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PLOS ONE  2014 

Analysis of the Salivary Gland Transcriptome of Frankliniella occidentalis

DOI: 10.1371/journal.pone.0094447

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Abstract:

Saliva is known to play a crucial role in insect feeding behavior and virus transmission. Currently, little is known about the salivary glands and saliva of thrips, despite the fact that Frankliniella occidentalis (Pergande) (the western flower thrips) is a serious pest due to its destructive feeding, wide host range, and transmission of tospoviruses. As a first step towards characterizing thrips salivary gland functions, we sequenced the transcriptome of the primary salivary glands of F. occidentalis using short read sequencing (Illumina) technology. A de novo-assembled transcriptome revealed 31,392 high quality contigs with an average size of 605 bp. A total of 12,166 contigs had significant BLASTx or tBLASTx hits (E≤1.0E?6) to known proteins, whereas a high percentage (61.24%) of contigs had no apparent protein or nucleotide hits. Comparison of the F. occidentalis salivary gland transcriptome (sialotranscriptome) against a published F. occidentalis full body transcriptome assembled from Roche-454 reads revealed several contigs with putative annotations associated with salivary gland functions. KEGG pathway analysis of the sialotranscriptome revealed that the majority (18 out of the top 20 predicted KEGG pathways) of the salivary gland contig sequences match proteins involved in metabolism. We identified several genes likely to be involved in detoxification and inhibition of plant defense responses including aldehyde dehydrogenase, metalloprotease, glucose oxidase, glucose dehydrogenase, and regucalcin. We also identified several genes that may play a role in the extra-oral digestion of plant structural tissues including β-glucosidase and pectin lyase; and the extra-oral digestion of sugars, including α-amylase, maltase, sucrase, and α-glucosidase. This is the first analysis of a sialotranscriptome for any Thysanopteran species and it provides a foundational tool to further our understanding of how thrips interact with their plant hosts and the viruses they transmit.

References

[1]  Musser RO, Hum-Musser SM, Eichenseer H, Peiffer M, Ervin G, et al. (2002) Herbivory: caterpillar saliva beats plant defences. Nature 416: 599–600. doi: 10.1038/416599a
[2]  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. doi: 10.1007/s10886-010-9830-2
[3]  Will T, Tjallingii WF, Thonnessen A, van Bel AJ (2007) Molecular sabotage of plant defense by aphid saliva. Proc Natl Acad Sci U S A 104: 10536–10541. doi: 10.1073/pnas.0703535104
[4]  Will T, van Bel AJE (2006) Physical and chemical interactions between aphids and plants. J Exp Bot 57: 729–737. doi: 10.1093/jxb/erj089
[5]  de la Paz Celorio-Mancera M, Greve LC, Teuber LR, Labavitch JM (2009) Identificantion of endo- and exo- polygalacturonase activity in Lygus hesperus (Knight) salivary glands. Arch Insect Biochem Physiol 70: 122–135. doi: 10.1002/arch.20282
[6]  Shackel KA, de la Paz Celorio-Mancera M, Ahmadi H, Greve LC, Teuber LR, et al. (2005) Micro-injection of Lygus salivary gland proteins to simulate feeding damage in alfalfa and cotton flowers. Arch Insect Biochem Physiol 58: 69–83. doi: 10.1002/arch.20033
[7]  Mutti NS, Park Y, Reese JC, Reek GR (2006) RNAi knockdown of a salivary transcript leading to lethality in the pea aphid, Acyrthosiphon pisum. J Insect Sci 6: 38. doi: 10.1673/031.006.3801
[8]  Plyusnin A, Beaty BJ, Elliott RM, Goldbach R, Kormelink R, et al. (2012) Family - Bunyaviridae In: King AMQ, Lefkowitz E, Adams MJ, Carstens EB, editors. Ninth Report of the International Committee on Taxonomy of Viruses. San Diego: Elsevier. pp. 725–741.
[9]  Rotenberg D, Krishna Kumar NK, Ullman DE, Montero-Astua M, Willis DK, et al. (2009) Variation in Tomato spotted wilt virus titer in Frankliniella occidentalis and its association with frequency of transmission. Phytopathology 99: 404–410. doi: 10.1094/phyto-99-4-0404
[10]  van de Wetering F, Hulshof J, Posthuma K, Harrewijn P, Goldbach R, et al. (1998) Distinct feeding behavior between sexes of Frankliniella occidentalis results in higher scar production and lower tospovirus transmission by females. Entomol Exp et App 88: 9–15. doi: 10.1046/j.1570-7458.1998.00340.x
[11]  van de Wetering F, van der Hoek M, Goldbach R, Peters D (1999) Differences in Tomato spotted wilt virus vector competency between males and females of Frankliniella occidentalis. Entomol Exp et App 93: 105–112. doi: 10.1046/j.1570-7458.1999.00567.x
[12]  Stafford CA, Walker GP, Ullman DE (2011) Infection with a plant virus modifies vector feeding behavior Proc Natl Acad Sci U S A. 108: 9350–9355. doi: 10.1073/pnas.1100773108
[13]  Kindt F, Joosten NN, Peters D, Tjallingii WF (2003) Characterization of the feeding behaviour of western flower thrips in terms of electrical penetration graph (EPG) waveforms. J Insect Physiol 49: 183–191. doi: 10.1016/s0022-1910(02)00255-x
[14]  Harrewijn P, Tjallingii WF, Mollema C (1996) Electrical recording of plant penetration by western flower thrips. Entomol Exp et App 79: 345–353. doi: 10.1111/j.1570-7458.1996.tb00842.x
[15]  Kumar NKK, Ullman DE, Cho JJ (1995) Resistance among Lycopersicon species to Frankliniella occidentalis (Thysanoptera: Thripidae). J Econ Entomol 88: 1057–1065.
[16]  Kirk WDJ (1997) Feeding. In: Lewis T, editor. Thrips as crop pests. Walingford, UK: CAB International. pp. 119–174.
[17]  Heming BS (1978) Structure and function of the mouthparts in larvae of Haplothrips verbasci (Osborn) (Thysanoptera; Tubulifera; Phlaeothripidae). J Morphol 156: 1–38. doi: 10.1002/jmor.1051560102
[18]  Childers CC, Achor DS (1991) Feeding and oviposition injury to 'Navel' orange flowers and developing buds by Frankliniella bispinosa (Thysanoptera: Thripidae) in Florida. Ann Entomol Soc Am 84.
[19]  Mitchell FL, Lowry VK, Kresta KK, Smith JW (1995) Histological study of tobacco thrips feeding on peanut foliage. In: Parker BL, Skinner M, Lewis T, editors. Thrips Biology and Management. New York, NY: Plenum Press. pp. 175–178.
[20]  Del Bene G, Dallai R, Marchini D (1991) Ultrastructure of the midgut and the adhering tubular salivary glands of Frankliniella occidentalis (Pergande) (Thysanopthera: Thripidae). Int J Insect Morphol Embryol 20: 12–15. doi: 10.1016/0020-7322(91)90024-4
[21]  Del Bene G, Cavallo V, Lupetti P, Dallai R (1999) Fine structure of the salivary glands of Heliothrips haemorrhoidalis (Bouche) (Thysanoptera: Thripidae). Int J Insect Morphol Embryol 28: 301–308. doi: 10.1016/s0020-7322(99)00033-1
[22]  Nagata T, Inoue-Nagata AK, Van Lent J, Goldbach R, Peters D (2002) Factors determining vector competence and specificity for transmission of Tomato spotted wilt virus. J Gen Virol 83: 663–671.
[23]  Nagata T, Inoue-Nagata AK, Smid HM, Goldbach R, Peters D (1999) Tissue tropism related to vector competence of Frankliniella occidentalis for tomato spotted wilt tospovirus. J Gen Virol 80.
[24]  Ullman D, Westcot D, Hunter W, Mau R (1989) Internal anatomy and morphology of Frankliniella occidentalis (Pergande) (Thysanopthera: Thripidae) with special reference to interactions between thrips and Tomato spotted wilt virus. Int J Insect Morphol Embryol: 289–310.
[25]  Montero-Astua M (2012) Unveiling and blocking the interaction between Tomato spotted wilt virus and its insect vector, Frankliniella occidentalis [Dissertation]: Kansas State. 163 p.
[26]  Ullman DE, Sherwood JL, German TL, Westcot DM, Chenault KD, et al. (1993) Location and composition of cytoplasmic inclusions in thrips cells infected with tomato spotted wilt tospovirus (TSWV). Phytopathology 83: 1374.
[27]  Arca B, Lombardo F, Valenzuela JG, Francischetti IM, Marinotti O, et al. (2006) An updated catalogue of salivary gland transcripts in the adult female mosquito, Anopheles gambiae. J Exp Biol 208: 3971–3986. doi: 10.1242/jeb.01849
[28]  Francischetti IM, Valenzuela JG, Pham VM, Garfield MK, Ribeiro JM (2002) Toward a catalog for the transcripts and proteins (sialome) from the salivary gland of the malaria vector Anopheles gambiae. J Exp Biol 205: 2429–2451.
[29]  Ribeiro JM, Arca B, Lombardo F, Calvo E, Pham VM, et al. (2007) An annotated catalogue of salivary gland transcripts in the adult female mosquito, Aedes aegypti. BMC Genomics 8: 6.
[30]  Arca B, Lombardo F, Francischetti IM, Pham VM, Mestres-Simon M, et al. (2007) An insight into the sialome of the adult female mosquito Aedes albopictus. Insect Biochem Mol Biol 37: 107–127. doi: 10.1016/j.ibmb.2006.10.007
[31]  Andersen JF, Pham VM, Meng Z, Champagne DE, Ribeiro JM (2009) An insight into the sialome of the black fly, Simulium vittatum. J Proteome Res 8: 1474–1488. doi: 10.1021/pr8008429
[32]  Assumpc?o TCF, Francischetti IMB, Andersen JF, Schwarz A, Santana JM, et al. (2008) An insight into the sialome of the blood-sucking bug Triatoma infestans, a vector of Chagas' disease. Insect Biochem Mol Biol 38: 213–232. doi: 10.1016/j.ibmb.2007.11.001
[33]  Alves-Silva J, Ribeiro JM, Abbeele JVD, Attardo G, Hao Z, et al. (2010) An insight into the sialome of Glossina morsitans morsitans. BMC Genomics 11: 213. doi: 10.1186/1471-2164-11-213
[34]  Ribeiro JM, Alarcon-Chaidez F, Francischetti IM, Mans BJ, Mather TN, et al. (2006) An annotated catalog of salivary gland transcripts from Ixodes scapularis ticks. Insect Biochem Mol Biol 36: 111–129. doi: 10.1016/j.ibmb.2005.11.005
[35]  Su YL, Li JM, Li M, Luan JB, Ye XD, et al. (2012) Transcriptomic analysis of the salivary glands of an invasive whitefly. PLoS ONE 7: e39303. doi: 10.1371/journal.pone.0039303
[36]  DeLay B, Mamidala P, Wijeratne A, Wijeratne S, Mittapalli O, et al. (2012) Transcriptome analysis of the salivary glands of potato leafhopper, Empoasca fabae. J Insect Physiol 58: 1626–1634. doi: 10.1016/j.jinsphys.2012.10.002
[37]  Cooper WR, Dillwith JW, Puterka GJ (2010) Salivary proteins of Russian wheat aphid (Hemiptera: Aphididae). Environ Entomol 39: 223–231. doi: 10.1603/en09079
[38]  Bos JIB, Prince D, Pitino M, Maffei ME, Win J, et al. (2010) A functional genomics approach identifies candidate effectors from the aphid pecies Myzus persicae (green peach aphid). PloS Genetics 6: 1–13. doi: 10.1371/journal.pgen.1001216
[39]  Carolan JC, Fitzroy CI, Ashton PD, Douglas AE, Wilkinson TL (2009) The secreted salivary proteome of the pea aphid Acyrthosiphon pisum characterised by mass spectrometry. Proteomics 9: 2457–2467. doi: 10.1002/pmic.200800692
[40]  Harmel N, Letocart E, Cherqui A, Giordanengo P, Mazzucchelli G, et al. (2008) Identification of aphid salivary proteins: a proteomic investigation of Myzus persicae. Insect Mol Biol 17: 165–174. doi: 10.1111/j.1365-2583.2008.00790.x
[41]  Cherqui A, Tjallingii WF (2000) Salivary proteins of aphids, a pilot study on identification, separation and immunolocalisation. J Insect Physiol 46: 1177–1186. doi: 10.1016/s0022-1910(00)00037-8
[42]  Rotenberg D, Whitfield AE (2010) Analysis of expressed sequence tags for Frankliniella occidentalis, the western flower thrips. Insect Mol Biol 20: 1–15. doi: 10.1111/j.1365-2583.2010.01012.x
[43]  Badillo-Vargas IE, Rotenberg D, Schneweis DJ, Hiromasa Y, Tomich JM, et al. (2012) Proteomic analysis of Frankliniella occidentalis and differentially expressed proteins in response to Tomato spotted wilt virus infection. J Virol 86: 8793–8809. doi: 10.1128/jvi.00285-12
[44]  Ullman DE, Cho JJ, Mau RFL, Westcot DM, Custer DM (1992) A midgut barrier to Tomato spotted wilt virus acquisition by adult western flower thrips. Phytopathology 82: 1333–1342. doi: 10.1094/phyto-82-1333
[45]  Christodoulou DC, Gorham JM, Herman DS, Seidman JG (2001) Construction of normalized RNA-seq libraries for next-generation sequencing using the crab duplex-specific nuclease. Curr Protocol Mol Biol: John Wiley & Sons, Inc.
[46]  Consortium TIAG (2010) Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biol 8.
[47]  Altschul SF, Gish W, Miller W, W ME, Lipman DJ (1990) Basic local alignment search tool. J Molec Biol 215: 403–410. doi: 10.1016/s0022-2836(05)80360-2
[48]  Conesa A, G?tz S, García-Gómez JM, Terol J, Talón M, et al. (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674–3676. doi: 10.1093/bioinformatics/bti610
[49]  Calvo E, Pham VM, Ribeiro JMC (2008) An insight into the sialotranscriptome of the non-blood feeding Toxorhynchites amboinensis mosquito. Insect Biochem Mol Biol 38: 499–507. doi: 10.1016/j.ibmb.2007.12.006
[50]  de la Paz Celorio-Mancera M, Courtiade J, Muck A, Heckel DG, Musser RO, et al. (2011) Sialome of a generalist lepidopteran herbivore: Identification of transcripts and proteins from Helicoverpa armigera labial salivary glands. PLos One 6.
[51]  Giebu?towicz J, Wolinowska R, Sztybor A, Pietrzak M, Wroczyński P, et al. (2009) Salivary aldehyde ehydrogenase: Activity towards aromatic aldehydes and comparison with recombinant ALDH3A1. Molecules 14: 2363–2372. doi: 10.3390/molecules14072363
[52]  Sophos NA, Vasiliou V (2003) Aldehyde dehydrogenase gene superfamily: the 2002 update. Chem Biol Interact 143–144: 5–22. doi: 10.1016/s0009-2797(02)00163-1
[53]  McAuslane HJ, Alborn HT, Toth JP (1997) Systemic induction of terpenoid aldehydes in cotton pigment glands by feeding of larval Spodoptera exigua. J Chem Ecol 23: 2861–2879. doi: 10.1023/a:1022575313325
[54]  Miles PW (1999) Aphid saliva. Biological Reviews of the Cambridge Philosophical Society 74: 41–85. doi: 10.1017/s0006323198005271
[55]  Nicholson SJ, Hartson SD, Puterka GJ (2012) Proteomic analysis of secreted saliva from Russian wheat aphid (Diuraphis noxia Kurd.) biotypes that dffer in virulence to wheat. J Proteomics 75: 2252–2268. doi: 10.1016/j.jprot.2012.01.031
[56]  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. doi: 10.1002/arch.20039
[57]  Cooper WR, Nicholson SJ, Puterka GJ (2013) Salivary proteins of Lygus hesperus (Hemiptera:Miridae). Ann Entomol Soc Am 106: 86–92. doi: 10.1603/an12096
[58]  Chang C, Werb Z (2001) The many faces of metalloproteases:cell growth, invasion, angiogenesis and metastasis. Trends Cell Biol 11: S37–S43. doi: 10.1016/s0962-8924(01)82222-4
[59]  Francischetti IMB, Mather TN, Ribeiro JMC (2003) Cloning of a salivary gland metalloprotease and characterization of gelatinase and fibrin(ogen)lytic activities in the saliva of the Lyme Disease tick vector Ixodes scapularis. Biochem Biophys Res Commun 305: 869–875. doi: 10.1016/s0006-291x(03)00857-x
[60]  Decrem Y, Beaufays J, Blasiolu V, Lahaye K, Brossard M, et al. (2008) A family of putatibe metalloproteases in the salivary glands of the tick Ixodes ricinus. FEBS Journal 275: 1485–1499. doi: 10.1111/j.1742-4658.2008.06308.x
[61]  Jia LG, Shimokawa K, Bjarnason JB, Fox JW (1996) Snake venome metalloproteinases: structure, function and relationship to the ADAMs family of proteins. Toxicon 34: 1269–1276. doi: 10.1016/s0041-0101(96)00108-0
[62]  Colebatch G, Cooper P, East P (2002) cDNA cloning of a salivary chymotrypsin-like protease and the identification of six additional cDNAs encoding putative digestive proteases from the green mirid, Creontiades dilutus (Hemiptera: Miridae). Insect Biochem Molec Biol 32: 1065–1075. doi: 10.1016/s0965-1748(02)00044-9
[63]  Hosseininaveh V, Bandani A, Hosseininaveh F (2009) Digestive proteolytic activity in the Sunn pest, Eurygaster integriceps. J Insect Sci 9.
[64]  Knop Wright M, Brandt SL, Coudron TA, Wagner RM, Habibi J, et al. (2006) Characterization of digestive proteolytic activity in Lygus hesperus Knight (Hemiptera: Miridae). J Insect Physiol 52: 717–728. doi: 10.1016/j.jinsphys.2006.03.012
[65]  Agusti N, Cohen AC (2000) Lygus hesperus and L. lineolaris (Hemiptera: Miridae), phytophages, zoophages, or omnivores:evidence of feeding adaptations suggested by the salivary and midgut digestive enzymes. J Insect Physiol 58: 391–396.
[66]  Eberhard SH, Hrassnigg N, Crailsheim K, Krenn HW (2007) Evidence of protease in the saliva of the butterfly Heliconius melpomene (L.) (Nymphalidae, Lepidoptera). J Insect Physiol 53: 126–131. doi: 10.1016/j.jinsphys.2006.11.001
[67]  Lewis T (1973) Thrips: Their Biology, Ecology, and Economic Importance. New York: Academic Press. 349 p.
[68]  Watanabe H, Tokuda G (2010) Cellulytic systems in insects. Ann Rev Entomol 55: 609–632. doi: 10.1146/annurev-ento-112408-085319
[69]  Campbell DC, Dreyer DL (1985) Host-plant resistance of sorghum pectic substances by polysacchrases of greenbug biotypes (Schizaphis graminium, Homoptera:Aphididae). Arch Insect Biochem Biophys 2: 203–215. doi: 10.1002/arch.940020208
[70]  Backus EA, Andrews KB, Shugart HJ, Greve LC, Labavitch JM, et al. (2012) Salivary enzymes are injected into xylem by the glassy-winged sharpshooter, a vector of Xylella fastidiosa. J Insect Physiol 58: 949–959. doi: 10.1016/j.jinsphys.2012.04.011
[71]  Watanabe H, Nakamura M, Tokuda G, Yamaoka I, Scrivener AM, et al. (1997) Site of secretion and properties of endogenous endo-β-1,4-glucanase components from Reticulitermes speratus (Kolbe), a Japanese subterranean termite. Insect Biochem Molec Biol 27: 305–313. doi: 10.1016/s0965-1748(97)00003-9
[72]  McAllan JW, Adams JB (1961) The significance of pectinase in plant penetration by aphids. Can J Zool 39: 305–310. doi: 10.1139/z61-034
[73]  Ma R, Reese JC, Black Iv WC, Bramel-Cox P (1990) Detection of pectinesterase and polygalacturonase from salivary secretions of living greenbugs, Schizaphis graminum (Homoptera: Aphididae). J Insect Physiol 36: 507–512. doi: 10.1016/0022-1910(90)90102-l
[74]  Zeng F, Cohen AC (2000) Comparison of α amylase and protease activites of a zoophytophagous and two phytozoophagous Heteroptera. Comp Biochem Physiol 126: 101–106. doi: 10.1016/s1095-6433(00)00193-8
[75]  Ohashi K, Natori S, Kubo T (1999) Expression of amylase and glucose oxidase in the hypopharyngeal gland with an age-dependendt role chage of the worker honeybee (Apis mellifera L.). Eur J Biochem 265: 127–133. doi: 10.1046/j.1432-1327.1999.00696.x
[76]  Cristofoletti PT, Ribeiro AF, Deraison C, Rahbe Y, Terra WR (2003) Midgut adaptation and digestive enzyme distribution in a phloem feeding insect, the pea aphid Acyrthosiphon pisum. J Insect Physiol 49.
[77]  Marinotti O, James AA (1990) An α glucosidase in the salivary glands of the vector mosquito, Aedes aegypti. Insect Biochem 20: 619–623. doi: 10.1016/0020-1790(90)90074-5
[78]  Calvo E, Pham VM, Lombardo F, Arca B, Ribeiro JMC (2006) The sialotranscriptome of adult male Anopheles gambiae mosquitoes. Insect Biochem Mol Biol 36: 570–575. doi: 10.1016/j.ibmb.2006.04.005

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