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Adapted Western Corn Rootworm (Diabrotica Virgifera Virgifera L.)

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Adapted Western Corn Rootworm (Diabrotica Virgifera Virgifera L.) ARTICLE IN PRESS Insect Biochemistry and Molecular Biology 38 (2008) 697– 704 Contents lists available at ScienceDirect Insect Biochemistry and Molecular Biology journal homepage: www.elsevier.com/locate/ibmb Increased expression of a cGMP-dependent protein kinase in rotation- adapted western corn rootworm (Diabrotica virgifera virgifera L.) Freydoun Garabagi a, B. Wade French c, Arthur W. Schaafsma b, K. Peter Pauls b,à a Department of Enviromental Biology, University of Guelph, Guelph, Ont., Canada N1G 2W1 b Department of Plant Agriculture, University of Guelph, Guelph, Ont., Canada N1G 2W1 c North Central Agricultural Research Laboratory, USDA, 2923 Medary Avenue, Brookings, SD 57006, USA article info abstract Article history: A new ‘variant’ behavior in western corn rootworm (WCR) has resulted in egg-laying into non- Received 21 June 2007 cornfields, compared to ‘normal’ deposition of eggs in cornfields, allowing these insects to circumvent Received in revised form crop rotation. No morphological or genetic characteristics have been defined to differentiate between 3 March 2008 the normal and variant biotypes. Cyclic GMP-dependent protein kinases (PKG) have been implicated in Accepted 29 March 2008 the regulation of behaviors in vertebrates, insects, and nematodes, including foraging behavior in Drosophila. A cDNA with homology to the Drosophila melanogaster foraging gene (called Dvfor1)was Keywords: cloned from WCR. The deduced DvFOR1 protein is approximately 70% similar to FOR proteins in Real-time PCR Drosophila, silkworm (Bombyx mori) and honeybee (Apis mellifera). It contains a coiled-coil region, two PKG tandem cyclic nucleotide-binding domains, a serine/threonine kinase catalytic domain, and a serine/ Foraging gene Ovipositioning threonine kinase catalytic domain extension, which are all characteristically found in PKG proteins. Diabrotica virgifera Real-time PCR assays of foraging transcript levels in heads of normal and rotation adapted females of Variant WCR obtained from lab-reared insect colonies indicated that the variants had higher levels (25%) of PKG expression than normals. The magnitude of this increase is similar to that observed in Drosophila rover phenotypes compared to sitter phenotypes. However, Diabrotica contains at least two different foraging gene transcripts, which complicates establishing a direct link between the level of gene expression and insect behavior. & 2008 Elsevier Ltd. All rights reserved. 1. Introduction rotation was losing its effectiveness in certain counties of eastern Illinois and there were increasing reports of major WCR damage to Western corn rootworm (WCR), Diabrotica virgifera virgifera first-year corn (Levine and Oloumi-Sadeghi, 1996). This unex- LeConte, has been a major pest of corn for over 50 years. The pected damage occurred because of the emergence of a new annual pest management (mainly soil insecticides) and yield loss behavior in WCR that was prompting the insects to lay eggs costs for WCR have been estimated to approximate 1 billion outside of cornfields (O’Neal et al., 1999). Because the non-corn dollars annually in the United States (Sappington et al., 2006), and fields were rotated back to corn in the following year, the over 260 million dollars in Canada during the mid 1980s (Madder abnormal egg-laying behavior provided the emerging larvae, the et al., 1988). Corn rootworms have been controlled effectively corn roots they require in the following year. The conditions that through crop rotation since the early 20th century, reducing their might have selected for this altered behavior are not certain but economic importance significantly (Schaafsma et al., 1999). might include high population densities (Onstad et al., 1999), WCR pass through only one generation per year and usually shifts in corn phenology (Darnell et al., 2000), and restricted oviposit in cornfields in late summer and fall. The larvae that cultural practices such as a high percentage of fields in corn/ emerge the following spring are obligate corn root feeders, soybean rotation (Onstad et al., 2001). therefore, planting a non-host crop such as soybeans after corn There are no phenotypic or morphological characteristics that is an effective management tool (Krysan and Branson, 1983). Crop can be used to distinguish rotation-adapted WCRs from their rotation strategies are based on the assumption that WCRs normal counterparts. The lack of a simple and quick diagnostic oviposit solely in cornfields. However, in the early 1990s, crop tool for identifying the variant insects makes it difficult to monitor their field occurrence in areas that are known to contain the variant insect, as well as in areas where the insect is expected to à Corresponding author. Tel.: +1519 824 4120x52460; fax: +1519 763 8933. spread. Accurate identification of a population of variant WCR in E-mail address: [email protected] (K. Peter Pauls). cornfields, through a genetic-based system, would allow corn 0965-1748/$ - see front matter & 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.ibmb.2008.03.011 ARTICLE IN PRESS 698 F. Garabagi et al. / Insect Biochemistry and Molecular Biology 38 (2008) 697–704 producers to implement alternative strategies to rotation to 3 min and cooled to room temperature. The reaction was control the pest. In a series of behavioral assays, Knolhoff et al. incubated at 37 1C for 30 min with 200 units SuperscriptII Reverse (2006) showed that D. v. virgifera females from lab-reared insects Transcriptase, 100 mM DTT, 2 mM dNTPs, 4 units RNaseOUT, in a that were originally collected from regions where crop rotation is 1  RT buffer (50 mM Tris–HCl, pH 8.3, 75 mM KCl, 3 mM MgCl2; no longer effective are more active than females collected from Invitrogen, Carlsbad, CA), followed by 90 1C for 10 min for enzyme regions where rotation remains effective. Based on differences inactivation. observed between normal and rotation-resistant populations of A clustalW multi-nucleotide alignment of published insect PKG beetles in similar environments, the authors suggest a genetic genes identified a highly conserved serine/threonine domain in these component as the underlying cause of this change in behavior but sequences (http://clustalw.genome.jp/; data not shown). Primers, no specific gene or genes were identified. designed on the basis of the Drosophila serine/threonine kinase Cyclic GMP-dependent protein kinases (PKG) have been domain (Dm-FOR-F 50-CGCCAGTGCTTTCAGACCATCATGATG-30,Dm- implicated in the regulation of behavioral processes in the FOR-R 50-GCGTCTCCACAATCTGTGACTTTTTCATCTG-30)wereusedto vertebrates, insects, and nematodes (Schafer, 2002). One exten- amplify a 650 bp fragment of the foraging gene from WCR cDNA. The sively studied example is the Drosophila PKG that was first presence of multiple stretches of sequence containing greater than identified as the foraging gene. The foraging gene has two naturally three guanine or cytosine nucleotides (particularly in the 50 region of occurring alleles that manifest in two food search behavioral the gene) made it difficult to amplify fragments larger than 700 bp. As phenotypes, named rover and sitter (Pereira and Sokolowski, a result, the complete foraging gene cDNA was compiled from four 1993; Sokolowski et al., 1997; Osborne et al., 1997). When placed overlapping pieces. A second internal fragment was cloned in the 50 into a patch of food, both larvae and adult rovers have long direction, utilizing a B. mori-based forward primer and a reverse foraging paths and have a greater tendency to leave the patch primer based on the newly obtained WCR sequence. The BD SMART compared to sitters, which have short foraging paths and less RACE cDNA Amplification Kit (BD Biosciences, Palo Alto, CA) was tendency to leave the food patch. The foraging gene is alternately utilized, as described by the manufacturer, to obtain the full-length 50 spliced to create three major transcripts with varying lengths, and 30 ends of the transcript. The primary fragments amplified by the namely T1, T2, and T3, as well as several minor transcripts kit were very faint and needed to be subjected to an extra round of (Kalderon and Rubin, 1989). Small differences in the abundance of re-amplification after gel purification. The 50 RACE reaction generated the T1 message between rovers and sitters account for the a truncated fragment, which required a second round of 50 RACE for observed behavioral variation (Osborne et al., 1997). The sitters acquiring the full-length sequence. were shown to have slightly (11%) lower levels of foraging transcript as well as PKG protein levels and enzyme activity. Rover insects could be converted by mutation to sitters by down regulating the foraging gene, or by treating them with inhibitors 2.2. Southern hybridization of PKG. The involvement of PKG in food search behavior has been Genomic DNA was extracted and pooled from thoraxes of demonstrated in several insects, including honeybee (Apis melli- normal and variant WCR female and male adults to obtain a total fera L., Ben-Shahar et al., 2002), red harvester ant (Pogonomyrmex of 30 mg. Genomic DNA was digested overnight with 100 units of barbatus Smith, Ingram et al., 2005), silkworm (Bombyx mori L., EcoRI (Invitrogen) at 37 1C, separated on an 1% agarose gel, Tanoue and Nishioka, 2003) as well as in the nematode transferred to a nylon membrane, and probed at high stringency Caenorhabditis elegans, Maupas, Daniels et al., 2000). In honeybee, with the DIG non-radioactive detection system (Roche Diagnostics up regulation of Amfor
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