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2. Exploring integument transcriptomes, cuticle ultrastructure, and cuticular hydrocarbons profiles in eusocial and solitary bee species displaying heterochronic adult cuticle maturation

Author

Falcon, Tiago, primary, Pinheiro, Daniel G., additional, Ferreira-Caliman, Maria Juliana, additional, Turatti, Izabel C. C., additional, Abreu, Fabiano C. Pinto de, additional, Galaschi-Teixeira, Juliana S., additional, Martins, Juliana R., additional, Elias-Neto, Moysés, additional, Soares, Michelle P. M., additional, Laure, Marcela B., additional, Figueiredo, Vera L. C., additional, Lopes, Norberto Peporine, additional, Simões, Zilá L. P., additional, Garófalo, Carlos A., additional, and Bitondi, Márcia M. G., additional

Published
2019
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3. Exploring integument transcriptomes, cuticle ultrastructure, and cuticular hydrocarbons profiles in eusocial and solitary bee species displaying heterochronic adult cuticle maturation

Author

Falcon, Tiago, primary, Pinheiro, Daniel G., additional, Ferreira-Caliman, Maria Juliana, additional, Turatti, Izabel C. C., additional, Pinto de Abreu, Fabiano C., additional, Galaschi-Teixeira, Juliana S., additional, Martins, Juliana R., additional, Elias-Neto, Moysés, additional, Soares, Michelle P. M., additional, Laure, Marcela B., additional, Figueiredo, Vera L. C., additional, Lopes, Norberto Peporine, additional, Simões, Zilá L. P., additional, Garófalo, Carlos A., additional, and Bitondi, Márcia M. G., additional

Published
2018
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4. The genomes of two key bumblebee species with primitive eusocial organization

Author

Sadd, Ben M., Barribeau, Seth M., Bloch, Guy, de Graaf, Dirk C., Dearden, Peter, Elsik, Christine G., Gadau, Jürgen, Grimmelikhuijzen, Cornelis J. P., Hasselmann, Martin, Lozier, Jeffrey D., Robertson, Hugh M., Smagghe, Guy, Stolle, Eckart, Van Vaerenbergh, Matthias, Waterhouse, Robert M., Bornberg-Bauer, Erich, Klasberg, Steffen, Bennett, Anna K., Câmara, Francisco, Guigó, Roderic, Hoff, Katharina, Mariotti, Marco, Munoz-Torres, Monica, Murphy, Terence, Santesmasses, Didac, Amdam, Gro V., Beckers, Matthew, Beye, Martin, Biewer, Matthias, Bitondi, Márcia M. G., Blaxter, Mark L., Bourke, Andrew F. G., Brown, Mark J. F., Buechel, Severine D., Cameron, Rossanah, Cappelle, Kaat, Carolan, James C., Christiaens, Olivier, Ciborowski, Kate L., Clarke, David F., Colgan, Thomas J., Collins, David H., Cridge, Andrew G., Dalmay, Tamas, Dreier, Stephanie, du Plessis, Louis, Duncan, Elizabeth, Erler, Silvio, Evans, Jay, Falcon, Tiago, Flores, Kevin, Freitas, Flávia C. P., Fuchikawa, Taro, Gempe, Tanja, Hartfelder, Klaus, Hauser, Frank, Helbing, Sophie, Humann, Fernanda C., Irvine, Frano, Jermiin, Lars S., Johnson, Claire E., Johnson, Reed M., Jones, Andrew K., Kadowaki, Tatsuhiko, Kidner, Jonathan H., Koch, Vasco, Köhler, Arian, Kraus, F. Bernhard, Lattorff, H. Michael G., Leask, Megan, Lockett, Gabrielle A., Mallon, Eamonn B., Antonio, David S. Marco, Marxer, Monika, Meeus, Ivan, Moritz, Robin F. A., Nair, Ajay, Näpflin, Kathrin, Nissen, Inga, Niu, Jinzhi, Nunes, Francis M. F., Oakeshott, John G., Osborne, Amy, Otte, Marianne, Pinheiro, Daniel G., Rossié, Nina, Rueppell, Olav, Santos, Carolina G., Schmid-Hempel, Regula, Schmitt, Björn D., Schulte, Christina, Simões, Zilá L. P., Soares, Michelle P. M., Swevers, Luc, Winnebeck, Eva C., Wolschin, Florian, Yu, Na, Zdobnov, Evgeny M., Aqrawi, Peshtewani K., Blankenburg, Kerstin P., Coyle, Marcus, Francisco, Liezl, Hernandez, Alvaro G., Holder, Michael, Hudson, Matthew E., Jackson, LaRonda, Jayaseelan, Joy, Joshi, Vandita, Kovar, Christie, Lee, Sandra L., Mata, Robert, Mathew, Tittu, Newsham, Irene F., Ngo, Robin, Okwuonu, Geoffrey, Pham, Christopher, Pu, Ling-Ling, Saada, Nehad, Santibanez, Jireh, Simmons, DeNard, Thornton, Rebecca, Venkat, Aarti, Walden, Kimberly Ko, Wu, Yuan-Qing, Debyser, Griet, Devreese, Bart, Asher, Claire, Blommaert, Julie, Chipman, Ariel D., Chittka, Lars, Fouks, Bertrand, Liu, Jisheng, O'Neill, Meaghan P., Sumner, Seirian, Puiu, Daniela, Qu, Jiaxin, Salzberg, Steven L., Scherer, Steven E., Muzny, Donna M., Richards, Stephen, Robinson, Gene E., Gibbs, Richard A., Schmid-Hempel, Paul, Worley, Kim C., Sadd, Ben M., Barribeau, Seth M., Bloch, Guy, de Graaf, Dirk C., Dearden, Peter, Elsik, Christine G., Gadau, Jürgen, Grimmelikhuijzen, Cornelis J. P., Hasselmann, Martin, Lozier, Jeffrey D., Robertson, Hugh M., Smagghe, Guy, Stolle, Eckart, Van Vaerenbergh, Matthias, Waterhouse, Robert M., Bornberg-Bauer, Erich, Klasberg, Steffen, Bennett, Anna K., Câmara, Francisco, Guigó, Roderic, Hoff, Katharina, Mariotti, Marco, Munoz-Torres, Monica, Murphy, Terence, Santesmasses, Didac, Amdam, Gro V., Beckers, Matthew, Beye, Martin, Biewer, Matthias, Bitondi, Márcia M. G., Blaxter, Mark L., Bourke, Andrew F. G., Brown, Mark J. F., Buechel, Severine D., Cameron, Rossanah, Cappelle, Kaat, Carolan, James C., Christiaens, Olivier, Ciborowski, Kate L., Clarke, David F., Colgan, Thomas J., Collins, David H., Cridge, Andrew G., Dalmay, Tamas, Dreier, Stephanie, du Plessis, Louis, Duncan, Elizabeth, Erler, Silvio, Evans, Jay, Falcon, Tiago, Flores, Kevin, Freitas, Flávia C. P., Fuchikawa, Taro, Gempe, Tanja, Hartfelder, Klaus, Hauser, Frank, Helbing, Sophie, Humann, Fernanda C., Irvine, Frano, Jermiin, Lars S., Johnson, Claire E., Johnson, Reed M., Jones, Andrew K., Kadowaki, Tatsuhiko, Kidner, Jonathan H., Koch, Vasco, Köhler, Arian, Kraus, F. Bernhard, Lattorff, H. Michael G., Leask, Megan, Lockett, Gabrielle A., Mallon, Eamonn B., Antonio, David S. Marco, Marxer, Monika, Meeus, Ivan, Moritz, Robin F. A., Nair, Ajay, Näpflin, Kathrin, Nissen, Inga, Niu, Jinzhi, Nunes, Francis M. F., Oakeshott, John G., Osborne, Amy, Otte, Marianne, Pinheiro, Daniel G., Rossié, Nina, Rueppell, Olav, Santos, Carolina G., Schmid-Hempel, Regula, Schmitt, Björn D., Schulte, Christina, Simões, Zilá L. P., Soares, Michelle P. M., Swevers, Luc, Winnebeck, Eva C., Wolschin, Florian, Yu, Na, Zdobnov, Evgeny M., Aqrawi, Peshtewani K., Blankenburg, Kerstin P., Coyle, Marcus, Francisco, Liezl, Hernandez, Alvaro G., Holder, Michael, Hudson, Matthew E., Jackson, LaRonda, Jayaseelan, Joy, Joshi, Vandita, Kovar, Christie, Lee, Sandra L., Mata, Robert, Mathew, Tittu, Newsham, Irene F., Ngo, Robin, Okwuonu, Geoffrey, Pham, Christopher, Pu, Ling-Ling, Saada, Nehad, Santibanez, Jireh, Simmons, DeNard, Thornton, Rebecca, Venkat, Aarti, Walden, Kimberly Ko, Wu, Yuan-Qing, Debyser, Griet, Devreese, Bart, Asher, Claire, Blommaert, Julie, Chipman, Ariel D., Chittka, Lars, Fouks, Bertrand, Liu, Jisheng, O'Neill, Meaghan P., Sumner, Seirian, Puiu, Daniela, Qu, Jiaxin, Salzberg, Steven L., Scherer, Steven E., Muzny, Donna M., Richards, Stephen, Robinson, Gene E., Gibbs, Richard A., Schmid-Hempel, Paul, and Worley, Kim C.

Abstract

BACKGROUND: The shift from solitary to social behavior is one of the major evolutionary transitions. Primitively eusocial bumblebees are uniquely placed to illuminate the evolution of highly eusocial insect societies. Bumblebees are also invaluable natural and agricultural pollinators, and there is widespread concern over recent population declines in some species. High-quality genomic data will inform key aspects of bumblebee biology, including susceptibility to implicated population viability threats. RESULTS: We report the high quality draft genome sequences of Bombus terrestris and Bombus impatiens, two ecologically dominant bumblebees and widely utilized study species. Comparing these new genomes to those of the highly eusocial honeybee Apis mellifera and other Hymenoptera, we identify deeply conserved similarities, as well as novelties key to the biology of these organisms. Some honeybee genome features thought to underpin advanced eusociality are also present in bumblebees, indicating an earlier evolution in the bee lineage. Xenobiotic detoxification and immune genes are similarly depauperate in bumblebees and honeybees, and multiple categories of genes linked to social organization, including development and behavior, show high conservation. Key differences identified include a bias in bumblebee chemoreception towards gustation from olfaction, and striking differences in microRNAs, potentially responsible for gene regulation underlying social and other traits. CONCLUSIONS: These two bumblebee genomes provide a foundation for post-genomic research on these key pollinators and insect societies. Overall, gene repertoires suggest that the route to advanced eusociality in bees was mediated by many small changes in many genes and processes, and not by notable expansion or depauperation.

Published
2015
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6. The genomes of two key bumblebee species with primitive eusocial organization.

Author

Sadd BM, Barribeau SM, Bloch G, de Graaf DC, Dearden P, Elsik CG, Gadau J, Grimmelikhuijzen CJ, Hasselmann M, Lozier JD, Robertson HM, Smagghe G, Stolle E, Van Vaerenbergh M, Waterhouse RM, Bornberg-Bauer E, Klasberg S, Bennett AK, Câmara F, Guigó R, Hoff K, Mariotti M, Munoz-Torres M, Murphy T, Santesmasses D, Amdam GV, Beckers M, Beye M, Biewer M, Bitondi MM, Blaxter ML, Bourke AF, Brown MJ, Buechel SD, Cameron R, Cappelle K, Carolan JC, Christiaens O, Ciborowski KL, Clarke DF, Colgan TJ, Collins DH, Cridge AG, Dalmay T, Dreier S, du Plessis L, Duncan E, Erler S, Evans J, Falcon T, Flores K, Freitas FC, Fuchikawa T, Gempe T, Hartfelder K, Hauser F, Helbing S, Humann FC, Irvine F, Jermiin LS, Johnson CE, Johnson RM, Jones AK, Kadowaki T, Kidner JH, Koch V, Köhler A, Kraus FB, Lattorff HM, Leask M, Lockett GA, Mallon EB, Antonio DS, Marxer M, Meeus I, Moritz RF, Nair A, Näpflin K, Nissen I, Niu J, Nunes FM, Oakeshott JG, Osborne A, Otte M, Pinheiro DG, Rossié N, Rueppell O, Santos CG, Schmid-Hempel R, Schmitt BD, Schulte C, Simões ZL, Soares MP, Swevers L, Winnebeck EC, Wolschin F, Yu N, Zdobnov EM, Aqrawi PK, Blankenburg KP, Coyle M, Francisco L, Hernandez AG, Holder M, Hudson ME, Jackson L, Jayaseelan J, Joshi V, Kovar C, Lee SL, Mata R, Mathew T, Newsham IF, Ngo R, Okwuonu G, Pham C, Pu LL, Saada N, Santibanez J, Simmons D, Thornton R, Venkat A, Walden KK, Wu YQ, Debyser G, Devreese B, Asher C, Blommaert J, Chipman AD, Chittka L, Fouks B, Liu J, O'Neill MP, Sumner S, Puiu D, Qu J, Salzberg SL, Scherer SE, Muzny DM, Richards S, Robinson GE, Gibbs RA, Schmid-Hempel P, and Worley KC

Subjects
Animals, Bee Venoms genetics, Bees classification, Bees physiology, Chemoreceptor Cells metabolism, Chromosome Mapping, Databases, Genetic, Evolution, Molecular, Female, Gene Expression Regulation, Gene Rearrangement, Genomics, Interspersed Repetitive Sequences, Male, Open Reading Frames, Polymorphism, Single Nucleotide, Selenoproteins genetics, Selenoproteins metabolism, Sequence Analysis, DNA, Species Specificity, Synteny, Bees genetics, Behavior, Animal, Genes, Insect, Social Behavior
Abstract

Background: The shift from solitary to social behavior is one of the major evolutionary transitions. Primitively eusocial bumblebees are uniquely placed to illuminate the evolution of highly eusocial insect societies. Bumblebees are also invaluable natural and agricultural pollinators, and there is widespread concern over recent population declines in some species. High-quality genomic data will inform key aspects of bumblebee biology, including susceptibility to implicated population viability threats., Results: We report the high quality draft genome sequences of Bombus terrestris and Bombus impatiens, two ecologically dominant bumblebees and widely utilized study species. Comparing these new genomes to those of the highly eusocial honeybee Apis mellifera and other Hymenoptera, we identify deeply conserved similarities, as well as novelties key to the biology of these organisms. Some honeybee genome features thought to underpin advanced eusociality are also present in bumblebees, indicating an earlier evolution in the bee lineage. Xenobiotic detoxification and immune genes are similarly depauperate in bumblebees and honeybees, and multiple categories of genes linked to social organization, including development and behavior, show high conservation. Key differences identified include a bias in bumblebee chemoreception towards gustation from olfaction, and striking differences in microRNAs, potentially responsible for gene regulation underlying social and other traits., Conclusions: These two bumblebee genomes provide a foundation for post-genomic research on these key pollinators and insect societies. Overall, gene repertoires suggest that the route to advanced eusociality in bees was mediated by many small changes in many genes and processes, and not by notable expansion or depauperation.

Published
2015
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7. Developmental characterization, function and regulation of a Laccase2 encoding gene in the honey bee, Apis mellifera (Hymenoptera, Apinae).

Author

Elias-Neto M, Soares MP, Simões ZL, Hartfelder K, and Bitondi MM

Subjects
Amino Acid Sequence, Animals, Bees genetics, Down-Regulation, Gene Knockdown Techniques, Insect Proteins genetics, Laccase genetics, Ligation, Molecular Sequence Data, RNA Interference, Bees enzymology, Ecdysteroids metabolism, Gene Expression Regulation, Developmental, Insect Proteins metabolism, Laccase metabolism
Abstract

In insects, exoskeleton (cuticle) formation at each molt cycle includes complex biochemical pathways wherein the laccase enzymes (EC 1.10.3.2) may have a key role. We identified an Amlac2 gene that encodes a laccase2 in the honey bee, Apis mellifera, and investigated its function in exoskeleton differentiation. The Amlac2 gene consists of nine exons resulting in an ORF of 2193 nucleotides. The deduced translation product is a 731 amino acid protein of 81.5 kDa and a pI of 6.05. Amlac2 is highly expressed in the integument of pharate adults, and the expression precedes the onset of cuticle pigmentation and the intensification of sclerotization. In accordance with the temporal sequence of exoskeleton differentiation from anterior to posterior direction, the levels of Amlac2 transcript increase earlier in the thoracic than in the abdominal integument. The gene expression lasts even after the bees emerge from brood cells and begin activities in the nest, but declines after the transition to foraging stage, suggesting that maturation of the exoskeleton is completed at this stage. Post-transcriptional knockdown of Amlac2 gene expression resulted in structural abnormalities in the exoskeleton and drastically affected adult eclosion. By setting a ligature between the thorax and abdomen of early pupae we could delay the increase in hemolymph ecdysteroid levels in the abdomen. This severely impaired the increase in Amlac2 transcript levels and also the differentiation of the abdominal exoskeleton. Taken together, these results indicate that Amlac2 expression is controlled by ecdysteroids and has a critical role in the differentiation of the adult exoskeleton of honey bees., ((c) 2010 Elsevier Ltd. All rights reserved.)

Published
2010
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8. A cuticle protein gene in the honeybee: expression during development and in relation to the ecdysteroid titer.

Author

Soares MP, Elias-Neto M, Simões ZL, and Bitondi MM

Subjects
Abdomen physiology, Amino Acid Sequence, Animals, Bees genetics, Bees growth & development, Down-Regulation, Insect Proteins chemistry, Insect Proteins genetics, Molecular Sequence Data, Sequence Alignment, Sequence Analysis, DNA, Thorax metabolism, Bees metabolism, Ecdysteroids metabolism, Gene Expression Regulation, Developmental, Insect Proteins metabolism
Abstract

A cDNA encoding a cuticle protein containing the R&R Consensus was characterized in the honeybee integument. AmelCPR14 developmental expression is distinguished by an on-off-on pattern, the transition from a low to a high level of transcripts occurring as the ecdysteroid titer is declining after the peak that triggers the onset of pharate (pupal and adult) development. The transcript is abundant during cuticle tanning and sclerotization, and persists even in the adult integument, suggesting that the corresponding protein is required for differentiation and maintenance of the adult cuticle. Such developmental pattern suggested that AmelCPR14 gene might be regulated by the titer of ecdysteroids. We confirmed this hypothesis using different experimental strategies. By tying a ligature in early pupae to prevent exposure of abdominal integument to a high ecdysteroid titer, we delayed the accumulation of AmelCPR14 transcripts in the abdominal integument. This is consistent with ecdysteroid priming being required in pupae for the increase in AmelCPR14 expression in pharate adults. By injecting 20-hydroxyecdysone (20E) in early pupae we demonstrated that hormone titer decay after the peak is critical for AmelCPR14 expression induction. Exposure of pupal integument in vitro to a 20E concentration mimicking the pupal ecdysteroid peak repressed AmelCPR14 expression, which was recovered by hormone removal. Taken together, these data are consistent with an ecdysteroid pulse (increase in hormone titer followed by its decline) being critical for a high AmelCPR14 gene expression in pharate adults.

Published
2007
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