Transcriptome sequencing as a platform to elucidate molecular components of the diapause response in the Asian tiger mosquito Aedes albopictus

Physiological Entomology

Volumn 38, Issue 2, 2013, Pages 173-181

  Poelchau, Monica F ^a   Reynolds, Julie A ^b   Denlinger, David L ^b   Elsik, Christine G ^c   Armbruster, Peter A ^a  

^a GEORGETOWN UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c UNIVERSITY OF MISSOURI   (United States)

Author keywords

Aedes albopictus; Diapause; Next generation sequencing; Transcriptome

Indexed keywords

ADAPTATION; DIAPAUSE; ENTOMOLOGY; EVOLUTIONARY BIOLOGY; GENE EXPRESSION; GENOME; INVASIVE SPECIES; LIFE HISTORY; MOSQUITO; PHYSIOLOGY; RANGE EXPANSION;

AEDES ALBOPICTUS;

EID: 84878208957     PISSN: 03076962     EISSN: 13653032     Source Type: Journal    
DOI: 10.1111/phen.12016     Document Type: Article

References (53)

1. Andrewartha, H.G. (1952) Diapause in relation to the ecology of insects. Biological Reviews, 27, 50-107.
2. Armbruster, P.A. & Conn, J.E. (2006) Geographic variation of larval growth in North American Aedes albopictus (Diptera: Culicidae). Annals of the Entomological Society of America, 99, 1234-1243.
3. Armbruster, P.A. & Hutchinson, R.A. (2002) Pupal mass and wing length as indicators of fecundity in Aedes albopictus and Aedes geniculatus (Diptera: Culicidae). Journal of Medical Entomology, 39, 699-704.
4. Ashburner, M., Ball, C.A., Blake, J.A. et al. (2000) Gene ontology: tool for the unification of biology. Nature Genetics, 25, 25-29.
5. Bean, D.W., Dalin, P. & Dudley, T.L. (2012) Evolution of critical day length for diapause induction enables range expansion of Diorhabda carinulata, a biological control agent against tamarisk (Tamarix spp.). Evolutionary Applications, 5, 511-523.
6. Benoit, J.B. (2010) Water management by dormant insects: comparisons between dehydration resistance during summer aestivation and winter diapause. Aesivation: Molecular and Physiological Aspects (eds. by C.A. Navas and J.E. Caralho ), pp. 209-229. Springer-Verlag, Germany.
7. Bradshaw, W.E. & Holzapfel, C.M. (2001) Genetic shift in photoperiodic response correlated with global warming. Proceedings of the National Academy of Sciences of the United States of America, 98, 14509-14511.
8. Brown, C.T., Howe, A., Zhang, Q. et al. (2012) A Reference-Free Algorithm for Computational Normalization of Shotgun Sequencing Data. arXiv:1203.4802.
9. Cox, M.P., Peterson, D.A. & Biggs, P.J. (2010) SolexaQA: at-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinformatics, 11, 485.
10. Danks, H.V. (1987) Insect Dormancy: An Ecological Perspective. Biological Survey of Canada (Terrestrial Arthropods), Canada.
11. Davey, J.W., Hohenlohe, P.A., Etter, P.D. et al. (2011) Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nature Reviews Genetics, 12, 499-510.
12. Denlinger, D.L., Yocum, G.D. & Rinehart, J.L. (2005) Hormonal control of diapause. Comprehensive Insect Molecular Science (eds. by L. Gilbert, K. Iatrou and S. Gill ), pp. 615-650. Elsevier Press, The Netherlands.
13. Hahn, D.A. & Denlinger, D.L. (2011) Energetics of insect diapause. Annual Review of Entomology, 56, 103-121.
14. Haider, S., Ballester, B., Smedley, D. et al. (2009) BioMart Central Portal-unified access to biological data. Nucleic Acids Research, 37, W23-W27.
15. Hawley, W.A., Reiter, P., Copeland, R.S. et al. (1987) Aedes albopictus in North America: probable introduction in used tires from northern Asia. Science, 236, 1114-1116.
16. Huang, X. & Madan, A. (1999) CAP3: a DNA sequence assembly program. Genome Research, 9, 868-877.
17. Kostal, V. (2006) Eco-physiological phases of insect diapause. Journal of Insect Physiology, 52, 113-127.
18. Kukal, O., Denlinger, D.L. & Lee, R.E. (1991) Developmental and metabolic changes induced by anoxia in diapausing and nondiapausing flesh fly pupae. Journal of Comparative Physiology B: Biochemical Systemic and Environmental Physiology, 160, 683-689.
19. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S.L. (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology, 10, R25.
20. Li, W.Z. & Godzik, A. (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics, 22, 1658-1659.
21. Martin, J.A. & Wang, Z. (2011) Next-generation transcriptome assembly. Nature Reviews Genetics, 12, 671-682.
22. Michaud, M.R. & Denlinger, D.L. (2007) Shifts in the carbohydrate, polyol, and amino acid pools during rapid cold-hardening and diapause-associated cold-hardening in flesh flies (Sarcophaga crassipalpis): a metabolomic comparison. Journal of Comparative Physiology B: Biochemical Systemic and Environmental Physiology, 177, 753-763.
23. Mori, A., Oda, T. & Wada, Y. (1981) Studies on the egg diapause and overwintering of Aedes albopictus in Nagasaki. Tropical Medicine, 23, 79-90.
24. Nene, V., Wortman, J.R., Lawson, D. et al. (2007) Genome sequence of Aedes aegypti, a major arbovirus vector. Science, 316, 1718-1723.
25. Ning, Z.M., Cox, A.J. & Mullikin, J.C. (2001) SSAHA: a fast search method for large DNA databases. Genome Research, 11, 1725-1729.
26. Pearson, R.G., Raxworthy, C.J., Nakamura, M. & Peterson, A.T. (2007) Predicting species distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar. Journal of Biogeography, 34, 102-117.
27. Poelchau, M.F., Reynolds, J.A., Denlinger, D.L. et al. (2011) A de novo transcriptome of the Asian tiger mosquito, Aedes albopictus, to identify candidate transcripts for diapause preparation. BMC Genomics, 12, 619.
28. Poelchau, M.F., Reynolds, J.A., Denlinger, D.L. et al. (2013) Deep sequencing reveals complex mechanisms of diapause preparation in the invasive mosquito, Aedes albopictus. Proceedings of the Royal Society of London Series B: Biological Sciences, 280, 21030143.
29. Ragland, G.J., Denlinger, D.L. & Hahn, D.A. (2010) Mechanisms of suspended animation are revealed by transcript profiling of diapause in the flesh fly. Proceedings of the National Academy of Sciences of the United States of America, 107, 14909-14914.
30. Ragland, G.J., Egan, S.P., Feder, J.L. et al. (2011) Developmental trajectories of gene expression reveal cadidates for diapause termination: a key life-history transition in the apple maggot fly Rhagoletis pomonella. Journal of Experimental Biology, 214, 3948-3959.
31. Reynolds, J.A. & Hand, S.C. (2009) Embryonic diapause highlighted by differential expression of mRNAs for ecdysteroidogenesis, transcription and lipid sparing in the cricket Allonemobius socius. Journal of Experimental Biology, 212, 2074-2083.
32. Reynolds, J.A., Poelchau, M.F., Rahman, Z. et al. (2012) Transcript profiling reveals mechanisms for lipid conservation during diapause in the mosquito, Aedes albopictus. Journal of Insect Physiology, 58, 966-973.
33. Rinehart, J.P., Li, A., Yocum, G.D. et al. (2007) Up-regulation of heat shock proteins is essential for cold survival during insect diapause. Proceedings of the National Academy of Sciences of the United States of America, 104, 11130-11137.
34. Robich, R.M. & Denlinger, D.L. (2005) Diapause in the mosquito Culex pipiens evokes a metabolic switch from blood feeding to sugar gluttony. Proceedings of the National Academy of Sciences of the United States of America, 102, 15912-15917.
35. Schulz, M.H., Zerbino, D.R., Vingron, M. & Birney, E. (2012) Oases: robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics, 28, 1086-1092.
36. Sim, C. & Denlinger, D.L. (2008) Insulin signaling and FOXO regulate the overwintering diapause of the mosquito Culex pipiens. Proceedings of the National Academy of Sciences of the United States of America, 105, 6777-6781.
37. Sim, C. & Denlinger, D.L. (2009a) A shut-down in expression of an insulin-like peptide, ILP-1, halts ovarian maturation during the overwintering diapause of the mosquito Culex pipiens. Insect Molecular Biology, 18, 325-332.
38. Sim, C. & Denlinger, D.L. (2009b) Transcription profiling and regulation of fat metabolism genes in diapausing adults of the mosquito Culex pipiens. Physiological Genomics, 39, 202-209.
39. Slater, G. & Birney, E. (2005) Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics, 6, 31.
40. Sota, T. & Mogi, M. (1992) Survival time and resistance to desication of diapause and non-diapause eggs of temperate Aedes (Stegomyia) mosquitoes. Entomologia Experimentalis et Applicata, 63, 155-161.
41. Surget-Groba, Y. & Montoya-Burgos, J. (2010) Optimization of de novo transcriptome assembly from next-generation sequencing data. Genome Research, 20, 1432-1440.
42. Tammariello, S.P. (2001) Regulation of the cell cycle during diapause. Insect timing: circadian rhythmicity to seasonality (eds. by D.L. Denlinger, J. Giebultowicz and D.S. Saunders ), pp. 173-183. Elsevier Science, B.V., The Netherlands.
43. Tammariello, S.P. & Denlinger, D.L. (1998) G0/G1 cell cycle arrest in the brain of Sarcophaga crassipalpis during pupal diapause and the expression pattern of the cell cycle regulator, proliferating cell nuclear antigen. Insect Biochemistry and Molecular Biology, 28, 83-89.
44. Tatar, M., Kopelman, A., Epstein, D. et al. (2001) A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science, 292, 107-110.
45. Tauber, M.J., Tauber, C.A. & Masaki, S. (1986) Seasonal Adaptations of Insects. Oxford University Press, New York, New York.
46. Trpis, M. (1970) A new bleaching and decalcifying method for general use in zoology. Canadian Journal of Zoology, 48, 892-893.
47. Urbanski, J.M., Benoit, J.B., Michaud, M.R. et al. (2010) The molecular basis of increased desiccation resistance during diapause in the Asian tiger mosquito, Aedes albopictus. Proceedings of the Royal Society of London Series B: Biological Sciences, 277, 2683-2692.
48. Urbanski, J., Mogi, M., O'Donnell, D. et al. (2012) Rapid adaptive evolution of photoperiodic response during invasion and range expansion across a climatic gradient. American Naturalist, 179, 490-500.
49. Wang, R.L. (1966) Observations on the influence of photoperiod on egg diapause in Aedes albopictus Skuse. Acta Entomologica Sinica, 15, 75-77.
50. Waterhouse, R.M., Zdobnov, E.M., Tegenfeldt, F. et al. (2011) OrthoDB: the hierarchical catalog of eukaryotic orthologs in 2011. Nucleic Acids Research, 39, D283-D288.
51. Williams, K.D., Busto, M., Suster, M.L. et al. (2006) Natural variation in Drosophila melanogaster diapause due to the insulin-regulated PI3-kinase. Proceedings of the National Academy of Sciences of the United States of America, 103, 15911-15915.
52. Wong, K., Jin, Y. & Moqtaderi, Z. (2013) Multiplex Illumina sequencing using DNA barcoding. Current Protocols in Molecular Biology, 7.11.1-7.11.11.
53. Zerbino, D.R. & Birney, E. (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Research, 18, 821-829.