Molecular approaches to mosquito parasite interactions

Archives of Insect Biochemistry and Physiology

Volumn 34, Issue 1, 1997, Pages 1-18

  Zheng, Liangbiao ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

Arbovirus; Brugia; Genetic map; Immunity; Plasmodium; QTL; Refractoriness; Vector

Indexed keywords

EID: 0002774011     PISSN: 07394462     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1520-6327(1997)34:1<1::AID-ARCH1>3.0.CO;2-1     Document Type: Article

References (111)

1. Adam R, Kaltmann B, Rudin W, Friedrich T, Marti T, Lucius R (1996): Identification of chitinase as the immunodominant filarial antigen recognized by sera of vaccinated rodents. J Biol Chem 271:1441-1447.
2. Afanasiev BN, Kozlov YV, Carlson JO, Beaty BJ (1994): Densovirus of Aedes aegypti as an expression vector in mosquito cells. Exp Parasitol 79:322-339.
3. Ashida M, Brey PT (1995): Role of the integument in insect defense: Pro-phenol oxidase cascade in the cuticular matrix. Proc Natl Acad Sci U S A 92:10698-10702.
4. Ashida M, Kinoshita K, Brey PT (1990): Studies on prophenoloxidase activation in the mosquito Aedes aegypti L. Eur J Biochem 188:507-515.
5. Aspan A, Huang TS, Cerenius L, Soderhall K (1995): cDNA cloning of prophenoloxidase from the freshwater crayfish Pacifastacus leniusculus and its activation. Proc Natl Acad Sci U S A 92:939-943.
6. Barillas-Mury C, Wells MA (1993): Cloning and sequencing of the blood meal-induced late trypsin gene from the mosquito Aedes aegypti and characterization of the upstream regulatory region. Insect Mol Biol 2:7-12.
7. Barillas-Mury C, Charlesworth A, Gross I, Richman A, Hoffmann JA, Kafatos FC (1996): Immune factor Gambif1, a new rel family member from the human malaria vector, Anopheles gambiae. EMBO J 15:4691-4701.
8. Barreau C, Touray M, Pimenta PF, Miller LH, Vernick KD (1995): Plasmodium gallinaceum: Sporozoite invasion of Aedes aegypti salivary glands is inhibited by anti-gland antibodies and by lectins. Exp Parasitol 81:332-343.
9. Beaty BJ, Calisher CH (1991): Bunyaviridae-natural history. Curr Top Microbiol Immunol 169:27-78.
10. Beerntsen BT, Severson DW, Christensen BM (1994): Aedes aegypti: Characterization of a hemolymph polypeptide expressed during melanotic encapsulation of filarial worms. Exp Parasitol 79:312-321.
11. Beerntsen BT, Severson DW, Klinkhammer JA, Kassner VA, Christensen BM (1995): Aedes aegypti: A quantitative trait locus (QTL) influencing filarial worm intensity is linked to QTL for susceptibility to other mosquito-borne pathogens. Exp Parasitol 81:355-362.
12. Benedict MQ, Besansky NJ, Chang H, Mukabayarie O, Collins FH (1996): Mutations in the Anopheles gambiae pink-eye and white genes define distinct, tightly linked eye-colour loci. J Hered 87:48-53.
13. Berner R, Rudin W, Hecker H (1983): Peritrophic membranes and protease activity in the midgut of the malaria mosquito, Anopheles stephensi (Liston) (Insecta: Diptera) under normal and experimental conditions. J Ultrastruc Res 83:195-204.
14. Besansky NJ, Finnerty V, Collins FH (1992) Molecular perspectives on the genetics of mosquitoes. Adv Genet 30:123-184.
15. Besansky NJ, Bedell JA, Benedict MQ, Mukabayaire O, Hilfiker D, Collins FH (1995): Cloning and characterization of the white gene from Anopheles gambiae. Insect Mol Biol 4:217-231.
16. Brey PT, Ahmed A, Lee W-J, Ashida M, Lehane MJ (1995): Tyrosinase-type prophenoloxidase distribution in the alimentary canal of strains of Anopheles gambiae refractory and susceptible to Plasmodium infection. Exp Parasitol 80:654-664.
17. Brown MR, Raikhel AS, Lea AO (1985): Ultrastructure of midgut endocrine cells in adult mosquito, Aedes negypti. Tissue Cell 17:709-721.
18. Brown SE, Menninger J, Difillipantonio M, Beaty BJ, Ward DC, Knudson DL (1995): Toward a physical map of Aedes aegypti. Insect Mol Biol 4:161-167.
19. Carlson JO, Olson KE, Higgs S, Beaty NJ (1995): Molecular genetic manipulation of mosquito vectors. Ann Rev Entomol 40:359-388.
20. Chalk R, Townson H, Natori S, Desmond H, Ham PJ (1994): Purification of an insect defensin from the mosquito, Aedes aegypti. Insect Biochem Mol Biol 24:403-410.
21. Chalk R, Albuquerque CM, Ham PJ, Townson H (1995a): Full sequence and characterization of two insect defensins: Immune peptides from the mosquito Aedes aegypti. Proc R Soc Lond [Biol] 261:217-221.
22. Chalk R, Townson H, Ham PJ (1995b): Brugia pahangi: The effects of cecropins on microfilariae in vitro and in Aedes aegypti. Exp Parasitol 80:401-406.
23. Champagne DE, Ribeiro JMC (1994): Siaokinin I and II: Vasodilatory tachykinins from the yellow fever mosquito Aedes aegypti. Proc Natl Acad Sci U S A 91:138-142.
24. Champagne DE, Smartt CT, Ribeiro JMC, James AA (1995): The salivary gland-specific apyrase of the mosquito Aedes aegypti is a member of the 5′-nucleotidase family. Proc Natl Acad Sci U S A 92:694-698.
25. Chikilian ML, Bradley TJ, Nayer JK, Knight JW (1994): Ultrastructural comparison of extracellular and intracellular encapsulation of Burgia malayi in Anopheles quadrimaculatus. J Parasitol 80:133-140.
26. Clements AN (1992) The Biology of Mosquitoes, Vol. 1. London: Chapman & Hall.
27. Collins FH, Paskewitz SM (1996): A review of the use of ribosomal DNA (rDNA) to differentiate among cryptic Anopheles gambiae. Insect Mol Biol 5:1-9.
28. Collins FH, Sakai RK, Vernick KD, Paskewitz S, Seeley DC, Miller LH, Collins WE, Campbell CC, Gwadz RW (1986): Genetic selection of a Plasmodium-refractory strain of the malaria vector Anopheles gambiae. Science 234:607-610.
29. Collins FS (1995): Positional cloning moves from perditional to traditional. Nature Genet 9:347-350.
30. Crews-Oyen AE, Kumar VK, Collins FH (1993): Association of two esterase genes, a chromosomal inversion, and susceptibility to Plasmodium cynomolgi in the African malaria vector Anopheles gambiae. Am J Trop Med Hyg 49:341-347.
31. Dimopoulos G, Zheng L, Kumar V, della Torre A, Kafatos FC, Louis C (in press): Integrated genetic map of Anopheles gambiae: Use of RAPD polymorphisms for genetic, cytogenetic and STS landmarks. Genetics 143:953-960.
32. Dunn PE, Bohnert TJ, Russell V (1994): Regulation of antibacterial protein synthesis following infection and during metamorphosis of Manduca sexta. Ann NY Acad Sci 712:117-130.
33. Fehlbaum P, Bulet P, Michaut L, Lagueux M, Broekaert WF, Hetru C, Hoffmann JA (1994): Insect immunity: Septic injury of Drosophila induces the synthesis of a potent antifungal peptides with sequence homology to plant antifungal peptides. J Biol Chem 269:33159-33163.
34. Fuhrman JA (1995): Filarial chitinases. Parasitol Today 11:259-261.
35. Fuhrman JA, Lane W, Smith R, Piessens W, Perler F (1992): Transmission-blocking antibodies recognize microfilarial chitinase in Brugian lymphatic filariasis. Proc Natl Acad Sci U S A 89:1548-1552.
36. Fuhrman JA, Lee J, Dalamagas D (1995): Structure and function of a family of chitinase isozymes from Brugian microfilariae. Exp Parasitol 80:672-680.
37. Fujimoto K, Okino N, Kawabata S, Iwanaga S, Ohnishi E (1995): Nucleotide sequence of the cDNA encoding the proenzyme of phenol oxidase A1 of Drosophila melanogaster. Proc Natl Acad Sci U S A 92:7769-7773.
38. Gaines PJ, Olson KE, Higgs S, Powers AM, Beaty BJ, Blair CD (1996): Pathogen-derived resistance to Dengue type-2 virus in mosquito cells by expression of the premembrane coding region of the viral genome. J Virol 70:2132-2137.
39. Gwadz WR, Kaslow D, Lee J, Maloy WL, Zasloff M, Miller LH (1989): Effects of magainins and cecropins on the sporogonic development of malaria parasites in mosquitoes. Infect Immun 57:2628-2633.
40. Hall M, Scott T, Sugumaran M, Soderhall K, Law JH (1995): Proenzyme of Manduca sexta phenol oxidase: Purification, activation, substrate specificity of the active enzyme, and molecular cloning. Proc Natl Acad Sci U S A 52:7764-7768.
41. Hart K, Wilcox M (1993): A Drosophila gene encoding an epithelial membrane protein with homology to CD36/LIMP II. J Mol Biol 234:249-253.
42. Hecker H (1977): Structure and function of midgut epithelial cells in Culicidae mosquitoes (Insecta, Diptera). Cell Tissue Res 184:321-341.
43. Hoffmann JA (1995): Innate immunity of insects. Curr Opin. Immunol 7:4-10.
44. Huber M, Cabib E, Miller LH (1991): Malaria parasite chitinase and penetration of the mosquito peritrophic membrane. Proc Natl Acad Sci U S A 88:2807-2810.
45. James AA (1994): Molecular and biochemical analysis of the salivary glands of vector mosquitoes. Bull Inst Pasteur 92:133-150.
46. Kawabata T, Yashuhara Y, Ochiai M, Matsuura S, Ashida M (1995): Molecular cloning of insect pro-phenol oxidase: A cooper-containing protein homologous to arthropod hemocyanin. Proc Natl Acad Sci U S A 92:7774-7778.
47. Kilama WL, Craig GB Jr (1969): Monofactorial inheritance of susceptibility to Plasmodium gallinaceum in Aedes aegypti. Ann Trop Med Parasitol 63:419-432.
48. Kotani E, Yamakawa M, Iwamoto S, Tashiro M, Mori H, Sumida M, Matsubara F, Taniai K, Kadono-Okuda K, Kato Y, Mori H (1995): Cloning and expression of the gene of hemocytin, an insect lectin which is homologous with the mammalian von Willebrand factor. Biochim Biophys Acta 1260:245-258.
49. Kumar VK, Collins FH (1994): A technique for nucleic acid in situ hybridization to polytene chromosomes of mosquitoes in the Anopheles gambiae complex. Insect Mol Biol 3:41-47.
50. Lanzaro GC, Zheng L, Toure YT, Traore SF, Kafatos FC, Vernick KD (1995): Microsatellite DNA and isozyme variability in a West African population of Anopheles gambiae. Insect Mol Biol 4:105-112.
51. Law JH, Ribeiro JMC, Wells MA (1992): Biochemical insights derived from insect diversity. Annu Rev Biochem 61:87-111.
52. Loukeris TG, Livadaras I, Area B, Zabalou S, Savakis C (1995): Gene transfer into the medfly, Ceratitis capitata, with a Drosophila hydei transposable element. Science 270:2002-2005.
53. Lowenberger C, Bulet P, Charlet M, Hetru C, Hodgeman B, Christensen BM, Hoffman JA (1995): Insect immunity: Isolation of three novel inducible antibacterial defensins from the vector mosquito, Aedes aegypti. Insect Biochem Mol Biol 25:867-873.
54. MacDonald WW, Ramachandran CP (1965): The influence of the gene fm (filarial susceptibility, Burgia malayi) on the susceptibility of Aedes aegypti to seven strains of Brugia, Wuchereria and Dirofilaria. Ann Trop Med Parasitol 59:64-73.
55. Meis JFGM, Pool G, Gemert GJV, Lensen AHW, Ponudurai T, Meuissen JHET (1989): Plasmodium falciparum ookinetes migrate intercellularly through Anopheles stephensi midgut epithelium. Parasitol Res 76:13-19.
56. Miller BR, Mitchell CJ (1991): Genetic selection of a flavivirus-refractory strain of the yellow fever mosquito Aedes aegypti. Am J Trop Med Hyg 45:399-407.
57. Miller N, Lehane MJ (1993): Peritrophic membranes, cell surface molecules and parasite tropisms within arthropod vectors. Parasitol Today 9:45-50.
58. Müller H-M, Crampton JM, della Torre A, Sinden R, Crisanti A (1993): Members of a trypsin gene family in Anopheles gambiae are induced in the gut by blood meal. EMBO J 12:2891-2900.
59. Nappi AJ, Vass E, Frey F, Carton Y (1995): superoxide anion generation in Drosophila during melanotic encapsulation of parasites. Eur J Cell Biol 68:450-456.
60. Noriega FG, Wang X-Y, Pennington JE, Barillas-Mury CV, Wells MA (in press): Early trypsin, a female-specific midgut protease in Aedes aegypti: Isolation, amino-terminal sequence determination, and cloning and sequencing of the gene. Insect Biochem Mol Biol 26:119-126.
61. O'Brien SJ (1993): Genetic Maps: Locus Map of Complex Genomes, 6th ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
62. Olson KE, Higgs S, Gaines PJ, Powers AM, Davis BS, Kamrud KI, Carlson JO, Blair CD, Beaty BJ (1996): Genetically engineered resistance to Dengue-2- virus transmission in mosquitoes. Science 272:884-886.
63. Paskewitz SM, Riehle MA (1994): Response of Plasmodium refractory and susceptible strains of Anopheles gambiae to inoculated Sephadex beads. Dev Comp Immunol 18:369-375.
64. Paskewitz SM, Brown MR, Lea AO, Collins FH (1988): Ultrastructure of the encapsulation of Plasmodium cynomolgi (B strain) on the midgut of a refractory strain of Anopheles gambiae. J Parasitol 74:432-439.
65. Paskewitz SM, Brown MR, Collins FH, Lea AO (1989): Ultrastructural localization of phenoloxidase in the midgut of refractory Anopheles gambiae and association of the enzyme with encapsulated Plasmodium cynomolgi. J Parasitol 75:594-600.
66. Pearson A, Lux A, Krieger M (1995): Expression cloning of dSR-CI, a class C macrophage-specific scavenger receptor from Drosophila melanogaster. Proc Natl Acad Sci U S A 92:4056-4060.
67. Perrone JB, Spielman A (1988): Time and site of assembly of the peritrophic membrane of the mosquito Aedes aegypti. Cell Tissue Res 252:473-478.
68. Powers AM, Olson KE, Higgs S, Carlson JO, Beaty BJ (1994): Interference to La Crosse virus superinfection by an antisense RNA generated from an infectious Sindbis virus vector. Virus Res 32:57-67.
69. Powers AM, Kamrud KI, Olson KE, Higgs S, Carlson JO, Beaty BJ (1996): Molecularly engineered resistance to California serogroup virus replication in mosquito cells and mosquitoes. Proc Natl Acad Sci U S A 93:4187-4191.
70. Raghavan N, Freedman DO, Fitzgerald PC, Unnasch TR, Ottesen EA, Nutman TB (1994): Cloning and characterization of a potentially protective chitinase-like recombinant antigen from Wuchereria bancrofti. Infect Immun 62:1901-1908.
71. Ratcliffe NA, Leonard C, Rowley AF (1984): Prophenoloxidase activation: Nonself recognition and cell cooperation in insect immunity. Science 226:557-559.
72. Richman A, Kafatos FC (1995): Immunity to eukaryotic parasites in vector insects. Curr Opin. Immunol 8:14-19.
73. Richman AM, Bulet P, Hetru C, Barillas-Mury C, Hoffmann JA, Kafatos FC (1996): Inducible immune factors of the vector mosquito Anopheles gambiae: Biochemical purification of a defensin antibacterial peptide and molecular cloning of preprodefensin cDNA. Insect Mol Biol 5:203-210.
74. Robson KJ, Frevert U, Rechmann I, Cowan G, Beier J, Scragg IG, Takehara K, Bishop DH, Pradel G, Sinden R, Saccheo S, Müller H-M, Crisanti A (1995): Thrombospondin-related adhesive protein (TRAP) of Plasmodium falciparum: Expression during sporozoite ontogeny and binding to human hepatocytes. EMBO J 14:3883-3894.
75. Rodriguez MDC, Zamudio F, Torres JA, Gonzalez-Ceron L, Possani LD, Rodriguez MH (1995): Effect of a cecropin-like synthetic peptide (Shiva-3) on the sporogonic development of Plasmodium berghei. Exp Parasitol 80:596-604.
76. Romans P, Seeley DC, Kew Y, Gwadz RW (1991): Use of restriction fragment length polymorphism (RFLP) as a genetic marker in crosses of Anopheles gambiae (Diptera: Culicidae): Independent assortment of a diphenol oxidase RFLP and an esterase locus. J Med Entomol 28:147-151.
77. Rosenberg R (1985): Inability of Plasmodium knowlesi sporozoites to invade Anopheles freeborni salivary glands. Am J Trop Med Hyg 34:687-691.
78. Russo J, Dupas S, Frey F, Carton Y, Brehelin M (1996): Insect immunity: Early events in the encapsulation process of parasitoid (Leptopilina boulardi) eggs in resistant and susceptible strains of Drosophila. Parasitology, 112:135-142.
79. Saiki RK, Gelfand DH, Toffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KB, Erlich HA (1988): Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239:487-491.
80. Severson DW (1994): Applications of molecular marker analysis to mosquito vector competence. Parasitol Today 10:336-340.
81. Severson DW, Mori A, Zhang Y, Christensen BM (1993): Linkage map for Aedes aegypti using restriction fragment length polymorphisms. J Hered 84:241-247.
82. Severson DW, Mori A, Zhang Y, Christensen BM (1994): Chromosomal mapping of two loci affecting filarial worm susceptibility in Aedes aegypti. Insect Mol Biol 3:67-73.
83. Severson DW, Mori A, Kassner VA, Christensen BM (1995a): Comparative linkage maps for the mosquitoes, Aedes albopictus and Ae. aegypti, based on common RFLP loci. Insect Mol Biol 4:41-45.
84. Severson DW, Thathy V, Mori A, Zhang Y, Christensen BM (1995b): Restriction fragment length polymorphism mapping of quantitative trait loci for malaria susceptibility in the mosquito Aedes aegypti. Genetics 139:1711-1717.
85. Shahabuddin M, Toyoshima T, Aikawa M, Kaslow DC (1993): Transmission-blocking activity of a chitinase inhibitor and activation of malaria parasite chitinase by mosquito protease. Proc Natl Acad Sci U S A 90:4266-4270.
86. Shahabuddin M, Kaidoh T, Aikawa M, Kaslow DC (1995a): Plasmodium gallinaceum: Mosquito peritrophic matrix and the parasite-vector compatibility. Exp Parasitol 81:386-393.
87. Shahabuddin M, Marsha C, Kaslow DC (1995b): Unique specificity of in vitro inhibition of mosquito midgut trypsin-like activity correlates with in vivo inhibition of malaria parasite infectivity. Exp Parasitol 80:2312-219.
88. Sieber KP, Huber M, Kaslow D, Banks SM, Torii M, Aikawa M, Miller LH (1991): The peritrophic membrane as a barrier: Its penetration by Plasmodium gallinaceum and the effect of a monoclonal antibody to ookinetes. Exp Parasitol 72:145-156.
89. Smartt CT, Kim AP, Grossman G, James AA (1995): The apyrase gene of the vector mosquito, Aedes aegypti is expressed specifically in the adult female salivary glands. Exp Parasitol 81:239-248.
90. Stark KR, James AA (1995): A factor Xa-directed anticoagulant from the salivary glands of the yellow fever mosquito Aedes aegypti. Exp Parasitol 81:321-331.
91. Sterling CR, Aikawa M, Vanderberg JP (1973): The passage of Plasmodium berghei sporozoites through the salivary glands of Anopheles stephensi: An electron microscope study. J Parasitol 59:593-605.
92. Sutherland DR, Christensen BM, Lasee BA (1986): Midgut barrier as a possible factor in filarial worm vector competency in Aedes trivittatus. J Invert Pathol 47:1-7.
93. Syafruddin, Arakawa R, Kaminura K, Kawamoto F (1991): Penetration of the mosquito midgut wall by the ookinetes of Plasmodium yoelii nigeriensis. Parasitol Res 77:230-236.
94. Titus RG, Ribeiro JMC (1988): Salivary gland lysates from the sand fly Lutzomyia longipalpis enhance Leishmania infectivity. Science 239:1306-1308.
95. Torii M, Nakamura K-I, Sieber KP, Miller LM, Aikawa M (1992): Penetration of the mosquito (Aedes aegypti) midgut wall by the ookinetes of Plasmodium gallinaceum. J Protozool 39:449-454.
96. Touray MG, Warburg A, Laughinghouse A, Krettli AU, Miller LH (1992): Developmentally regulated infectivity of malaria sporozoites for mosquito salivary glands and the vertebrate host. J Exp Med 175:1607-1612.
97. Vernick KD, Collins FH (1989): Association of a Plasmodium-refractory phenotype with an esterase locus in Anopheles gambiae. Am J Trop Med Hyg 40:593-597.
98. Vernick KD, Collins FH, Gwadz RW (1989): A general system of resistance to malaria infection in Anopheles gambiae controlled by two main genetic loci. Am J Trop Med Hyg 40:585-592.
99. Vernick KD, Fujioka H, Seeley DC, Tandler B, Aikawa M, Miller LH (1995): Plasmodium gallinaceum: A refractory mechanism of ookinete killing in the mosquito, Anopheles gambiae. Exp Parasitol 80:583-595.
100. Wallis GP, Aitken THG, Beaty BJ, Lorenz L, Amato GD, Tabachnick WJ (1985): Selection for susceptibility and refractoriness of Aedes aegypti to oral infection with yellow fever virus. Am J Trop Med Hyg 34:1225-1231.
101. Walters LL, Irons KP, Guzman H, Tesh RB (1995): Peritrophic envelopes of Lutzomyia spinicrassa (Diptera: Psychodidae). J Med Entomol 32:711-725.
102. Wang Y, Willott E, Kanost MR (1995): Organization and expression of the hemolin gene, a member of the immunoglobulin superfamily in an insect, Manduca sexta. Insect Mol Biol 4:113-123.
103. Warburg A, Miller LH (1992): Sporogonic development of a malaria parasite in vitro. Science 255:448-450.
104. Warburg A, Touray M, Krettli AU, Miller LM (1992): Plasmodium gallinaceum: Antibodies to circumsporozoite protein prevent sporozoites from invading the salivary glands of Aedes aegypti. Exp Parasitol 75:303-307.
105. Warburg A, Saraiva E, Lanzaro GC, Titus RG, Neva F (1994): Saliva of Lutzomyia longipalpis sibling species differs in its composition and capacity to enhance leishmaniasis. Philos Trans R Soc Lond [Biol] 345:223-230.
106. Willott E, Trenczek T, Thrower LW, Knost MR (1994): Immunochemical identification of insect hemocyte populations: Monoclonal antibodies distinguish four major hemocyte types in Manduca sexta. Eur J Cell Biol 65:417-423.
107. Zheng L, Saunders RDC, Fortini D, dell Torre A, Coluzzi M, Glover DM, Kafatos FC (1991): Low resolution genome map of the malaria mosquito Anopheles gambiae. Proc Natl Acad Sci U S A 88:11187-11191.
108. Zheng L, Collins FH, Kumar V, Kafatos FC (1993): A detailed genetic map for the X chromosome of the malaria vector, Anopheles gambiae. Science 261:605-608.
109. Zheng L, Whang LH-S, Kumar V, Kafatos FC (1995): Two genes encoding midgut-specific maltase-like polypeptides from Anopheles gambiae. Exp Parasitol 81:272-283.
110. Zheng L, Benedict MQ, Cornel AJ, Collins FH, Kafatos FC (in press): An integrated genetic map of the African human malaria vector mosquito, Anopheles gambiae. Genetics 143:941-952.
111. Zwiebel LJ, Saccone G, Zacharopoulou A, Besansky NJ, Favia G, Collins FH, Louis C, Kafatos FC (1995): The white gene of Ceratitis capitata: A phenotype marker for germline transformation. Science 270:2005-2008.