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Differentiation Between Aphis Pomi and Aphis Spiraecola Using Multiplex Real-Time PCR Based on DNA Barcode Sequences A

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Differentiation Between Aphis Pomi and Aphis Spiraecola Using Multiplex Real-Time PCR Based on DNA Barcode Sequences A J. Appl. Entomol. ORIGINAL CONTRIBUTION Differentiation between Aphis pomi and Aphis spiraecola using multiplex real-time PCR based on DNA barcode sequences A. M. Naaum1, R. G. Foottit2, H. E. L. Maw2 & R. Hanner1 1 Department of Integrative Biology, University of Guelph, Guelph, Ontario, Canada 2 Agriculture and Agri-Food Canada, Invertebrate Biodiversity, National Environmental Health Program, Ottawa, Ontario, Canada Keywords apple aphid, pest identification, TaqMan Abstract The green apple aphid (Aphis pomi) and the spirea aphid (Aphis spiraeco- Correspondence la) are pests of apples in North America. Although management regimes Amanda M. Naaum (Corresponding author), Department of Integrative Biology, University exist to effectively control these pests, they differ significantly because of Guelph, 50 Stone Road. E., Guelph, Ontario of varying susceptibility of each species to common pesticides and differ- N1G 2W1, Canada. ences in their life cycles. Therefore, accurate identification of the species E-mail: [email protected] present is essential for pest control. However, the identification process is complicated because of the morphological similarity between these Received: September 21, 2011; accepted: two species. As a result, confusion between A. pomi and A. spiraecola January 5, 2011. often occurs. DNA barcoding has been proven to accurately identify spe- doi: 10.1111/j.1439-0418.2012.01706.x cies of Aphididae. A further study demonstrated that DNA barcodes could be used to accurately differentiate A. pomi and A. spiraecola. DNA barcoding represents an important step towards rapid identification of these pests as distinctions can be easily made between morphologically similar species as well as from eggs and immature individuals in addition to adults. However, samples must still be sent to specially equipped facil- ities for sequence analysis, which can take between several hours and days. Real-time PCR is emerging as a useful tool for more rapid pest identification. The purpose of this study was to develop a real-time PCR assay for differentiation of A.pomi from A. spiraecola based on DNA bar- code sequences from the Barcode of Life Data System. This assay was designed on the portable SmartCycler II platform and can be used in field settings to differentiate these species quickly and accurately. It has the potential to be a valuable tool to improve pest management of A. pomi and A. spiraecola. their life cycles (Foottit et al. 2009). Therefore, accu- Introduction rate identification of the species present is essential The green apple aphid (Aphis pomi De Geer 1783) for pest control. However, the identification process and the spirea aphid (Aphis spiraecola Patch 1914) are is complicated because of the morphological similar- pests of apples in North America (Foottit et al. ity between these two species. As a result, confusion 2006). They play a role in disease transmission between A. pomi and A. spiraecola often occurs (Blackman and Eastop 2000) and affect healthy (Blackman and Eastop 2000; Foottit et al. 2009). growth of their hosts (Kaakeh et al. 1993). Although DNA barcoding using the 5¢ end of the mitochon- management regimes exist to effectively control drial cytochrome C oxidase I (COI) gene (Hebert these pests, they differ significantly because of vary- et al. 2003) has been proven to accurately identify ing susceptibility of each species to common pesti- most species of Aphididae (Foottit et al. 2008; Lee cides (Lowery et al. 2005, 2006) and differences in et al. 2011). A further study demonstrated that DNA 704 J. Appl. Entomol. 136 (2012) 704–710 ª 2012 Blackwell Verlag, GmbH A. M. Naaum et al. Differentiation between Aphis pomi and Aphis spiraecola barcodes could be used to accurately differentiate Aphididae’. These sequences were derived from indi- between A. pomi and A. spiraecola (Foottit et al. viduals collected over a wide geographical range. Pri- 2009). DNA barcoding represents an important step mer and probe design was based on all unique towards rapid identification of these pests as distinc- haplotypes from this project. Haplotype analysis was tions can be easily made between morphologically carried out using the haplotype variation tool at similar species as well as from eggs and immature ibarcode.org. In total, 209 unique haplotypes were individuals in addition to adults based on sequence used for primer and probe design, including a single differences as demonstrated recently in cereal aphids haplotype of A. pomi from four individuals collected (Shufran and Puterka 2011). However, samples must from Canada and the US and a single haplotype of still be sent to specially equipped facilities for A. spiraecola from 11 individuals collected from Can- sequence analysis, which can take between several ada, the United States, Palau, Marshall Islands, hours and days. Hawaii and Guam. Primers and probes were also Real-time PCR is emerging as a reliable method tested for specificity against sequences from unique for pest insect identification (Huang et al. 2010; haplotypes of A. spiraecola from the public BOLD Walsh et al. 2005; Yu et al. 2005; Madani et al. project ‘Aphis Species on Apple (A. pomi, A. spiraeco- 2005). These assays can produce results much la)’. These haplotypes were identical to the haplo- quicker than traditional barcoding, often in 1 h, and types used in primer and probe design at the primer the results are simple to interpret. The one-step pro- and probe sites. Primers and probes (Table 1) were cess not only reduces the length of time required to developed using AlleleID (version 7.7; Premier Bio- identify specimens, but also reduces the chance of soft International, Palo Alto, CA, USA). The A. pomi contamination by eliminating the post-PCR process- -specific probe was tagged at the 5¢ end with the ing steps necessary for DNA barcoding. In addition fluorescent reporter tetrachloro-6-carboxyfluorescein to being more rapid than DNA barcoding, some real- (TET) and at the 3¢ end with Black Hole Quencher-1 time PCR platforms are portable. Paired with the use (BHQ-1) quenching dye. The A. spiraecola -specific of lyophilized reagents, this would allow accurate probe was tagged with the fluorescent reporter 6-carb- identification in field settings, eliminating the need oxyfluorescein (FAM) at the 5¢ end, and BHQ-1 at the to send samples off-site. 3¢ end. Optimization of probe and primer concentra- Species-specific primers and probes for use with tions and cycling conditions was carried out according real-time PCR can be designed using the DNA bar- to the guidelines set by Cepheid for the Smart Cycler code sequences of target species in publically avail- II System (SmartNote 6.2; http://www.cepheid.com/ able projects in the Barcode of Life Data System systems-and-software/smartcycler-system/). (BOLD; http://www.boldsystems.org; Ratnasingham and Hebert 2007). Using sequences from related Species selection and sample collection individuals to avoid cross-amplification with other species is an important aspect of primer and probe A number of species with various degrees of related- design. As errors arising from misidentification are ness to the target species were selected for specific- often found in GenBank (Harris 2003; Vigalys 2003), ity testing, following the classification scheme of the use of sequences from vouchered specimens in BOLD can lead to more accurate primer and probe design. The objective of this study was to create a real-time PCR assay for accurate and rapid differenti- Table 1 Sequences of species-specific oligonucleotides used in this ation of A. pomi and A. spiraecola, based on COI DNA study and respective amplicon length. All primers and probes target barcode sequences from BOLD, to be run on a porta- portions of the C oxidase I DNA barcode region ble platform. Aphis Aphis pomi spiraecola Material and Methods Forward primer TGCCCAGATATA GAGCAATTAATTTT sequence (5¢-3¢) TCTTTCC ATTTGTACA Multiplex PCR Primer and probe design Reverse primer CCTGTTCCT GCTAGAACTGGTAGAGA Species-specific primers and TaqMan probes were sequence (5¢-3¢) GTTCCATTA developed for Aphis pomi and Aphis spiraecola using Probe sequence TET-AGATTCTGATTATT 6FAM-TTAAATCAAAT (5¢-3¢) ACCGCCTTCACT-BHQ1 CCCACTATTTCCATG-BHQ1 690 COI barcode sequences from 338 species in the Amplicon Length 110 base pairs 130 base pairs publically available BOLD project ‘Barcoding the J. Appl. Entomol. 136 (2012) 704–710 ª 2012 Blackwell Verlag, GmbH 705 Differentiation between Aphis pomi and Aphis spiraecola A. M. Naaum et al. Remaudie`re and Remaudie`re (1997). The following according to manufacturer guidelines. PCR cycling species were selected: other species of genus Aphis conditions were as follows: an initial step of 95°C for (Aphis coreopsidis (Thomas), Aphis craccivora Koch, 120 s, followed by 40 cycles of 94°C for 11 s, 60°C Aphis fabae Scopoli, Aphis farinose Gmelin, Aphis gly- for 40 s and 72°C for 25 s. Fluorescence readings cines Matsumura, Aphis gossypii Glover, Aphis helianthi were taken at the annealing step of each cycle. All Monell in Riley and Monell, Aphis hyperici Monell in reactions were carried out on the SmartCycler II Riley and Monell, Aphis illinoisensis Shimer, Aphis im- platform (Cepheid). The cycle threshold (Ct) value patientis Thomas, Aphis lugentis Williams, Aphis macu- was determined as the number of cycles at which latae Oestlund, Aphis nasturtii Kaltenbach, Aphis the fluorescence reading exceeded the detection neilliae Oestlund, Aphis neogillettei Palmer, Aphis nerii threshold. If no signal was observed, a Ct value
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