Expressed sequence tags from Atta laevigata and identification of candidate genes for the control of pest leaf-cutting ants
© Bacci et al; licensee BioMed Central Ltd. 2011
Received: 15 November 2010
Accepted: 17 June 2011
Published: 17 June 2011
Leafcutters are the highest evolved within Neotropical ants in the tribe Attini and model systems for studying caste formation, labor division and symbiosis with microorganisms. Some species of leafcutters are agricultural pests controlled by chemicals which affect other animals and accumulate in the environment. Aiming to provide genetic basis for the study of leafcutters and for the development of more specific and environmentally friendly methods for the control of pest leafcutters, we generated expressed sequence tag data from Atta laevigata, one of the pest ants with broad geographic distribution in South America.
The analysis of the expressed sequence tags allowed us to characterize 2,006 unique sequences in Atta laevigata. Sixteen of these genes had a high number of transcripts and are likely positively selected for high level of gene expression, being responsible for three basic biological functions: energy conservation through redox reactions in mitochondria; cytoskeleton and muscle structuring; regulation of gene expression and metabolism. Based on leafcutters lifestyle and reports of genes involved in key processes of other social insects, we identified 146 sequences potential targets for controlling pest leafcutters. The targets are responsible for antixenobiosis, development and longevity, immunity, resistance to pathogens, pheromone function, cell signaling, behavior, polysaccharide metabolism and arginine kynase activity.
The generation and analysis of expressed sequence tags from Atta laevigata have provided important genetic basis for future studies on the biology of leaf-cutting ants and may contribute to the development of a more specific and environmentally friendly method for the control of agricultural pest leafcutters.
The tribe Attini comprises over 200 ant species  which culture mutualistic fungi for their feeding . The most evolutionary derived attines are the leaf-cutting ants in the genera Atta and Acromyrmex which are considered major herbivores in the tropics .
Some Atta species contributes to nutrient cycling, aeration and drainage of water in the soil , as well as maintenance of plant diversity [5, 6]. Their nests were also found to host arthropods [7–9], reptiles and amphibians , and microorganisms [10–14].
However, despite of these ecological roles, many leafcutter species are considered agricultural pests which impose severe economic damages to agriculture [15, 16]. Some of the characteristics contributing to the pest status of leafcutters are their ability of exploiting a great variety of plant species , reaching high population density  and long life spanning queens constantly laying eggs for up to 15 years .
Atta laevigata is a pest leafcutter distinguished by a very large and shiny head in soldiers, a characteristic which has rendered the species with the popular name "cabeça de vidro" (meaning glass head). It can be found in Venezuela, Colombia, Guyana, Bolivia, Paraguay and, in Brazil, from the Amazonian Rain Forest in the North to the Paraná state in the South . It cuts leaves from many plantations, like pine tree , cocoa  and eucalyptus , as well as wide variety of native plants from different biomes such as the Cerrado or the Rain Forest, where its intense herbivory challenges reforestation of degraded areas [23, 24].
The control of pest leafcutters in small properties can be done by biological methods  or even utilizing the waste material generated by the ants , but in extensive monocultures this control utilizes massive amounts of broad spectrum insecticides which are toxic to other animals and persist in the environment . Thus, the development of a more specific and environmentally friendly process for controlling the leafcutters is required .
Genomic studies can contribute with that by characterizing genes involved in key functions for the leafcutters, like longevity, fertility and plasticity to exploit different vegetations, raising more specific targets for the ant control. Genomics is also a valuable resource for ecological and evolutionary studies of leaf-cutting ants.
In the present investigation, we carried out a genomic study in the pest leafcutter Atta laevigata by generating 3,203 expressed sequence tags (ESTs) which characterized 2,006 unique sequences (US). We postulate important differences in expression level among the transcripts and identified 146 potential target sequences for the control of pest leaf-cutting ants.
Two grams of soldiers and major workers of Atta laevigata were macerated under liquid nitrogen, total RNA was extracted with the TRIzol method (Invitrogen, UK) and mRNA was purified using the PolyATract System (Promega, USA). The CloneMiner cDNA Library Construction Kit (Invitrogen, UK) and 2 μg of mRNA were utilized for the synthesis of first and second cDNA strands which were then size-fractioned in a 1.0 ml Sephacryl S-500 resin column, inserted in a pDONR222 plasmid (Invitrogen, UK) and transformed into DH10B Escherichia coli. Cells were plated onto solid Circle Grow medium (QBIO-GENE, Canada) containing 25 μg.ml-1 kanamicin and individually picked into a permanent culture plate with 96 wells. After 22 hours growth in liquid Circle Grow medium (25 mg.ml-1 kanamicin), plasmid DNA was purified by alkaline lysis  and sequenced in reactions containing 300 ng template DNA, 5 pmol M13 forward primer and the DYEnamic ET Dye Terminator kit reactant (GE Healthcare, UK), according to the manufacturer's protocol. The amplified products were resolved in a MEGA-BACE 1000 automated DNA sequence machine (GE Healthcare, UK).
The pipeline generation system EGene  was used to clean and assemble ESTs in contigs and singlets. Sequences were filtered by quality using phred values >20 and 90% of minimum identity percent in window. Filtered sequences were then masked against vector and primer sequences, selected by size (>100 bp) and assembled using CAP3  with an overlap percent identity cutoff (p) of 90 and a minimum overlap length cutoff (o) of 50.
The program Blast2GO (B2G)  was used to associate every Atta laevigata singlet and contig to blastx  results (nr protein database; E-value ≤ 10-5), Gene Ontology (GO) terms , InterProScan classification [35, 36] including signal peptide  and transmembrane regions predictions, Kyoto Encyclopedia of Genes and Genomes (KEGG) maps (http://www.genome.jp/kegg/), and Enzyme Commission (EC) numbers (IUBMB). The results generated by B2G and those obtained from Conserved Domain Database (CCD) were manually inspected, in order to group contigs and singlets in functional categories and to infer transcript abundance in Atta laevigata.
Results and Discussion
EST generation and assembly
Filtered by quality
Filtered by size
High-quality (after filtering)
Unique Sequences (US)
The high-quality sequences were assembled in 340 contigs (619 bp average) and 1,666 singlets which we assume to represent 2,006 unique sequences (US). It is likely that some of the US came from the same gene due to non-overlapping ESTs from a single gene or products of alternative splicing .
Comparative analysis of Atta laevigata genes
The number of US per category gives us an idea on the diversity of genes existing in each cell function. This diversity was found high within transcripts related with signaling pathways, membrane or regulation of gene expression, but very low within transcripts related to secondary metabolism, cuticular and peritrophic membranes or homeobox.
Variation of the number of reads per contig
Contigs with high read number in the Atta laevigata cDNA library.
Best hit (organism)
COX I (Myrmica rubra)
Similar to paramyosin CG5939-PA (Apis mellifera)
ATP synthase F0 subunit 6 (Camponotus sayi)
COX III (Bombyx mandarina)
Similar to muscle protein 20 CG4696-PA (Apis mellifera)
COX II (Atta colombica)
Actin-5 (Bactrocera dorsalis)
Similar to limpet CG32171-PD (Apis mellifera)
Muscle LIM protein (Nasonia vitripennis)
Cytochrome b (Formica pratensis)
Similar to muscle LIM protein at 84B (Apis mellifera)
Similar to CG5023-PA (Apis mellifera)
Troponin I (Apis mellifera)
Similar to muscle LIM protein at 84B (Apis mellifera)
NADH dehydrogenase subunit 4 (Harpiosquilla harpax)
AGAP005400-PA (Anopheles gambiae)
Identification of candidate genes for the control of pest leafcutters
Inhibition of the translation of genes which play essential functions in insects by feeding these insects with dsRNA  or using transgenic plants  seems a promising procedure for the control of agricultural pests . One of the advantages of this procedure is that it targets mRNA molecules which may be species-specific.
Candidate genes for the control of pest leafcutter ants.
Process [GenBank Acc*]
Cytochrome P450 activity
Development and longevity
Development, growth and differentiation
[JI332430- JI332440, JI332711-JI332736]
Oxidative stress protection
Juvenile hormone binding and synthesis
Immunity and resistance to pathogens
Serine protease inhibitor
Melanization and pathogen encapsulation
Communication [JI332453-JI332457, JI332762-JI332767]
Pheromone/odorant binding and transport
Generation and stability of signaling
[JI332458, JI332459, JI332768-JI332773]
Courtship and behavior
[JI332460, JI332461, JI332774-JI332782]
Learning and memory
Polysaccharide metabolism [JI332462, JI332463, JI332783]
Glycogen and starch degradation
Intermediary metabolism [JI332464, JI332465]
Arginine kynase activity
The function and potential utilization of these 146 US as targets for the control of pest leafcutters are considered below.
Cytochrome P450, carboxylesterases, and glutathione transferases are involved in insecticide metabolism . In insects, P450 also participates in the metabolism of many endogenous (including juvenile hormones, ecdysteroids, and pheromones) and exogenous compounds (plant allelochemicals and insecticides) .
The enzyme glutathione S-transferase catalyzes the initial conjugation of insecticides with glutathione. Both enzyme and glutathione are very abundant in the cells and essential for detoxification of electrophiles causing cytotoxic or genotoxic damage . The enzyme may play a role in insecticide resistance , herbicide resistance in plants , resistance of cancer cells to chemotherapeutic agents , and antibiotic resistance in bacteria . In our study we found 25 US in the cytochrome P450 family and 12 US probably related with detoxification of xenobiotics, including glutathione S-transferase, glutamate cysteine ligase and aldehyde oxidase (Table 3). All these genes may be important targets for the control of leafcutters.
Development and longevity genes
Of the 18 US we found (Table 3) involved with development, growth and differentiation, four are putatively related with nervous system development, two of which contained the immunoglobulin domain: one wrapper one lachesin homolog. The protein lachesin has a role in early neuronal differentiation as well in axon outgrowth, cell recognition events, cell adhesion or intercellular communication . The other 14 US in this category (Table 3) may be involved in different phases of insect development like egg, or larvae, or development of tissues or organs like mesoderma, spermatechae and antennae.
Queen and worker ants develop from identical eggs, being genetically identical, but the caste system produces a long-lived queen and a short-lived worker with up to ten-fold lifespan differences . Harman  stated that lifespan is determined by the rate at which oxidative damage occurs due to the accumulation of by-products of oxidative energy metabolism. Harman's theory implicates that long-lived organisms produce fewer reactive oxygen species or have increased antioxidant production , although the degree of lifespan extension can be sex- or genotype-specific  and sometimes poorly correlated with antioxidant levels .
We found 13 US likely involved in organism lifespan by protection from oxidative stress (Table 3) and which are directly involved in the degradation of superoxide radicals and hydrogen peroxide or neutralization of reactive oxygen species, such as the putative Cu/Zn superoxide dismutase, catalase, Rpd3 histone deacetylase, peroxiredoxin 5, thioredoxin reductase and phospholipid hydroperoxide glutathione peroxidase.
Our library contained four US putatively coding for juvenile hormone binding protein (JHBP) domain and two for putative proteins that participate in JHBP biosynthesis (Table 3). Juvenile hormones (JH) regulate a great number of physiological processes in insect development. Larvae requires JH to maintain larval state and JH must be absent in the last larval instar for metamorphosis to start [57, 58]. They are also necessary for reproduction in adults .
The characterization of genes which are related to development and longevity in Atta laevigata allows future investigation on the effect of the expression of these genes on queen maturation and lifespan, which are a key features associated with leafcutter pest ability.
Genes associated with immunity and resistance to pathogens
Pathogens, parasites or injury triggers in insects innate immune responses that are in essence similar and comprise both cellular and humoral components. Cellular mechanisms include phagocytosis by special blood cells and encapsulation of large invaders . Humoral responses involve events of proteolytic cascades leading to melanization  and the production of antimicrobial peptides initiated via two distinct signaling pathways, Toll and Immune Deficiency, which depend on the pathogen recognition . There are two types of recognition proteins: peptidoglycan recognition proteins and Gram-negative bacteria-binding proteins.
We found 37 US that may be involved with immunity or pathogen resistance (Table 3), including the putative toll like interacting protein, prophenoloxidase subunit 3 and easter CG4920-PA, the last two with role in melanin synthesis. We also found sequences putatively coding for the antimicrobial peptides hymenoptaecin and defensin 2, and for the peptidoglycan recognition protein precursor, as well as transferrin and transferrin 2 which participate in response to microbial infection by sequestering iron that is an essential nutrient for some pathogens .
Leaf-cutting ants and their mutualistic fungus are constantly challenged by pathogenic microorganisms  which ultimately regulate host population . Therefore, the 37 US we found probably involved in resistance to microbial pathogens are important markers for understanding antimicrobial mechanisms in leafcutters and putative targets for controlling pest leafcutters.
Communication plays a central part in social insects necessary for division of labor and task partitioning which are essential for harvesting food, nursing the broods and sexual reproduction . Thus, targeting genes involved in communication seems a promising strategy for the control of leaf-cutting ants.
Our library contained 11 US probably related to communication, one of them putatively coding for the pheromone binding protein (PBP), which is important for chemical recognition of insect conspecifics by transporting odorant molecules from cuticular pores to receptors . In Solenopsis invicta, the gene Gp-9, which is a PBP homolog, seems to have a role in worker ability to discriminate queens and regulate their numbers . Other important communication gene found putatively codes for fatty acid binding protein involved in transport of communication molecules in insects .
Four of the communication US we found were in the lipocalin family which is composed of secreted proteins binding small hydrophobic molecules or forming macromolecular complexes associated with cell surface receptors important for transport, pheromone signaling and olfaction . These sequences putatively code for the odorant binding proteins, apolipophorin III or PP238.
We also found three homologs to the chemosensory protein from Nasonia vitripennis, chemosensory protein 2 from Apis mellifera and chemosensory protein 5 from Bombyx mori. Chemosensory proteins may be specifically expressed in sensory organs which are important in ant behavior  and participate in cellular processes that require lipophilic compounds .
The putative genes gustatory receptor and dihidrooratate dehydrogenase involved in odorant reception in insects were also found.
Tetraspanin is an important signaling membrane protein expressed in antennae of moths and honeybees , being a molecular facilitator of signal transduction and cell adhesion . In our library, six US putatively coding for tetraspanin were present.
We also found two US corresponding to nicotinic acetylcholine receptor which plays a role in visual processing, learning and memory, olfactory signal processing, and mechanosensory antennal input in honeybee . These receptors are targets of neonicotinoids insecticides used against piercing-sucking pests .
Eleven Atta laevigata US in this category (Table 3) were homolog to genes involved in behavior, learning, memory and courtship in Apis mellifera, Drosophila melanogaster or Solenopsis invicta. Some of the genes controlling social behavior and complex tasks or abilities may be specific to Hymenoptera  and thus may be specific targets for the control of pest leafcutters.
Polysaccharide metabolism genes
Food sources for worker leafcutters relies mostly on the plant polysaccharides cellulose, xylane and starch, which are degraded by extracellular enzymes secreted by the mutualistic fungus , generating mono and disaccharides readily assimilated by the ants . Degradation of cellulose by the mutualistic fungus generates cellobiose  and degradation of starch generates maltose, both disaccharides being consumed by leafcutters  through the production of alpha- and beta-glucosidase, respectively. In addition, workers assimilate starch at certain extent , which demands production of alpha-amylase.
Our library contained 59 US (Figure 3) corresponding to genes related to carbohydrate metabolism, including alpha-glucosidase-like, beta-glucosidase and alpha-amylase (Table 3) which are promising targets for leafcutters control.
Arginine kinase gene
Arginine kinase catalyses the reversible transfer of phosphate between ATP and guanidine substrates and acts in cells that need readily available energy sources . This enzyme activity in cockroaches was found to be inhibited by nitrates and borates  which were then used as insecticides. Our library contained two US which are putative arginine kinase genes (Table 3) that may also be important for the control of leafcutters.
The 146 US here proposed as targets for the control of leaf-cutting ants can be used for primer designing in order to study gene expression through real time PCR. For instance, over-expression of sequences here proposed as related to immunity or antixenobiosis in A. laevigata challenged by pathogens or insecticides should validate the protective role of the respective gene products in leafcutters exposed to adverse conditions, helping us to understand the molecular basis of pest ant resistance to hazardous chemicals. A future scenario can be envisaged in which inhibition of gene expression, gene translation or the related protein activities would make pest leafcutters more susceptible to pathogens, insecticides or anti-herbivory chemicals produced by crops. In summary, inhibition of genes or gene products related to the processes described in Table 3 may specifically hamper the colonization of crop areas by pest leafcutters.
Leaf-cutting ants are the major neotropical herbivores, many of which are important agricultural pests. We characterized 2,006 unique sequences (US) in Atta laevigata, one of the most geographically spread pest leaf-cutting ant in South America, and found that 16 of the genes are likely under positively selected high expression and responsible for energy conservation or cell structuring or regulation. Another set of 146 US which play important part in anti-xenobiosis, longevity, immunity, development, communication, nutrition or insecticide action were identified as putative targets for the control of pest leafcutters. Our findings provided genetic background for basic and applied studies on these ants.
List of abbreviation used
- EST :
Expressed Sequence Tags
- US :
- mRNA :
- cDNA :
- bp :
- B2G :
- nr :
- GO :
- KEGG :
Kyoto Encyclopedia of Genes and Genomes
- EC :
- IUBMB :
International Union of Biochemistry and Molecular Biology
- CDD :
Conserved Domain Database
- JHBP :
juvenile hormone binding protein
- JH :
- PBP :
pheromone binding protein
- PCR :
polymerase chain reaction.
We thank CAPES, CNPq 476250/2008-0 and 304661/2009-0 and FAPESP 2008/54386-9 for financial support as well as the trainees Alexandre H Takara, Cristiane P Garcia, Pamella A Malagrino, Rafael B Souza, Fernando K Cochi and Washington Luiz Pires for clone picking and miniprep and Caio C Batista for computational support.
- Bolton BA, Alpert G, Ward PS, Naskrecki P: Bolton's catalogue of ants of the world: 1758-2005. 2006, Cambridge: Harvard University PressGoogle Scholar
- Mueller UG, Schultz TR, Currie CR, Adams RM, Malloch D: The origin of the attine ant-fungus mutualism. Q Rev Biol. 2001, 76: 169-97. 10.1086/393867.PubMedView ArticleGoogle Scholar
- Hölldobler B, Wilson EO: The Ants. 1990, Massachusetts: Belknap Press of Harvard UniversityView ArticleGoogle Scholar
- Weber NA: Gardening ants: the Attines. 1972, Philadelphia: The American Philosophical SocietyGoogle Scholar
- Garrettson M, Stetzel JF, Halpern BS, Hearn DJ, Lucey BT, McKone MJ: Diversity and abundance of understorey plants on active and abandoned nests of leaf-cutting ants (Atta cephalotes) in a Costa Rican rain forest. J Trop Ecol. 1998, 14: 17-26. 10.1017/S0266467498000029.View ArticleGoogle Scholar
- Wirth R, Herz H, Ryel RJ, Beyschlag W, Hölldobler B: Herbivory of leaf-cutting ants. A case study on Atta colombica in the tropical rain forest of Panama. 2003, Berlin: SpringerView ArticleGoogle Scholar
- Moser JC, Neff SE: Pholeomyia comans (Diptera: Milichiidae) an associate of Atta texana: larval anatomy and notes on biology. Z Angew Entomol. 1971, 69: 343-348.View ArticleGoogle Scholar
- Steiner WE: The first records of Bycrea villosa Pascoe (Coleoptera: Tenebrionidae) in the United States, Central America and Colombia and notes on its association with leaf-cutting ants. Coleopterists Bulletin. 2004, 58: 329-334. 10.1649/619.View ArticleGoogle Scholar
- Waller DA, Moser JC: Invertebrate enemies and nest associates of the leaf cutting ant Atta texana (Buckley) (Formicidae, Attini). Applied myrmecology: a world perspective. Edited by: Vander Meer RK, Jaffe K, Cedeño A. Boulder. 1990, Colorado: Westview Press, 255-273.Google Scholar
- Bacci M, Anversa MM, Pagnocca FC: Cellulose degradation by Leucocoprinus gongylophorus, the fungus cultured by the leaf-cutting ant Atta sexdens rubropilosa. Antonie van Leeuwenhoek Int J Gen Mol Microbiol. 1995, 67: 385-386. 10.1007/BF00872939.View ArticleGoogle Scholar
- Carreiro SC, Pagnocca FC, Bacci M, Lachance MA, Bueno OC, Hebling MJA, Ruivo CCC, Rosa CA: Sympodiomyces attinorum sp nov., a yeast species associated with nests of the leaf-cutting ant Atta sexdens. Int J Syst Evol Microbiol. 2004, 54: 1891-1894. 10.1099/ijs.0.63200-0.PubMedView ArticleGoogle Scholar
- Currie CR: A community of ants, fungi, and bacteria: A multilateral approach to studying symbiosis. Annu Rev Microbiol. 2001, 55: 357-380. 10.1146/annurev.micro.55.1.357.PubMedView ArticleGoogle Scholar
- Rodrigues A, Pagnocca FC, Bacci M, Hebling MJA, Bueno OC, Pfenning LH: Variability of non-mutualistic filamentous fungi associated with Atta sexdens rubropilosa nests. Folia Microbiol. 2005, 50: 421-425. 10.1007/BF02931424.View ArticleGoogle Scholar
- Pinto-Tomás AA, Anderson MA, Suen G, Stevenson DM, Chu FST, Cleland WW, Weimer PJ, Currie CR: Symbiotic nitrogen fixation in the fungus gardens of leaf-cutter ants. Science. 2009, 326: 1120-1123. 10.1126/science.1173036.PubMedView ArticleGoogle Scholar
- Fowler HG, Silva VP, Saes NB: Population dynamics of leaf-cutting ants: a brief review. Fire ants and leaf-cutting ants: biology and management. Edited by: Lofgren CS, Vander Meer RK. 1986, Boulder, Colorado: West-View Press, 123-145.Google Scholar
- Cameron RS: Distribution, impact and control of the Texas leaf-cutting ant: 1983 survey results. 1985, Texas Forest Service PublicationGoogle Scholar
- Vasconcelos HL: Foraging activity of two species of leaf-cutting ants (Atta) in a primary Forest of the Central Amazon. Insectes Soc. 1990, 37: 131-145. 10.1007/BF02224026.View ArticleGoogle Scholar
- Keller L: Queen lifespan and colony characteristics in ants and termites. Insectes Soc. 1998, 45: 235-246. 10.1007/s000400050084.View ArticleGoogle Scholar
- Borgmeier T: Estudos sobre Atta (Hym. Formicidae). Memórias do Instituto Oswaldo Cruz. 1950, 48: 239-263.PubMedView ArticleGoogle Scholar
- Hernández JV, Jaffé K: Economic damage caused by leaf-cutting ant populations of Atta laevigata (F. Smith) on pine plantations (Pinus caribaeae Mor.) and elements for managing of the pest. An Soc Entomol. 1995, 24: 287-298.Google Scholar
- Delabie JHC: The ant problems of cocoa farms in Brazil. Applied myrmecology: a world perspective. Edited by: Vander Meer RK, Jaffe K, Cedeño A. Boulder. 1990, Colorado USA: Westview Press, 555-569.Google Scholar
- Zanetti R, Zanuncio JC, Souza-Silva A, Mendonça LA, Mattos JOS, Rizental MS: Efficiency of products for thermonebulization on the control of Atta laevigata (Hymenoptera: Formicidae) in eucalypus plantations. Ciênc Agrotec. 2008, 32: 1313-1316. 10.1590/S1413-70542008000400043.View ArticleGoogle Scholar
- Vasconcelos HL, Cherret JM: Leaf-cutting ants and early Forest regeneration in central Amazonia: effects of herbivory on the seedling establishment. J Trop Ecol. 1977, 13: 357-370.View ArticleGoogle Scholar
- Viana LR, Santos JC, Arruda LJ, Santos GP, Fernandes GW: Foraging patterns of the leaf-cutter ant Atta laevigata (Smith) (Myrmicinae: Attini) in an area of cerrado vegetation. Neotrop Entomol. 2004, 33: 391-393. 10.1590/S1519-566X2004000300019.View ArticleGoogle Scholar
- Michels K, Cromme N, Glatzle A, Schultze-Kraft R: Biological Control of Leaf-Cutting Ants Using Forage Grasses: Nest Characteristics and Fungus Growth. J Agron Crop Sci. 2001, 187: 259-267. 10.1046/j.1439-037X.2001.00528.x.View ArticleGoogle Scholar
- Ballari SA, Farji-Brener AG: Refuse dumps of leaf-cutting ants as a deterrent for ant herbivory: does refuse age matter?. Entomol Exp Appl. 2006, 121: 215-219. 10.1111/j.1570-8703.2006.00475.x.View ArticleGoogle Scholar
- Ying GG, Kookana RS: Persistence and movement of fipronil termiticide with under slab and trenching treatments. Environ Toxicol Chem. 2006, 25: 2045-2050. 10.1897/05-652R.1.PubMedView ArticleGoogle Scholar
- Ambrozin ARP, Leite AC, Bueno FC, Vieira PC, Fernandes JB, Bueno OC, Silva MFGF, Pagnocca FC, Hebling MJA, Bacci M: Limonoids from andiroba oil and Cedrela fissilis and their insecticidal activity. J Braz Chem Soc. 2006, 17: 542-547.View ArticleGoogle Scholar
- Vettore AL, Silva FR, Kemper EL, Arruda P: The libraries that made SUCEST. Genet Mol Biol. 2001, 24: 1-7. 10.1590/S1415-47572001000100002.View ArticleGoogle Scholar
- Durham AM, Kashiwabara AY, Matsunaga FT, Ahagon PH, Rainone F, Varuzza L, Gruber A: EGene: a configurable pipeline generation system for automated sequence analysis. Bioinformatics. 2005, 21: 2812-2813. 10.1093/bioinformatics/bti424.PubMedView ArticleGoogle Scholar
- Huang X, Madan A: CAP3: A DNA sequence assembly program. Genome Res. 1999, 9: 868-877. 10.1101/gr.9.9.868.PubMedPubMed CentralView ArticleGoogle Scholar
- Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M: Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005, 21: 3674-3676. 10.1093/bioinformatics/bti610.PubMedView ArticleGoogle Scholar
- Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25: 3389-3402. 10.1093/nar/25.17.3389.PubMedPubMed CentralView ArticleGoogle Scholar
- Gene Ontology Consortium: The Gene Ontology (GO) project in 2006. Nucleic Acids Res. 2006, 34: D322-326.PubMed CentralView ArticleGoogle Scholar
- Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R: InterProScan: protein domains identifier. Nucleic Acids Res. 2005, 33: W116-120. 10.1093/nar/gki442.PubMedPubMed CentralView ArticleGoogle Scholar
- Zdobnov EM, Apweiler R: InterProScan - an integration platform for the signature-recognition methods in InterPro. Bioinformatics. 2001, 17: 847-848. 10.1093/bioinformatics/17.9.847.PubMedView ArticleGoogle Scholar
- Emanuelsson O, Brunak S, Heijne G, Nielsen H: Locating proteins in the cell using TargetP, SignalP, and related tools. Nat Protoc. 2007, 2: 953-971. 10.1038/nprot.2007.131.PubMedView ArticleGoogle Scholar
- Wang J, Jemielity S, Paolo U, Wurm Y, Gräff J, Keller L: An annotated cDNA library and microarray for large-scale gene-expression studies in the ant Solenopsis invicta. Genome Biol. 2007, 8: R9-10.1186/gb-2007-8-1-r9.PubMedPubMed CentralView ArticleGoogle Scholar
- The Honeybee Genome Sequencing Consortium: Insights into social insects from the genome of the honeybee Apis mellifera. Nature. 2006, 443: 931-949. 10.1038/nature05260.PubMed CentralView ArticleGoogle Scholar
- The Nasonia Genome Working Group: Functional and Evolutionary Insights from the Genomes of Three Parasitoid Nasonia Species. Science. 2010, 327: 343-348. 10.1126/science.1178028.PubMed CentralView ArticleGoogle Scholar
- Wagner A: Energy costs constrain the evolution of gene expression. J Exp Zool (Mol Dev Evol). 2007, 308: 322-324.View ArticleGoogle Scholar
- Zhu F, Xu J, Palli R, Ferguson J, Palli SR: Ingested RNA interference for managing the populations of the Colorado potato beetle, Leptinotarsa decemlineata. Pest Manag Sci. 2011, 67: 175-182. 10.1002/ps.2048.PubMedView ArticleGoogle Scholar
- Barbosa AEAD, Albuquerque EVS, Silva MCM, Souza DSL, Oliveira-Neto OB, Valencia A, Rocha TL, Grossi-de-Sa MF: α-amylase inhibitor-1 gene from Phaseolus vulgaris expressed in Coffea arabica plants inhibits α-amylases from the coffee berry borer pest. BMC Biotechnol. 2010, 10: 44-10.1186/1472-6750-10-44.PubMedPubMed CentralView ArticleGoogle Scholar
- Huvenne H, Smagghe G: Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: a review. J Insect Physiol. 2010, 56: 227-235. 10.1016/j.jinsphys.2009.10.004.PubMedView ArticleGoogle Scholar
- Ranson H, Claudianos C, Ortelli F, Abgrall C, Hemingway J, Sharakhova MV, Unger MF, Collins FH, Feyereisen R: Evolution of supergene families associated with insecticide resistance. Science. 2002, 298: 179-181. 10.1126/science.1076781.PubMedView ArticleGoogle Scholar
- Hodgson E: Microsomal mono-oxygenases. Comprehensive Insect Physiology Biochemistry and Pharmacology. Edited by: Kerkut GA, Gilbert LC. 1985, Oxford: Pergamon Press, 647-712.Google Scholar
- Ketterer B, Coles B, Meyer DJ: The role of glutathione in detoxication. Environ Health Perspect. 1983, 49: 59-69.PubMedPubMed CentralView ArticleGoogle Scholar
- Ranson H, Rossiter L, Ortelli F, Jensen B, Wang X, Roth CW, Collins FH, Hemingway J: Identification of a novel class of insect glutathione S-transferases involved in resistance to DDT in the malaria vector Anopheles gambiae. Biochem J. 2001, 359: 295-304. 10.1042/0264-6021:3590295.PubMedPubMed CentralView ArticleGoogle Scholar
- Hatton PJ, Cummins I, Cole DJ, Edwards R: Glutathione transferases involved in herbicide detoxification in the leaves of Setaria faberi (giant toxtail). Physiol Plant. 1999, 105: 9-16. 10.1034/j.1399-3054.1999.105103.x.View ArticleGoogle Scholar
- Hayes JD, Pulford DJ: The glutathione S-transferase supergene family: regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit Rev Biochem Mol Biol. 1995, 30: 445-600. 10.3109/10409239509083491.PubMedView ArticleGoogle Scholar
- Arca P, Hardisson C, Suarez J: Purification of a glutathione S-transferase that mediates fosfomycin resistance in bacteria. Antimicrob Agents Chemother. 1997, 34: 844-848.View ArticleGoogle Scholar
- Karlstrom RO, Wilder LP, Bastiani MJ: Lachesin: an immunoglobulin superfamily protein whose expression correlates with neurogenesis in grasshopper embryos. Development. 1993, 118: 509-522.PubMedGoogle Scholar
- Harman D: Aging: a theory based on free radical and radiation chemistry. J Gerontol. 1956, 11: 298-300.PubMedView ArticleGoogle Scholar
- Corona M, Hughes KA, Weaver DB, Robinson GE: Gene expression patterns associated with queen honey bee longevity. Mech Ageing Dev. 2005, 126: 1230-1238. 10.1016/j.mad.2005.07.004.PubMedView ArticleGoogle Scholar
- Spencer CC, Howell CE, Wright AR, Promislow DE: Testing an 'aging gene' in long-lived Drosophila strains: increased longevity depends on sex and genetic background. Aging Cell. 2003, 2: 123-130. 10.1046/j.1474-9728.2003.00044.x.PubMedPubMed CentralView ArticleGoogle Scholar
- Perez-Campo R, Lopez-Torres M, Cadenas S, Rojas C, Barja G: The rate of free radical production as a determinant of the rate of aging: evidence from the comparative approach. J Comp Physiol. 1998, 168: 149-158.View ArticleGoogle Scholar
- Riddiford LM: Cellular and molecular actions of juvenile hormone I. General considerations and premetamorphic actions. Adv Insect Physiol. 1994, 24: 213-274.View ArticleGoogle Scholar
- Truman JW, Riddiford LM: The origins of insect metamorphosis. Nature. 1999, 401: 447-452. 10.1038/46737.PubMedView ArticleGoogle Scholar
- Wyatt GR, Davey KG: Cellular and molecular action of juvenile hormone II. Roles of juvenile hormone in adult insects. Adv Insect Physiol. 1996, 26: 1-155.View ArticleGoogle Scholar
- Gillespie JP, Kanost MR, Trenczed T: Biological mediators of insect immunity. Annu Rev Entomol. 1997, 42: 611-643. 10.1146/annurev.ento.42.1.611.PubMedView ArticleGoogle Scholar
- Ferrandon D, Imler JL, Hetru C, Hoffmann JA: The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat Rev Immunol. 2007, 7: 862-874. 10.1038/nri2194.PubMedView ArticleGoogle Scholar
- Nichol H, Law JH, Winzerling JJ: Iron metabolism in insects. Annu Rev Entomol. 2002, 47: 535-559. 10.1146/annurev.ento.47.091201.145237.PubMedView ArticleGoogle Scholar
- Rodrigues A, Bacci M, Mueller UG, Ortiz A, Pagnocca FC: Microfungal Weeds in the Leafcutter Ant Symbiosis. Microb Ecol. 2008, 56: 604-614. 10.1007/s00248-008-9380-0.PubMedView ArticleGoogle Scholar
- Poulin R, Morand S: Parasite biodiversity. 2004, Washington: Smithsonian BooksGoogle Scholar
- Jackson DE, Ratnieks FLW: Communication in ants. Curr Biol. 2006, 16: 570-574. 10.1016/j.cub.2006.01.064.PubMedView ArticleGoogle Scholar
- Vogt RG: The molecular basis of pheromone reception: its influence on behavior. Pheromone Biochemistry. Edited by: Prestwich GD, Blomquist GJ. 1987, New York: Academic Press, 385-431.Google Scholar
- Krieger MJB, Ross KG: Identification of a Major Gene Regulating Complex Social Behavior. Science. 2002, 295: 328-332. 10.1126/science.1065247.PubMedView ArticleGoogle Scholar
- Kamikouchi A, Morioka M, Kubo T: Identification of honeybee antennal proteins/genes expressed in a sex- and/or caste selective manner. Zool Sci. 2004, 21: 53-62. 10.2108/0289-0003(2004)21[53:IOHAGE]2.0.CO;2.PubMedView ArticleGoogle Scholar
- Flower DR: The lipocalin protein family: structure and function. Biochem J. 1996, 318: 1-14.PubMedPubMed CentralView ArticleGoogle Scholar
- Ozaki M, Wada-Katsumata A, Fujikawa K, Iwasaki M, Yokohari F, Satoji Y, Nisimura T, Yamaoka R: Ant nestmate and non-nestmate discrimination by a chemosensory sensillum. Science. 2005, 309: 311-314. 10.1126/science.1105244.PubMedView ArticleGoogle Scholar
- Forêt S, Wanner KW, Maleszka R: Chemosensory proteins in the honey bee: Insights from the annotated genome, comparative analysis and expressional profiling. Insect Biochem Mol Biol. 2007, 37: 19-28. 10.1016/j.ibmb.2006.09.009.PubMedView ArticleGoogle Scholar
- Todres E, Nardi JB, Robertson HM: The tetraspanin superfamily in insects. Insect Mol Biol. 2000, 9: 581-590. 10.1046/j.1365-2583.2000.00222.x.PubMedView ArticleGoogle Scholar
- Maecker HT, Todd SC, Levy S: The tetraspanin superfamily: molecular facilitators. FASEB J. 1997, 11: 428-442.PubMedGoogle Scholar
- Thany SH, Crozatier M, Raymond-Delpech V, Gauthier M, Lenaers G: Apisα2, Apisα7-1 and Apisα7-2: Three new neuronal nicotinic acetylcholine receptor α-subunits in the honeybee brain. Gene. 2005, 344: 125-132.PubMedView ArticleGoogle Scholar
- Matsuda K, Buckingham SD, Kleier D, Rauh JJ, Grauso M, Sattelle DB: Neonicotinoids: Insecticides acting on insect nicotinic acetylcholine receptors. Trends Pharmacol Sci. 2001, 22: 573-580. 10.1016/S0165-6147(00)01820-4.PubMedView ArticleGoogle Scholar
- Siqueira CG, Bacci M, Pagnocca FC, Bueno OA, Hebling MJA: Metabolism of plant polysaccharies by Leucoagariccus gongylophorus, the symbiotic fungus of the ant Atta sexdens L. Appl Environ Microbiol. 1998, 64: 4820-4822.Google Scholar
- Silva A, Bacci M, Siqueira CG, Bueno OC, Pagnocca FC, Hebling MJA: Survival of Atta sexdens workers on different food sources. J Insect Physiol. 2003, 49: 307-313. 10.1016/S0022-1910(03)00004-0.PubMedView ArticleGoogle Scholar
- Zhou G, Somasundaram T, Blanc E, Parthasarathy G, Ellington WR, Chapman MS: Transition state struture of arginine kinase: implications for catalysis of biomolecular reactions. Proc Natl Acad Sci USA. 1998, 95: 8449-8454. 10.1073/pnas.95.15.8449.PubMedPubMed CentralView ArticleGoogle Scholar
- Brown AE, Grossman SH: The mechanism and modes of inhibition of arginine kinase from the cockroach (Periplaneta americana). Arch Insect Biochem Physiol. 2004, 57: 166-177. 10.1002/arch.20026.PubMedView ArticleGoogle Scholar
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