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The Ceratotoxin Gene Family in the Medfly Ceratitis Capitata and The Heredity (2003) 90, 382–389 & 2003 Nature Publishing Group All rights reserved 0018-067X/03 $25.00 www.nature.com/hdy The ceratotoxin gene family in the medfly Ceratitis capitata and the Natal fruit fly Ceratitis rosa (Diptera: Tephritidae) M Rosetto1,3, D Marchini1, T de Filippis1, S Ciolfi1, F Frati1, S Quilici2 and R Dallai1 1Department of Evolutionary Biology, University of Siena, Siena, Italy; 2CIRAD-FLHOR, Laboratoire d’Entomologie, Saint-Pierre, France Ceratotoxins (Ctxs) are a family of antibacterial sex-specific with an anti-Ctx serum. Four nucleotide sequences encoding peptides expressed in the female reproductive accessory Ctx-like precursors in C. rosa were determined. Sequence glands of the Mediterranean fruit fly Ceratitis capitata.Asa and phylogenetic analyses show that Ctxs from C. rosa fall first step in the study of molecular evolution of Ctx genes in into different groups as C. capitata Ctxs. Our results suggest Ceratitis, partial genomic sequences encoding four distinct that the evolution of the ceratotoxin gene family might be Ctx precursors have been determined. In addition, anti- viewed as a combination of duplication events that occurred Escherichia coli activity very similar to that of the accessory prior to and following the split between C. capitata and C. gland secretion from C. capitata was found in the accessory rosa. Genomic hybridization demonstrated the presence of gland secretion from Ceratitis (Pterandrus) rosa. SDS–PAGE multiple Ctx-like sequences in C. rosa, but low-stringency analysis of the female reproductive accessory glands from C. Southern blot analyses failed to recover members of this rosa showed a band with a molecular mass (3 kDa) gene family in other tephritid flies. compatible with that of Ctx peptides, also slightly reacting Heredity (2003) 90, 382–389. doi:10.1038/sj.hdy.6800258 Keywords: female-specific peptides; antibacterial peptides; insect immunity; molecular evolution; gene duplication Introduction previously isolated (Rosetto et al, 1997). One of the genes encoded a second form of Ctx A precursor protein, The female reproductive accessory glands of the Medi- named Ctx A2. Two genes encoding Ctx C (C1 and C2) terranean fruit fly Ceratitis capitata (family Tephritidae) were also found. The other gene in the cluster encoded a produce a secretion with antibacterial properties, partly novel peptide of the same family, named Ctx D. The due to the presence of short cationic antibacterial genes corresponding to the previously sequenced Ctx A peptides named Ceratotoxins (Ctxs) (Marchini et al, and B cDNAs were not present in the isolated genomic 1991, 1993). Three peptides, named Ctxs A, B and C, clone. Indeed, genomic Southern blot analysis showed were previously isolated from the gland secretion, and the presence of additional Ctx genes that may have their amino-acid and cDNA nucleotide sequences were included A and B mapping outside the sequenced cluster determined (Marchini et al, 1993, 1995; Rosetto et al, 1996). (Rosetto et al, 1997). The analysis of polytene and mitotic Unlike most insect antibacterial peptides, Ctxs are not chromosomes by in situ hybridization showed that induced by bacterial infection, but they are expressed in Ctx genes map on the X chromosome (Rosetto et al, the female reproductive accessory glands of adult insects 2000), the first report of a female-specific X-linked gene (Marchini et al, 1995; Rosetto et al, 1996) in response to in C. capitata. juvenile hormone stimulation (Manetti et al, 1997). Since In this paper, we report the partial genomic sequences Ctxs are produced only after sexual maturity is achieved, encoding two Ctx A and two Ctx B precursors. We also their possible physiological role could be related to the report the detection of Ctx-like peptides in the female protection of the female reproductive tract from bacterial accessory gland secretion of the Natal fruit fly Ceratitis invasion during mating. However, the presence of (Pterandrus) rosa and the partial nucleotide sequences biologically active Ctx peptides on the laid egg surface encoding four of them. Phylogenetic analysis has been suggests at least a function of Ctxs in protecting embryos performed to investigate the pattern of evolution of the and early larvae from environmental bacteria (Marchini Ctx genes from C. capitata and their evolutionary et al, 1997, 2002). relations with the homologous genes from C. rosa. A genomic clone containing four clustered genes encoding different members of the Ctx family has been Materials and methods Correspondence: R Dallai, Department of Evolutionary Biology, Via A. Insects Moro 2, University of Siena, I-53100 Siena, Italy. E-mail: [email protected] 3Current address: Department of Environmental Sciences, Univer- C. capitata flies were reared in standard laboratory sity of Tuscia, Viterbo, Italy conditions, at 231C, 70% relative humidity and 14:10 Received 15 July 2002; accepted 17 January 2003 light–dark regime (Rabossi et al, 1991). Adult specimens Evolution of ceratotoxins in C. capitata and C. rosa M Rosetto et al 383 of C. rosa were reared from pupae collected from infested Hasegawa method (SH test: Shimodaira and Hasegawa, fruits of guava (Psidium guajava L.) in two localities in the 1999) as implemented in PAUP*, using RELL (10 000 south of Reunion Island (Bassin Martin, Ravine des bootstrap replicates). Cabris, France), in the Indian Ocean. Bactrocera (Dacus) The possible occurrence of selection was tested by oleae pupae were collected from olive fruits in Puglia calculating the ratio between the number of nonsynon- (southern Italy). Rhagoletis pomonella pupae were col- ymous (dN) and synonymous (dS) substitutions using the lected from Crataegus mollis in East Lansing (Michigan Nei and Gojobori (1986) method as implemented in State). Anastrepha fraterculus pupae were collected from MEGA, version 2.0 (Kumar et al, 2001). infested fruits of Psidium guajava in Louveira, Sao Paulo State, Brazil. Anastrepha obliqua pupae were collected Recovery of female accessory gland secretion and from Psidium guajava in Bauru, Sao Paulo State, Brazil. protein assay Adults were maintained in the laboratory as reported Accessory glands from sexually mature C. capitata and C. above for C. capitata. rosa females were dissected, homogenized in Eppendorf tubes with Eppendorf micropestles and centrifuged DNA isolation, sequencing and Southern blot analysis essentially as described in Marchini et al (1989) and Genomic DNA was extracted from adult flies according Rosetto et al (1996). The supernatant, containing the to the method described by Sambrook et al (1989). To secretion in 100 mM Na-phosphate buffer at pH 6.8 (PB) isolate Ctx sequences, PCR reactions were performed (1 gland equivalent/1–4 ml PB), was freeze-dried and using approximately 300 ng of genomic DNA, and stored at À201C. The protein content of the accessory degenerate primers encoding the amino- and carboxyl- gland secretion was determined according to Bradford terminal ends of Ctx precursor peptides: 50-TTCAC- (1976) using BSA as a standard. CATGGCMAAYMTTAAAGCT-30 (primer 1) and 50-MYWYWTTATCCTACAAGH-30 (primer 2). C. rosa Assay for antibacterial activity Ctx sequences were amplified using primer 1 and Escherichia coli LE 392, cultured in Luria–Bertani medium 50-CAATGGGKAWGGCGAYCTTDSCAA-30 (primer 3). (Sambrook et al, 1989), was used as a test organism to Amplification reactions were performed as follows: five assay antibacterial activity. Inhibition zone assay was cycles of 941C for 1 min, 501C for 2 min, 721C for 2 min, carried out as previously reported (Faye and Wyatt, 1980; followed by 40 cycles of 941C for 1 min, 351C for 2 min Marchini et al, 1997), using a chemically synthesized Ctx and 721C for 2 min. An extension at 721C for 10 min was A 1-36 (Dompe´ S.p.A., Milano, Italy) as a control of added at the end of the reaction. The amplification antibacterial activity. products were inserted into the Bluescript II SK (À) vector (Stratagene). Nucleotide sequences were deter- Electrophoresis and Western blot analysis mined by the MWG-BIOTECH automated DNA Sequen- SDS–PAGE was performed according to Laemmli (1970). cing Service (Ebersberg, Germany). Tubulin-specific Low molecular weight markers were purchased from primers were used in PCR reactions to control the Promega. Chemically synthesized Ctx A 1-36 and Ctx C intactness of genomic DNA. Southern blot analysis was 1-32 (Dompe´ S.p.A., Milano, Italy) were also used as performed with genomic DNA digested with Eco RI and markers. After electrophoresis, proteins were transferred Eco RV restriction enzymes, run on 1% agarose gel and onto a nitrocellulose filter (Bioblot-NC, Costar) as then transferred to a Protran nitrocellulose transfer described by Towbin et al (1979). Ctxs were detected as membrane (Schleicher & Schuell GmbH, Dassel, Ger- previously reported (Marchini et al, 1995): filters were many). A Ctx A cDNA probe (Marchini et al, 1995) was soaked for 30 min in 16 mM PB, pH 7.4, 150 mM NaCl 32P-labeled by random priming using the Prime-a-gene containing 3% BSA and 0.1% Triton X-100 (PBSAT) and kit (Promega). High-stringency hybridization was per- incubated overnight with an anti-Ctx serum (Marchini formed overnight at 651C in 300 mM NaCl, 30 mM et al, 1995), diluted 1:200 in PBSAT. The second antibody sodium citrate, pH 7.0 (2 Â SSC), 1 Â Denhardt’s (goat anti-rabbit IgG, 1:1000 dilution, horseradish perox- solution and 50 mg/ml salmon sperm DNA. The filter idase conjugated, Cappel) was applied after rinsing of was washed twice in 2 Â SSC, 0.1% SDS for 5 min at the filters with PBSAT. The color reaction was developed room temperature, and then three times at 651C for by 4-chloro-1-naphthol (Sigma) in 50 mM Tris-HCl, pH 30 min in the same solution. Low-stringency hybridiza- 6.8 and stopped with distilled water. tion and washes were performed at 501Cin4Â SSC. Results Nucleotide sequence analysis Sequences were aligned with Clustal W (Thompson et al, Isolation of novel Ctx sequences in C.
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