Hostname: page-component-848d4c4894-p2v8j Total loading time: 0.001 Render date: 2024-05-17T18:51:16.099Z Has data issue: false hasContentIssue false
  • English
  • Français

Salivary proteins of plant-feeding hemipteroids – implication in phytophagy

Published online by Cambridge University Press:  26 November 2013

A. Sharma ,
A.N. Khan ,
S. Subrahmanyam ,
A. Raman ,
G.S. Taylor  and
M.J. Fletcher
A. Sharma
Affiliation:
School of Agricultural & Wine Sciences, Charles Sturt University, PO Box 883, Orange, NSW 2800, Australia
A.N. Khan
Affiliation:
School of Agricultural & Wine Sciences, Charles Sturt University, PO Box 883, Orange, NSW 2800, Australia
S. Subrahmanyam
Affiliation:
School of Agricultural & Wine Sciences, Charles Sturt University, PO Box 883, Orange, NSW 2800, Australia
A. Raman*
Affiliation:
School of Agricultural & Wine Sciences, Charles Sturt University, PO Box 883, Orange, NSW 2800, Australia E. H. Graham Centre for Agricultural Innovation, Wagga Wagga, NSW 2678, Australia
G.S. Taylor
Affiliation:
Australian Centre for Evolutionary Biology and Biodiversity, and School of Earth and Environmental Sciences, University of Adelaide, SA 5005, Australia
M.J. Fletcher
Affiliation:
Orange Agricultural Institute, NSW Department of Primary Industries, Forest Road, Orange, NSW 2800, Australia
*
*Author for correspondence Phone: +61 2 6365 7833 Fax: +61 2 6365 7578 E-mail: araman@csu.edu.au
Get access Rights & Permissions [Opens in a new window]

Abstract

Many hemipteroids are major pests and vectors of microbial pathogens, infecting crops. Saliva of the hemipteroids is critical in enabling them to be voracious feeders on plants, including the economically important ones. A plethora of hemipteroid salivary enzymes is known to inflict stress in plants, either by degrading the plant tissue or by affecting their normal metabolism. Hemipteroids utilize one of the following three strategies of feeding behaviour: salivary sheath feeding, osmotic-pump feeding and cell-rupture feeding. The last strategy also includes several different tactics such as lacerate-and-flush, lacerate-and-sip and macerate-and-flush. Understanding hemipteroid feeding mechanisms is critical, since feeding behaviour directs salivary composition. Saliva of the Heteroptera that are specialized as fruit and seed feeders, includes cell-degrading enzymes, auchenorrhynchan salivary composition also predominantly consists of cell-degrading enzymes such as amylase and protease, whereas that of the Sternorhyncha includes a variety of allelochemical-detoxifying enzymes. Little is known about the salivary composition of the Thysanoptera. Cell-degrading proteins such as amylase, pectinase, cellulase and pectinesterase enable stylet entry into the plant tissue. In contrast, enzymes such as glutathione peroxidase, laccase and trehalase detoxify plant chemicals, enabling the circumvention of plant-defence mechanisms. Salivary enzymes such as M1-zinc metalloprotease and CLIP-domain serine protease as in Acyrthosiphon pisum (Aphididae), and non-enzymatic proteins such as apolipophorin, ficolin-3-like protein and ‘lava-lamp’ protein as in Diuraphis noxia (Aphididae) have the capacity to alter host-plant-defence mechanisms. A majority of the hemipteroids feed on phloem, hence Ca++-binding proteins such as C002 protein, calreticulin-like isoform 1 and calmodulin (critical for preventing sieve-plate occlusion) are increasingly being recognized in hemipteroid–plant interactions. Determination of a staggering variety of proteins shows the complexity of hemipteroid saliva: effector proteins localized in hemipteran saliva suggest a similarity to the physiology of pathogen–plant interactions.

Keywords

insect–plant interactionmolecular ecologyplant stressproteomicssalivary proteins
Type
Review Article
Information
Bulletin of Entomological Research , Volume 104 , Issue 2 , April 2014 , pp. 117 - 136
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahmad, A., Kaushik, S., Ramamurthy, V.V., Lakhanpaul, S., Ramani, R., Sharma, K.K. & Vidyarthi, A.S. (2012) Mouthparts and stylet penetration of the lac insect Kerria lacca (Kerr) (Hemiptera: Tachardiidae). Arthropod Structure and Development 41, 435–441.Google Scholar
Ali, J.G. & Agrawal, A.A. (2012) Specialist versus generalist insect herbivores and plant defense. Trends in Plant Science 17, 293–302.CrossRefGoogle ScholarPubMed
Allen, M.L. & Mertens, J.A. (2008) Molecular cloning and expression of three polygalacturonase cDNAs from the tarnished plant bug, Lygus lineolaris . Journal of Insect Science 8: 27, 14, Available online at http://insectscience.org/8.27.Google Scholar
Altmann, F., Staudacher, E., Wilson, I.B. & März, L. (1999) Insect cells as hosts for the expression of recombinant glycoproteins. Glycoconjugate Journal 16, 109–123.CrossRefGoogle ScholarPubMed
Arimura, G-I., Ozawa, R. & Maffei, M.E. (2011) Recent advances in plant early signaling in response to herbivory. International Journal of Molecular Sciences 12, 3723–3739.CrossRefGoogle ScholarPubMed
Asaduzzaman, Md. & Toshiki, A. (2012) Autotoxicity in beans and their allelochemicals. Scientia Horticulturae 134, 26–31.Google Scholar
Atkinson, N.J. & Urwin, P.E. (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. Journal of Experimental Botany, doi:10.1093/jxb/ers100.CrossRefGoogle ScholarPubMed
Backus, E.A. (1985) Anatomical and sensory mechanism of leaf hopper and plant hopper feeding behaviour. pp. 163–194 in Nault, L.R. & Rodriguez, J.G. (Eds) The Leafhoppers and Planthoppers. New York, Wiley & Sons.Google Scholar
Backus, E.A. (1988) Sensory systems and behaviours which mediate hemipteran plant-feeding: a taxonomic overview. Journal of Insect Physiology 34, 151–165.CrossRefGoogle Scholar
Backus, E.A., Habibi, J., Yan, F. & Ellersieck, M. (2005 a) Stylet penetration by adult Homalodisca coagulata on grape: electrical penetration graph waveform characterization, tissue correlation, and possible implications for transmission of Xylella fastidiosa . Annals of the Entomological Society of America 98, 787–813.CrossRefGoogle Scholar
Backus, E.A., Serrano, M.S. & Ranger, C.M. (2005 b) Mechanisms of hopperburn: an overview of insect taxonomy, behavior, and physiology. Annual Review of Entomology 50, 125–151.CrossRefGoogle ScholarPubMed
Backus, E.A., Andrews, K.B., Shugart, H.J., Greve, L.C., Labavitch, J.M. & Alhaddad, H. (2012) Salivary enzymes are injected into xylem by the glassy-winged sharpshooter, a vector of Xylella fastidiosa . Journal of Insect Physiology 58, 949–959.CrossRefGoogle ScholarPubMed
Baea, H., Hermanb, E., Baileya, B., Baec, H.−J. & Sicher, R. (2005) Exogenous trehalose alters Arabidopsis transcripts involved in cell wall modification, abiotic stress, nitrogen metabolism, and plant defense. Physiologia Plantarum 125, 114–126.Google Scholar
Balakrishna, P. & Raman, A. (1992) Cecidogenesis of leaf galls of Strychnos nux-vomica (Loganiaceae) induced by the jumping plant louse species Diaphorina truncata (Homoptera: Psylloidea: Psyllidae). Entomologia Generalis 17, 285–292.Google Scholar
Baxendale, F.P., Heng-Moss, T. & Riordan, T. (1999) Blissus occiduus (Hemiptera: Lygaeidae): a chinch bug pest new to buffalograss turf. Journal of Economic Entomology 92, 1172–1176.Google Scholar
Berlin, D.H. & Hibbs, E.T. (1963) Digestive system morphology and salivary enzymes of the potato leafhopper, Empoasca fabae (Harris). Iowa Academy of Science 70, 527–540.Google Scholar
Bettencourt da Cruz, A., Schwärzel, M., Schulze, S., Niyyati, M., Heisenberg, M. & Kretzschmar, D. (2005) Disruption of the MAP1B-related protein FUTSCH leads to changes in the neuronal cytoskeleton, axonal transport defects, and progressive neurodegeneration in Drosophila . Molecular Biology of the Cell 16, 2433–2442.CrossRefGoogle ScholarPubMed
Bigham, M. & Hosseininaveh, V. (2010) Digestive proteolytic activity in the pistachio green stink bug, Brachynema germari Kolenati (Hemiptera: Pentatomidae). Journal of Asia-Pacific Entomology 13, 221–227.Google Scholar
Bonani, J.P., Fereres, A., Garzo, E., Miranda, M.P., Appezzato-da-Gloria, B. & Lopes, J.R.S. (2010) Characterization of electrical penetration graphs of the Asian citrus psyllid, Diaphorina citri, in sweet orange seedlings. Entomologia Experimentalis et Applicata 134, 35–49.CrossRefGoogle Scholar
Bos, J.I.B., Prince, D., Pitino, M., Maffei, M.E., Win, J. & Hogenhout, S.A. (2010) A functional genomics approach identifies candidate effectors from the aphid species Myzus persicae (green peach aphid). PLoS Genetics 6, e1001216. doi:10.1371/journal.pgen.1001216.CrossRefGoogle ScholarPubMed
Boyd, D.W. Jr., Cohen, A.C. & Alverson, D.R. (2002) Digestive enzymes and stylet morphology of Deraeocoris nebulosus (Hemiptera: Miridae), a predacious plant bug. Annals of the Entomological Society of America 95, 395–401.CrossRefGoogle Scholar
Boyko, E.V., Smith, C.M., Thara, V.K., Bruno, J.M., Deng, Y., Starkey, S.R. & Klaahsen, D.L. (2006) Molecular basis of plant gene expression during aphid invasion: wheat Pto- and Pti-like sequences are involved in interactions between wheat and russian wheat aphid (Homoptera: Aphididae). Journal of Economic Entomology 99, 1430–1445.CrossRefGoogle ScholarPubMed
Butler, C.D., Walker, G.P. & Trumble, J.T. (2012) Feeding disruption of potato psyllid, Bactericera cockerelli, by imidacloprid as measured by electrical penetration graphs. Entomologia Experimentalis et Applicata 142, 247–257.Google Scholar
Campbell, D.C. & Dreyer, D.L. (1990) The role of plant matrix polysaccharides in aphid-plant interactions. pp. 149–170 in Campbell, R.K. & Eikenbary, R.D. (Eds) Aphid – Plant Genotype Interactions . Amsterdam, Elsevier.Google Scholar
Campbell, D.C., Jones, K.C. & Dreyer, D.L. (1986) Discriminative behavioral responses by aphids to various plant matrix polysaccharides. Entomologia Experimentalis et Applicata 41, 17–24.Google Scholar
Carolan, J.C., Fitzroy, C.I., Ashton, P.D., Douglas, A.E. & Wilkinson, T.L. (2009) The secreted salivary proteome of the pea aphid Acyrthosiphon pisum characterised by mass spectrometry. Proteomics 9, 2457–2467.CrossRefGoogle ScholarPubMed
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. & Edwards, O.R. (2011) Predicted effector molecules in the salivary secretome of the pea aphid (Acyrthosiphon pisum): a dual transcriptomic/proteomic approach. Journal of Proteome Research 10, 1505–1518.CrossRefGoogle ScholarPubMed
Calatayud, P.A., Boher, B., Nicole, M. & Geiger, J.P. (1996) Interactions between cassava mealybug and cassava: cytochemical aspects of plant cell wall modifications. Entomologia Experimentalis et Applicata 80, 242–245.CrossRefGoogle Scholar
Celorio–Mancera, M., Greve, L.C., Teuber, L.R. & Labavitch, J.M. (2009) Identification of endo- and exo-polygalacturonase activity in Lygus hesperus (Knight) salivary glands. Archives of Insect Biochemistry and Physiology 70, 122–135.CrossRefGoogle ScholarPubMed
Cherqui, A. & Tjallingii, W.F. (2000) Salivary proteins of aphids, a pilot study on identification, separation and immunolocalisation. Journal of Insect Physiology 46, 1177–1186.Google Scholar
Clément, M., Ketelaar, T., Rodiuc, N., Banora, M.Y., Smertenko, A., Engler, G., Abad, P., Hussey, P.J. & de Almeida Engler, J. (2009) Actin-depolymerizing factor 2-mediated actin dynamics are essential for root-knot nematode infection of Arabidopsis . Plant Cell 21, 2963–2979.Google Scholar
Cohen, A.C. & Hendrix, D.L. (1994) Demonstration and preliminary characterization of α-amylase in the sweet potato whitefly, Bemisia tabaci (Aleyrodidae: Homoptera). Comparative Biochemistry and Physiology 109B, 593–601.Google Scholar
Cooper, W.R., Dillwith, J.W. & Puterka, G.J. (2010) Salivary proteins of russian wheat aphid (Hemiptera: Aphididae). Environmental Entomology 39, 223–231.Google Scholar
Couldridge, C., Newbury, H.J., FordLloyd, B., Bale, J. & Pritchard, J. (2007) Exploring plant responses to aphid feeding using a full Arabidopsis microarray reveals a small number of genes with significantly altered expression. Bulletin of Entomological Research 97, 523–532.CrossRefGoogle ScholarPubMed
Cox-Foster, D.L. & Stehr, J.E. (1994) Induction and localization of FAD–glucose dehydrogenase (GLD) during encapsulation of abiotic implants in Manduca sexta larvae. Journal of Insect Physiology 40, 235–249.Google Scholar
Crews, I.J., Mccully, M.A., Canny, M.J., Huang, C.X. & Ling, L.E.C. (1998) Xylem feeding by spittlebug nymphs: some observations by optical and cryo-scanning electron microscopy1. American Journal of Botany 85, 449–460.Google Scholar
Cristofoletti, P.T., Riberio, A.F., Deraison, C., Rahbé, Y. & Terra, W.R. (2003) Midgut adaptation and digestive enzyme distribution in a phloem feeding insect, the pea aphid Acyrthosiphon pisum . Journal of Insect Physiology 49, 11–24.Google Scholar
DeLay, B., Mamidala, P., Wijeratne, A., Wijeratne, S., Mittapalli, O., Wang, J. & Lamp, W. (2012) Transcriptome analysis of the salivary glands of potato leafhopper, Empoasca fabae . Journal of Insect Physiology 58, 1626–1634.Google Scholar
Del Bene, G., Cavallo, V., Lupetti, P. & Dallai, R. (1999) Fine structure of the salivary glands of Heliothrips haemorrhoidalis (Bouché) (Thysanoptera: Thripidae). International Journal of Insect Morphology and Embryology 28, 301–308.Google Scholar
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., Métraux, J.-P., Van Loon, L.C., Dicke, M. & Pieterse, C.M.J. (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Molecular Plant – Microbe Interactions 18, 923–937.Google Scholar
Divol, F., Vilaine, F., Thibivilliers, S., Amselem, J., Palauqui, J.C., Kusiak, C. & Dinant, S. (2005) Systemic response to aphid infestation by Myzus persicae in the phloem of Apium graveolens . Plant Molecular Biology 57, 517–540.Google Scholar
Duffey, S.S. & Stout, M.J. (1996) Antinutritive and toxic components of plant defense against insects. Archives of Insect Biochemistry and Physiology 32, 3–37.Google Scholar
Dugravot, S., Backus, E.A., Reardon, B.J. & Miller, T.A. (2008) Correlations of cibarial muscle activities of Homalodisca spp. sharpshooters (Hemiptera: Cicadellidae) with EPG ingestion waveform and excretion. Journal of Insect Physiology 54, 1467–1478.Google Scholar
Eichenseer, H., Mathews, M.C., Bi, J.L., Murphy, J.B. & Felton, G.W. (1999) Salivary glucose oxidase: multifunctional roles for Helicoverpa zea? Archives Insect Biochemistry and Physiology 42, 99–109.Google Scholar
Endo, Y., Matsushita, M. & Fujita, T. (2011) The role of ficolins in the lectin pathway of innate immunity. International Journal of Biochemistry and Cell Biology 43, 705–12.Google Scholar
Fernandez, O., Béthencourt, L., Quero, A., Sangwan, R.S. & Clément, C. (2010) Trehalose and plant stress responses: friend or foe? Trends in Plant Science 5, 409–417.CrossRefGoogle Scholar
Feyereisen, R. (1999) Insect P450 enzymes. Annual Review of Entomology 44, 507–533.Google Scholar
Frati, F., Galletti, R., Lorenzo, G.D., Salerno, G. & Conti, E. (2006) Activity of endo-polygalacturonases in mirid bugs (Heteroptera: Miridae) and their inhibition by plant cell wall proteins (PGIPs). European Journal of Entomology 103, 515–522.Google Scholar
Funk, C.J. (2001) Alkaline phosphatase activity in whitefly salivary glands and saliva. Archives of Insect Biochemistry and Physiology 46, 165–174.Google Scholar
Furch, A.C., van Bel, A.J., Fricker, M.D., Felle, H.H., Fuchs, M. & Hafke, J.B. (2009) Sieve element Ca2+ channels as relay stations between remote stimuli and sieve tube occlussion in Vicia faba . Plant Cell 21, 2118–2132.Google Scholar
Gardiner, J. & Marc, J. (2011) Arabidopsis thaliana, a plant model organism for the neuronal microtubule cytoskeleton? Journal of Experimental Botany 62, 89–97.Google Scholar
Gasper, R., Sot, B. & Wittinghofer, A. (2010) GTPase activity of Di-Ras proteins is stimulated by Rap1GAP proteins. Small Gtpases 1, 133–141.Google Scholar
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 aphids manipulate plant responses. Comptes Rendus Biologies 333, 516–523.Google Scholar
Gomi, K., Satoh, M., Ozawa, R., Shinonaga, Y., Sanada, S., Sasaki, K., Matsumura, M., Ohashi, Y., Kanno, H., Akimitsu, K. & Takabayashi, J. (2010) Role of hydroperoxide lyase in white-backed planthopper (Sogatella furcifera Horvath)-induced resistance to bacterial blight in rice, Oryza sativa L. The Plant Journal 61, 46–57.CrossRefGoogle ScholarPubMed
Gullan, P.J., Miller, D.R. & Cook, L.G. (2005) Gall-inducing scale insects (Hemiptera: Sternorrhyncha: Coccoidea). pp. 159–230 in Raman, A., Schaefer, C.W. & Withers, T.M. (Eds) Biology, Ecology, and Evolution of Gall-inducing Arthropods. New Hampshire, Science Publishers.Google Scholar
Hall, A. & Lalli, G. (2010) Rho and Ras GTPases in axon growth, guidance, and branching. Cold Spring Harbor Perspectives in Biology 2, 2:a001818.Google Scholar
Harmel, N., Létocart, E., Cherqui, A., Giordanengo, P., Mazzucchelli, G., Guillonneau, F., De Pauw, E., Haubruge, E. & Francis, F. (2008) Identification of aphid salivary proteins: a proteomic investigation of Myzus persicae . Insect Molecular Biology 17, 165–174.Google Scholar
Harper, S. & Horne, P.A. (2012) The feeding effects of western flower thrips (Frankliniella occidentalis (Pergande) and wind damage on French beans (Phaseolus vulgaris L.). Australian Journal of Entomology 51, 205–208.Google Scholar
Hattori, M., Konishi, H., Tamura, Y., Konno, K. & Sogawa, K. (2005) Laccase-type phenoloxidase in salivary glands and watery saliva of the green rice leafhopper, Nephotettix cincticeps . Journal of Insect Physiology 51, 1359–1365.Google Scholar
Hattori, M., Tsuchihara, K., Noda, H., Konishi, H., Tamura, Y., Shinoda, T., Nakamura, M. & Hasegawa, T. (2010) Molecular characterization and expression of laccase genes in the salivary glands of the green rice leafhopper, Nephotettix cincticeps (Hemiptera: Cicadellidae). Insect Biochemistry and Molecular Biology 40, 331–338.Google Scholar
Hattori, M., Nakamura, M., Komatsu, S., Tsuchihara, K., Tamura, Y. & Hasegawa, T. (2012) Molecular cloning of a novel calcium-binding protein in the secreted saliva of the green rice leafhopper Nephotettix cincticeps . Insect Biochemistry and Molecular Biology 42, 1–9.Google Scholar
He, Y.P., Chen, L., Chen, J., Zhang, J., Chen, L., Shenc, J. & Zhud, Y.C. (2011) Electrical penetration graph evidence that pymetrozine toxicity to the rice brown planthopper is by inhibition of phloem feeding. Pest Management Science 67, 483–491.CrossRefGoogle Scholar
Herrmann, H. & Strelkov, S.V. (2011) History and phylogeny of intermediate filaments: now in insects. BMC Biology 9, doi:10.1186/1741-7007-9-16.Google Scholar
Hogenhout, S.A. & Bos, J.I.B. (2011) Effector proteins that modulate plant-insect interactions. Current Opinion in Plant Biology 14, 422–428.Google Scholar
Hogenhout, S.A., Oshima, K., Ammar, el-D., Kakizawa, S., Kingdom, H.N. & Namba, S. (2008 a) Phytoplasmas: bacteria that manipulate plants and insects. Molecular Plant Pathology 9, 403–423.Google Scholar
Hogenhout, S.A., Ammar, El-D., Whitfield, A.E. & Redinbaugh, M.G. (2008 b) Insect vector interactions with persistently transmitted viruses. Annual Review of Phytopathology 46, 327–359.Google Scholar
Hori, K. (1992) Insects secretion and their effect on plant growth, with special reference to hemipterans. pp. 157–170 in Shorthouse, J.D. & Rohfritch, O. (Eds) Biology of Insect-Induced Galls. New York, Oxford University Press.Google Scholar
Hori, K. (2000) Possible causes of diseases symptoms resulting from the phytophagous Heteroptera. pp. 11–35 in Schaefer, C.W. & Panizzi, A.R. (Eds) Heteroptera of Economic Importance. Boca Raton, CRC Press.Google Scholar
Horsch, M., Mayer, C., Sennhauser, U. & Rast, D.M. (1997) Beta-N-acetylhexosaminidase: a target for the design of antifungal agents. Pharmacology and Therepeutics 76, 187–218.Google Scholar
Hosseininaveh, V., Bandani, A. & Hosseininaveh, F. (2009) Digestive proteolytic activity in the Sunn pest, Eurygaster integriceps . Journal of Insect Science 9, Available online at http://insectscience.org/9.70, doi: 10.1673/031.009.7001.CrossRefGoogle ScholarPubMed
Howe, G.A. & Jander, G. (2008) Plant immunity to insect herbivores. Annual Review of Plant Biology 59, 41–66.Google Scholar
Huang, F., Tjallingii, W.F., Zhang, P., Zhang, J., Lu, Y. & Lin, J. (2012) EPG waveform characteristics of Solenopsis mealybug stylet penetration on cotton. Entomologia Experimentalis et Applicata 143, 47–54.CrossRefGoogle Scholar
Hunter, W.B. & Backus, E.A. (1989) Mesophyll-feeding by the potato leafhopper, Empoasca fabae (Homoptera: Cicadellidae): results from electronic monitoring and thin-layer chromatography. Environmental Entomology 18, 465–472.Google Scholar
Hunter, W.B. & Ullman, D.E. (1989) Analysis of mouthpart movements during feeding of Frankliniella occidentalis (Pergande) and F. schultzei Trybom (Thysanoptera: Thripidae). International Journal of Insect Morphology and Embryology 18, 161–171.Google Scholar
Ishizaki, M., Yasuda, T. & Watanabe, T. (2007) Feeding behavior of rice bug Leptocorisa chinensis (Dallas) (Heteroptera: Alydidae) nymphs on rice panicles and rice plant extract. Applied Entomology and Zoology 42, 83–88.Google Scholar
Jensen, S.E. (2000) Insecticide resistance in the Western Flower thrips, Frankliniella occidentalis . PhD Thesis, Roskilde University, Denmark.Google Scholar
Jones, J.D.G. & Dangl, J.L. (2006) The plant immune system. Nature 444, 323–329.Google Scholar
Kaloshian, I. & Walling, L.L. (2005) Hemipterans as plant pathogens. Annual Review of Phytopathology 43, 491–521.Google Scholar
Kindt, F., Joosten, N.N., Peters, D. & Tjallingii, W.F. (2003) Characterisation of the feeding behaviour of western flower thrips in terms of electrical penetration graph (EPG) waveforms. Journal of Insect Physiology 49, 183–191.Google Scholar
Kirk, W.D.J. (1997) Feeding. pp. 119–174 in Lewis, T. (Ed.) Thrips as Crop Pests. Wallingford, CAB International.Google Scholar
Knoblauch, M. & van Bel, A.J.E. (1998) Sieve tubes in action. Plant Cell 10, 35–50.Google Scholar
Kostaropoulos, I., Papadopoulos, A.I., Metaxakis, A., Boukouvala, E. & Papadopoulou-Mourkidou, E. (2001) Glutathione S-transferase in the defence against pyrethroids in insects. Insect Biochemistry and Molecular Biology 31, 313–319.Google Scholar
Larcher, W. (1987) Stress bei Pflanzen. Naturwissenschaften 74, 158–167.Google Scholar
Laurema, S. & Nuorteva, P. (1961) On the occurrence of pectic polygalacturonase in the salivary glands of Heteroptera and Homoptera Auchenorrhyncha. Annales Entomologici Fennici 27, 89–93.Google Scholar
Lehane, M. (2005) Managing the blood meal. pp. 87–109 in Lehane, M. (Ed.) The biology of blood sucking in insects. Cambridge, Cambridge University Press.Google Scholar
Li, C., Williams, M.M., Loh, Y-T., Lee, G.I. & Howe, G.A. (2002) Resistance of cultivated tomato to cell content-feeding herbivores is regulated by the octadecanoid-signaling pathway. Plant Physiology 130, 494–503.Google Scholar
Ma, G., Hay, D., Li, D., Asgari, S. & Schmidt, O. (2006) Recognition and inactivation of LPS by lipophorin particles. Developmental and Comparative Immunology 30, 619–626.Google Scholar
Ma, R., Reese, J.C., Black, W.C. IV & Bramel-cox, P. (1990) Detection of pectinesterase and polygalacturonase from salivary secretions of living greenbugs, Schizaphis graminum (Homoptera: Aphididae). Journal of Insect Physiology 36, 507–512.Google Scholar
Manda, G., Nechifor, M.T. & Neagu, T.M. (2009) Reactive oxygen species, cancer and anti-cancer therapies. Current Chemical Biology 3, 342–366.CrossRefGoogle Scholar
Martinez de Ilarduya, O., Xie, Q.G. & Kaloshian, I. (2003) Aphid-induced defense responses in Mi-1-mediated compatible and incompatible tomato interactions. Molecular Plant-Microbe Interactions 16, 699–708.Google Scholar
Mehrabadi, M. & Bandani, A.R. (2009) Study on salivary glands α-amylase in wheat bug Eurygaster maura (Hemiptera: Scutelleridae). American Journal of Applied Sciences 6, 555–560.Google Scholar
Miles, P.W. (1999) Aphid saliva. Biological Reviews 74, 41–85.Google Scholar
Miles, P.W. & Oertli, J.J. (1993) The significance of antioxidants in the aphid–plant interaction: the redox hypothesis. Entomologia Experimentalis et Applicata 67, 275–283.Google Scholar
Miles, P.W. & Taylor, G.S. (1994) ‘Osmotic pump’ feeding by coreids. Entomologia Experimentalis et Applicata 73, 163–173.Google Scholar
Mitchell, P.l. (2004) Heteroptera as vectors of plant pathogens. Neotropical Entomology 33, 519–545.Google Scholar
Montesano, M., Hyytiainen, H., Wettstein, R. & Palva, E.T. (2003) A novel potato defence-related alcohol: NADP – oxidoreductase induced in response to Ervinia carotovora . Plant Molecular Biology 52, 177–189.Google Scholar
Moran, P.J. & Thompson, G.A. (2001) Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiology 125, 1074–1085.Google Scholar
Moritz, G. (1995) Morphogenetic development of some species of the Order Thysanoptera (Insecta). pp. 489–504 in Parker, B.L., Skinner, M. & Lewis, T. (Eds) Thrips Biology and management. New York, Plenum Press.Google Scholar
Morkunas, I., van Chung, M. & Gabrys, B. (2011) Phytohormonal signaling in plant responses to aphid feeding. Acta Physiologica Plantarum 33, 2057–2073.Google Scholar
Mound, L.A. & Morris, D.C. (2005) Gall-inducing Thrips: an evolutionary perspective. pp. 59–72 in Raman, A., Schaefer, C.W. & Withers, T.M. (Eds) Biology, Ecology and Evolution of Gall – inducing Arthropods. Vol. 1. New Hampshire, USA, Science publishers.Google Scholar
Mutikainen, P., Walls, M., Ovaska, J., Keinänen, M., Julkunen-Tiitto, R. & Vapaavuori, E. (2002) Costs of herbivoure resistance in clonal saplings of Betula pendula . Oecologia 133, 364–371.Google Scholar
Mutti, N.S., Louis, J., Pappan, L.K., Pappan, K., Begum, K., Chen, M.S., Park, Y., Dittmer, N., Marshall, J., Reese, J.C. & Reeck, G.R. (2008) A protein from the salivary glands of the pea aphid, Acyrthosiphon pisum, is essential in feeding on a host plant. Proceedings of the National Academy of Sciences 105, 9965–9969.CrossRefGoogle ScholarPubMed
Ni, X., Quisenberry, S.S., Pornkulwat, S., Figarola, J.L., Skoda, S.R. & Foster, J.E. (2000) Hydrolases and oxidoreductase activities in Diuraphis noxia and Rhopalosiphum padi (Hemiptera: Aphididae). Annals of the Entomological Society of America 93, 595–601.Google Scholar
Ni, X., Quisenberry, S.S., Heng-Moss, T., Markwell, J.P. & Sarath, G. (2001) Oxidative responses of resistant and susceptible cereal leaves to symptomatic and nonsymptomatic cereal aphid (Hemiptera: Aphididae) feeding. Journal of Economical Entomology 94, 743–751.Google Scholar
Nicholson, S.J., Hartso, S.D. & Puterka, G.J. (2012) Proteomic analysis of secreted saliva from Russian wheat aphid (Diuraphis noxia Kurd.) biotypes that differ in virulence to wheat. Journal of Proteomics 75, 2252–2268.Google Scholar
Nickel, H. (2003) The Leafhoppers and Planthoppers of Germany (Hemiptera, Auchenorrhyncha): Patterns and Strategies in a Highly Diverse Group of Phytophagous Insects. Pensoft series faunistica no. 28. Sofia, Pensoft Publishers + Keltern,Goecke & Evers, p. 460.Google Scholar
Ozgur, E. (2006) Identification and characterization of hydrolytic enzymes of sunn pest (Eurygaster integriceps) and cotton bollworm (Helicoverpa armigera). PhD Thesis, Middle East Technical University, Çankaya Ankara, Turkey.Google Scholar
Powell, G. (2005) Intracellular salivation is the aphid activity associated with inoculation of non-persistently transmitted viruses. Journal of General Virology 86, 469–472.Google Scholar
Powell, G. & Hardie, J. (2000) Host-selection behaviour by genetically identical aphids with different plant preferences. Physiological Entomology 25, 54–62.CrossRefGoogle Scholar
Powell, G., Tosh, C.R. & Hardie, J. (2006) Host plant selection by aphids: behavioral, evolutionary, and applied perspectives. Annual Review of Entomology 51, 309–330.Google Scholar
Prado, E. & Tjallingii, W. (2007) Behavioral evidence for local reduction of aphid-induced resistance. Journal of Insect Science 7, Available online at: http://insectscience.org/7.48.Google Scholar
Prado, E. & Tjallingii, W.F. (1994) Aphid activities during sieve element puncture. Entomologia Experimentalis et Applicata 72, 157–165.CrossRefGoogle Scholar
Purcell, A.H. & Almeida, R.P.P. (2005) Insects as vectors of disease agents. Encyclopedia of Plant and Crop Science, doi: 10.1081/E-EPCS-120010496.Google Scholar
Rajadurai, S., Mani, T., Balakrishna, P. & Raman, A. (1990) On the digestive enzymes and soluble proteins of the nymphal salivary glands of Trioza jambolanae Crawford (Triozinae: Psyllidae: Homoptera), the gall maker of the leaves of Syzygium cumini (L.) Skeels (Myrtaceae). Phytophaga 3, 47–53.Google Scholar
Rakitov, R. & Appel, E. (2012) Life history of the Camelthorn Gall Leafhopper, Scenergates viridis (Vilbaste) (Hemiptera, Cicadellidae). Psyche 2012, Article ID 930975, 19, doi:10.1155/2012/930975.Google Scholar
Raman, A. (2003) Cecidogenetic behavior of some gall-inducing thrips, psyllids, coccids, and gall midges and morphogenesis of their galls. Oriental Insects 37, 359–413.Google Scholar
Raman, A. (2010) Insect–plant interactions: the gall factor. pp. 121–146 in Seckbach, J. & Dubinsky, Z. (Eds) All Flesh is Grass: Plant–Animal Interrelationships. Heidelberg, Springer.Google Scholar
Raman, A. (2011) Morphogenesis of insect-induced plant galls: facts and questions. Flora 206, 517–533.Google Scholar
Raman, A. (2012) Gall induction by hemipteroid insects. Journal of plant interactions 7, 29–44.Google Scholar
Raman, A. & Takagi, S. (1992) Galls induced on Hopea ponga (Dipterocarpaceae) in southern India and their gall-maker belonging to the Beesoniidae. Instecta matsumurana (New Series) 47, 1–32.Google Scholar
Raman, A., Ananthakrishnan, T.N. & Swaminathan, S. (1978) On the simple leaf galls of Casearia tomentosa Roxb., (Samydaceae) induced by Gynaikothrips flaviantennatus Moulton (Thysanoptera: Phlaeothripidae). Proceedings of the Indian Academy of Sciences, B 87, 231–242.Google Scholar
Raman, A., Rajadurai, S., Mani, T. & Balakrishna, P. (1999) On the salivary enzymes and soluble proteins of the Mimusops gall thrips Arrhenothrips ramakrishnae Hood Tubulifera: Thysanoptera: Insecta. Zeitschrift fuer Angewandte Zoologie 78, 131–136.Google Scholar
Raman, A., Beiderbeck, R. & Herth, W. (2009) Early subcellular responses of susceptible and resistant Vitis taxa to feeding by grape phylloxera Daktulosphaira vitifoliae . Botanica Helvetica 119, 31–39.Google Scholar
Rathore, R.S., Garg, N., Garg, S. & Kumar, A. (2009) Starch phosphorylase: role in starch metabolism and biotechnological applications. Critical Review in Biotechnology 29, 214–224.Google Scholar
Saguez, J., Hainez, R., Cherqui, A., Van Wuytswinkel, O., Jeanpierre, H., Lebon, G., Noiraud, N., Beaujean, A., Jouanin, L., Laberche, J.C., Vincent, C. & Giordanengo, P. (2005) Unexpected effects of chitinases on the peach-potato aphid (Myzus persicae Sulzer) when delivered via transgenic potato plants (Solanum tuberosum Linné) and in vitro . Transgenic Research 14, 57–67.Google Scholar
Sarker, M. & Mukhopadhyay, A. (2006) Studies on salivary and midgut enzymes of a major sucking pest of tea, Helopeltis theivora (Heteroptera: Miridae) from Darjeeling plains. Indian Journal of Entomological Research Soceity 8, 27–36.Google Scholar
Schaefer, C.W. (1997) The origin of secondary carnivory from herbivory in Heteroptera (Hemiptera). pp. 229–239 in Raman, A. (Ed.) Ecology and Evolution of Plant–feeding Insects in Natural and Man–made Environments. New Delhi, International Scientific Publications.Google Scholar
Schaefer, C.W. & Panizzi, A.R. (2000) Economic importance of Heteroptera: a general view. pp. 3–10 in Schaefer, C.W. & Panizzi, A.R. (Eds) Heteroptera of Economic Importance. Boca Raton, CRC Press.Google Scholar
Sjölund, R.D. (1997) The phloem sieve element: a river runs through it. Plant Cell 9, 1137–1141.Google Scholar
Smith, C.M. (2005). Plant Resistance to Arthropods. Netherlands, Springer.Google Scholar
Somssich, I.E., Wernert, P., Kiedrowski, S. & Hahlbrock, K. (1996) Arabidopsis thaliana defense-related protein ELI3 is an aromatic alcohol: NADP – oxidoreductase. Proceedings of the National Academy of Sciences 93, 14199–14203.Google Scholar
Soyelu, O.L., Akingbohungbe, A.E. & Okonji, R.E. (2007) Salivary glands and their digestive enzymes in pod-sucking bugs (Hemiptera: Coreoidea) associated with cowpea Vigna unguiculata ssp. unguiculata in Nigeria. International Journal of Tropical Insect Science 27, 40–47.Google Scholar
Stafford, C.A., Gregory, P.W. & Ullman, D.E. (2012) Hitching a ride, vector feeding and virus transmission. Communicative and Integrative Biology 5, 43–49.CrossRefGoogle ScholarPubMed
Steinbauer, M.J., Taylor, G.S. & Madden, J.L. (1997) Comparison of damage to Eucalyptus caused by Amorbus obscuricornis and Gelonus tasmanicus . Entomologia Experimentalis et Applicata 82, 175–180.Google Scholar
Strong, F.E. & Kruitwagen, E.C. (1968) Polygalacturonase in salivary apparatus of Lygus hesperus (Hemiptera). Journal of Insect Physiology 14, 1113–1119.Google Scholar
Taylor, G.S. & Miles, P.W. (1994) Composition and variability of the saliva of coreids in relation to phytotoxicoses and other aspects of the salivary physiology of phytophagous Heteroptera. Entomologia experimentalis et applicata 73, 265–277.Google Scholar
Thompson, G.A. & Goggin, F.L. (2006) Transcriptomics and functional genomics of plant defence induction by phloem-feeding insects. Journal of Experimental Botany 57, 755–766.Google Scholar
Tjallingii, W.F. (2006) Salivary secretions by aphids interacting with proteins of phloem wound responses. Journal of Experimental Botany 57, 739–745.Google Scholar
Trebicki, P., Tjajjingii, W.F., Harding, R.M., Rodoni, B.C. & Powell, K.S. (2012) EPG monitoring of the probing behaviour of the common brown leafhopper Orosius orientalis on artificial diet and selected host plants. Arthropod-Plant Interactions 6, 405–415.Google Scholar
Tumlinson, J.H. & Lait, C.G. (2005) Biosynthesis of fatty acid amide elicitors of plant volatiles by insect herbivores. Archives of Insect Biochemistry and Physiology 58, 54–68.Google Scholar
Urbanska, A. & Leszczynski, B. (1997) Enzymatic adaptations of cereal aphids to plant glycosides. Communication of Plants with the Environment (Abstracts). p. 25 in Proceedings of Phytochemical Society of North American and Phytochemical Society of Europe, 20–23 April 1997, Noordwijkerhout, The Netherlands.Google Scholar
Urbanska, A., Tjallingii, W.F. & Leszczynski, B. (1994) Application of agarose-sucrose gels for investigation of aphid salivary enzymes. Aphids and Other Homopterous Insects 4, 81–87.Google Scholar
Urbanska, A., Leszczynski, B., Laskowska, I. & Matok, H. (1998) Enzymatic defence of grain aphid against plant phenolics. pp. 119–124 in Nieto, J.M. & Dixon, A.F.G. (Eds) Aphids in Natural and Managed Ecosystems. Universidad de León, Leon, Secretario de Publicaciones.Google Scholar
Uzest, M., Gargani, D., Drucker, M., Hebrard, E., Garzo, E., Candresse, T., Fereres, A. & Blanc, S. (2007) A protein key to plant virus transmission at the tip of the insect vector stylet. Proceedings of the National Academy of Sciences 104, 17959–17964.Google Scholar
Uzest, M., Gargani, D., Dombrovsky, A., Cazevieille, C., Cot, D. & Blanc, S. (2010) The “acrostyle”: a newly described anatomical structure in aphid stylets. Arthropod Structure and Development 39, 221–229.Google Scholar
van der Horst, D.J. & Rodenburg, K.W. (2010) Locust flight activity as a model for hormonal regulation of lipid mobilization and transport. Journal of Insect Physiology 56, 844–853.Google Scholar
van Loon, L.C., Rep, M. & Pieterse, C.M.J. (2006) Significance of inducible defense-related proteins in infected plants. Annual Review of Phytopathology 44, 135–162.Google Scholar
Walling, L.L. (2000) The myriad plant responses to herbivores. Journal of Plant Growth Regulation 19, 195–216.Google Scholar
Walling, L.L. (2008) Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiology 146, 859–866.Google Scholar
Wang, J., Sykes, B.D. & Ryan, R.O. (2002) Structural basis for the conformational adaptability of apolipophorin III, a helix-bundle exchangeable apolipoprotein. Proceedings of the National Academy of Sciences 99, 1188–1193.Google Scholar
Will, T. & van Bel, A.J.E. (2006) Physical and chemical interactions between aphids and plants. Journal of Experimental Botany 57, 729–735.Google Scholar
Will, T., Tjallingii, W.F., Thönnessen, A. & van Bel, A.J.E. (2007) Molecular sabotage of plant defense by aphid saliva. Proceedings of the National Academy of Sciences the USA 104, 10536–10541.Google Scholar
Will, T., Kornemann, S.R., Furch, A.C., Tjallingii, W.F. & van Bel, A.J.E. (2009) Aphid watery saliva counteracts sieve-tube occlusion: a universal phenomenon? Journal of Experimental Biology 212, 3305–3312.CrossRefGoogle ScholarPubMed
Williams, L., Rodriguez-Saona, C., Paré, P.W. & Crafts-Brandner, S.J. (2005) The piercing-sucking herbivores Lygus hesperus and Nezara viridula induce volatile emissions in plants. Archives of Insect Biochemistry and Physiology 58, 84–96.CrossRefGoogle ScholarPubMed
Wu, H., Haig, T., Pratley, J., Lemerle, D. & An, M. (2000) Distribution and exudation of allelochemicals in wheat Triticum aestivum . Journal of Chemical Ecology 26, 2141–2154.Google Scholar
Yan, Y., Peng, L., Liu, W.-X., Wan, F.-H. & Harris, M.K. (2011) Host plant effects on alkaline phosphatase activity in the whiteflies, Bemisia tabaci Biotype B and Trialeurodes vaporariorum . Journal of Insect Science 11, Available online at http://insectscience.org/11.9 Google Scholar
Youn, Y.N. (1998) Electrically recorded feeding behavior of Nephotettix cincticeps . Asia-Pacific Entomology 1, 147–161.CrossRefGoogle Scholar
Zdybicka-Barabas, A. & Cytryńska, M. (2011) Involvement of apolipophorin III in antibacterial defense of Galleria mellonella larvae. Comparative Biochemistry and Physiology B: Biochemistry and Molecular Biolology 158, 90–98.Google Scholar
Zhao, J., Davis, L.C. & Verpoorte, R. (2005) Elicitor signal transduction leading to production, of plant secondary metabolites. Biotechnology Advances 23, 283–333.Google Scholar
Zhao, S., Xu, C., Qian, H., Lv, L., Ji, C., Chen, C., Zhao, X., Zheng, D., Gu, S., Xie, Y. & Mao, Y. (2008) Cellular retinaldehyde-binding protein-like (CRALBPL), a novel human Sec14p-like gene that is upregulated in human hepatocellular carcinomas, may be used as a marker for human hepatocellular carcinomas. DNA and Cell Biology 27, 159–163.Google Scholar
Zibaee, A., Hoda, H. & Fazeli-Dinan, M. (2012) Purification and biochemical properties of a salivary α-amylase in Andrallus spinidens Fabricius (Hemiptera: Pentatomidae). Invertebrate Survival Journal 9, 49–57.Google Scholar