE; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATASE 13A1; APYRASE; ETHYLENE; HYDROLASE; JASMONIC ACID; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; UNCLASSIFIED DRUG;

ARTICLE; CATERPILLAR; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME REPRESSION; ENZYME STRUCTURE; GENE CONTROL; GENE REPRESSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT DEFENSE; PLANT GENE; PLANT LEAF; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SALIVARY GLAND; SEQUENCE ANALYSIS; TOMATO; TRICHOME;

ADENOSINE TRIPHOSPHATE; ANIMALS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HYDROLYSIS; LEPIDOPTERA; LYCOPERSICON ESCULENTUM; PLANT LEAVES; SALIVA; SEQUENCE ANALYSIS, DNA;

ARTHROPODA; ESCHERICHIA COLI; HELICOVERPA ZEA; LYCOPERSICON ESCULENTUM;

EID: 84864376665     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041947     Document Type: Article

References (54)

1. Mattiacci L, Dicke M, Posthumus MA, (1995) Beta-Glucosidase: an elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps. Proc Natl Acad Sci USA 92: 2036-2040.
2. Alborn HT, Turlings TCJ, Jones TH, Stenhagen G, Loughrin JH, et al. (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science 276: 945-949.
3. Alborn HT, Hansen TV, Jones TH, Bennett DC, Tumlinson JH, et al. (2007) Disulfooxy fatty acids from the American bird grasshopper Schistocerca americana, elicitors of plant volatiles. Proc Natl Acad Sci USA 104: 12976-12981.
4. Eichenseer H, Mathews MC, Bi JL, Murphy JB, Felton GW, (1999) Salivary glucose oxidase: multifunctional roles for Helicoverpa zea? Arch Insect Biochem Physiol 42: 99-109.
5. Halitschke R, Schittko U, Pohnert G, Boland W, Baldwin IT, (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. Plant Physiol 125: 711-717.
6. Korth KL, Dixon RA, (1997) Evidence for chewing insect-specific molecular events distinct from a general wound response in leaves. Plant Physiol 115: 1299-1305.
7. Musser RO, Hum-Musser SM, Eichenseer H, Peiffer M, Ervin G, et al. (2002) Herbivory: caterpillar saliva beats plant defences-A new weapon emerges in the evolutionary arms race between plants and herbivores. Nature 416: 599-600.
8. Felton GW, Eichenseer H, (1999) Herbivore saliva and its effects on plant defense against herbivores and pathogens. In: Agrawal AA, Tuzun S, Bent EH, editors. Induced Plant Defenses Against Pathogens and Herbivores Saint Paul The American Phytopathological Society pp. 19-36.
9. Schmelz EA, LeClere S, Carroll MJ, Alborn HT, Teal PEA, (2007) Cowpea chloroplastic ATP synthase is the source of multiple plant defense elicitors during insect herbivory. Plant Physiol 144: 793-805.
10. Tian D, Peiffer M, Shoemaker E, Tooker J, Haubruge E, et al. (2012) Salivary glucose oxidase from caterpillars mediates the induction of rapid and delayed-induced defenses in the tomato plant. PLoS One 7: e36168.
11. Musser RO, Cipollini DF, Hum-Musser SM, Williams SA, Brown JK, et al. (2005) Evidence that the caterpillar salivary enzyme glucose oxidase provides herbivore offense in solanaceous plants. Arch Insect Biochem Physiol 58: 128-137.
12. Diezel C, von Dahl CC, Gaquerel E, Baldwin IT, (2009) Different lepidopteran elicitors account for crosstalk in herbivory-induced phytohormone signaling. Plant Physiol 150: 1576-1586.
13. Hu YH, Leung DW, Kang L, Wang CZ, (2008) Diet factors responsible for the change of the glucose oxidase activity in labial salivary glands of Helicoverpa armigera. Arch Insect Biochem Physiol 68: 113-121.
14. Eichenseer H, Mathews MC, Powell JS, Felton GW, (2010) Survey of a salivary effector in caterpillars: glucose oxidase variation and correlation with host range. J Chem Ecol 36: 885-897.
15. Afshar K, Dufresne PJ, Pan L, Merkx-Jacques M, Bede JC, (2010) Diet-specific salivary gene expression and glucose oxidase activity in Spodoptera exigua (Lepidoptera: Noctuidae) larvae. J Insect Physiol 56: 1798-1806.
16. Zahoor Z, Davies AJ, Kirk RS, Rollinson D, Walker AJ, (2008) Disruption of ERK signalling in Biomphalaria glabrata defence cells by Schistosoma mansoni: implications for parasite survival in the snail host. Dev Comp Immunol 32: 1561-1571.
17. Zambrano-Villa S, Rosales-Borjas D, Carrero JC, Ortiz-Ortiz L, (2002) How protozoan parasites evade the immune response. Trends Parasitol 18: 272-278.
18. Faudry E, Lozzi SP, Santana JM, D'Souza-Ault M, Kieffer S, et al. (2004) Triatoma infestans apyrases belong to the 5′-nucleotidase family. J Biol Chem 279: 19607-19613.
19. Boisson B, Jacques JC, Choumet V, Martin E, Xu J, et al. (2006) Gene silencing in mosquito salivary glands by RNAi. FEBS Lett 580: 1988-1992.
20. Ribeiro JM, Sarkis JJ, Rossignol PA, Spielman A, (1984) Salivary apyrase of Aedes aegypti: characterization and secretory fate. Comp Biochem Physiol B 79: 81-86.
21. Thomas C, Rajagopal A, Windsor B, Dudler R, Lloyd A, et al. (2000) A role for ectophosphatase in xenobiotic resistance. Plant Cell 12: 519-533.
22. Roux SJ, Steinebrunner I, (2007) Extracellular ATP: an unexpected role as a signaler in plants. Trends Plant Sci 12: 522-527.
23. Kim SY, Sivaguru M, Stacey G, (2006) Extracellular ATP in plants. Visualization, localization, and analysis of physiological significance in growth and signaling. Plant Physiol 142: 984-992.
24. Jeter CR, Tang W, Henaff E, Butterfield T, Roux SJ, (2004) Evidence of a novel cell signalling role for extracellular adenosine triphosphates and diphosphates in Arabidopsis. Plant Cell 16: 2652-2664.
25. Chivasa S, Ndimba BK, Simon WJ, Lindsey K, Slabas AR, (2005) Extracellular ATP functions as an endogenous external metabolite regulating plant cell viability. Plant Cell 17: 3019-3034.
26. Steinebrunner I, Wu J, Sun Y, Corbett A, Roux SJ, (2003) Disruption of apyrases inhibits pollen germination in Arabidopsis. Plant Physiol 131: 1638-1647.
27. Tang W, Brady SR, Sun Y, Muday GK, Roux SJ, (2003) Extracellular ATP inhibits root gravitropism at concentrations that inhibit polar auxin transport. Plant Physiol 131: 147-154.
28. Wu J, Steinebrunner I, Sun Y, Butterfield T, Torres J, et al. (2007) Apyrases (nucleoside triphosphate-diphosphohydrolases) play a key role in growth control in Arabidopsis. Plant Physiol 144: 961-975.
29. Clark G, Torres J, Finlayson S, Guan X, Handley C, et al. (2010) Apyrase (nucleoside triphosphate-diphosphohydrolase) and extracellular nucleotides regulate cotton fiber elongation in cultured ovules. Plant Physiol 152: 1073-1083.
30. Chivasa S, Murphy AM, Hamilton JM, Lindsey K, Carr JP, et al. (2009) Extracellular ATP is a regulator of pathogen defence in plants. Plant J 60: 436-448.
31. Blobel G, (2000) Protein targeting (Nobel lecture). Chembiochem 1: 86-102.
32. Vidya CSS, Manoharan M, Sita GL, (1999) Cloning and characterization of salicylic acid-induced, intracellular pathogenesis-related gene from tomato (Lycopersicon esculentum). J Biosci 24: 287-293.
33. Wen PF, Chen JY, Kong WF, Pan QH, Wan SB, et al. (2005) Salicylic acid induced the expression of phenylalanine ammonia-lyase gene in grape berry. Plant Sci 169: 928-934.
34. Mueller MJ, Brodschelm W, Spannagl E, Zenk MH, (1993) Signaling in the elicitation process is mediated through the octadecanoid pathway leading to jasmonic acid. Proc Natl Acad Sci USA 90: 7490-7494.
35. Howe GA, Ryan CA, (1999) Suppressors of systemin signaling identify genes in the tomato wound response pathway. Genetics 153: 1411-1421.
36. Li L, Zhao Y, McCaig BC, Wingerd BA, Wang J, et al. (2004) The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell 16: 126-143.
37. Kang JH, Wang L, Giri A, Baldwin IT, (2006) Silencing threonine deaminase and JAR4 in Nicotiana attenuata impairs jasmonic acid-isoleucine-mediated defenses against Manduca sexta. Plant Cell 18: 3303-3320.
38. Adie B, Chico JM, Rubio-Somoza I, Solano R, (2007) Modulation of plant defenses by ethylene. J Plant Growth Regul 26: 160-177.
39. Nelson DE, Raghothama KG, Singh NK, Hasegawa PM, Bressan RA, (1992) Analysis of structure and transcriptional activation of an osmotin gene. Plant Mol Biol 19: 577-588.
40. Schmelz EA, Engelberth J, Alborn HT, Tumlinson JH 3rd, Teal PE, (2009) Phytohormone-based activity mapping of insect herbivore-produced elicitors. Proc Natl Acad Sci USA 106: 653-657.
41. Stinchcombe J, Bossi G, Griffiths GM, (2004) Linking albinism and immunity: the secrets of secretory lysosomes. Science 305: 55-59.
42. Zehe C, Engling A, Wegehingel S, Schäfer T, Nickel W, (2006) Cell-surface heparan sulfate proteoglycans are essential components of the unconventional export machinery of FGF-2. Proc Natl Acad Sci USA 103: 15479-15484.
43. Stoorvogel W, Kleijmeer MJ, Geuze HJ, Raposo G, (2002) The biogenesis and functions of exosomes. Traffic 3: 321-330.
44. Hughes RC, (1999) Secretion of the galectin family of mammalian carbohydrate-binding proteins. Biochim Biophys Acta 1473: 172-185.
45. Leon-Reyes A, Van der Does D, De Lange ES, Delker C, Wasternack C, et al. (2010) Salicylate-mediated suppression of jasmonate-responsive gene expression in Arabidopsis is targeted downstream of the jasmonate biosynthesis pathway. Planta 232: 1423-1432.
46. Koornneef A, Leon-Reyes A, Ritsema T, Verhage A, Den Otter FC, et al. (2008) Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol 147: 1358-1368.
47. Dalin P, Ågren J, Björkman C, Huttunen P, Kärkkäinen K, (2008) Leaf trichome formation and plant resistance to herbivory. In: Schaller A, editors. Induced Plant Resistance to Herbivory Heidelberg Springer pp. 89-105.
48. Clark G, Roux SJ, (2009) Extracellular nucleotides: Ancient signaling molecules. Plant Sci 177: 239-244.
49. Ribeiro JM, Francischetti IM, (2003) Role of arthropod saliva in blood feeding: sialome and post-sialome perspectives. Annu Rev Entomol 48: 73-88.
50. Chippendale GM, (1970) Metamorphic changes in fat body proteins of the southwestern corn borer, Diatraea grandiosella. J Insect Physiol 16: 1057-1068.
51. Wittig I, Schägger H, (2005) Advantages and limitations of clear-native PAGE. Proteomics 5: 4338-4346.
52. Terry ME, Bonner BA, (1980) An examination of centrifugation as a method of extracting an extracellular solution from peas, and its use for the study of indoleacetic acid-induced growth. Plant Physiol 66: 321-325.
53. Petersen TN, Brunak S, von Heijne G, Nielsen H, (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785-786.
54. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25: 402-408.