RNA-Seq reveals early distinctions and late convergence of gene expression between diapause and quiescence in the Asian tiger mosquito, Aedes albopictus

Journal of Experimental Biology

Volumn 216, Issue 21, 2013, Pages 4082-4090

  Poelchau, Monica F ^a   Reynolds, Julie A ^b   Elsik, Christine G ^c   Denlinger, David L ^b   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; Invasive species; Metabolism; Quiescence; RNA Seq

Indexed keywords

TRANSCRIPTOME;

AEDES; AEDES ALBOPICTUS; ANIMAL; ARTICLE; DIAPAUSE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; INVASIVE SPECIES; LARVA; LIPID METABOLISM; METABOLISM; METAMORPHOSIS; MOLECULAR GENETICS; QUIESCENCE; RNA-SEQ; SEQUENCE ANALYSIS; TIME;

AEDES ALBOPICTUS; DIAPAUSE; INVASIVE SPECIES; METABOLISM; QUIESCENCE; RNA-SEQ;

AEDES; ANIMALS; FEMALE; GENE EXPRESSION REGULATION; LARVA; LIPID METABOLISM; METAMORPHOSIS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, RNA; TIME FACTORS; TRANSCRIPTOME;

EID: 84886506050     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.089508     Document Type: Article

References (83)

1. Armbruster, P. A. and Conn, J. E. (2006). Geographic variation of larval growth in North American Aedes albopictus (Diptera: Culicidae). Ann. Entomol. Soc. Am. 99, 1234-1243.
2. Armbruster, P. A. and Hutchinson, R. A. (2002). Pupal mass and wing length as indicators of fecundity in Aedes albopictus and Aedes geniculatus (Diptera: Culicidae). J. Med. Entomol. 39, 699-704.
3. Arrese, E. L. and Soulages, J. L. (2010). Insect fat body: energy, metabolism, and regulation. Annu. Rev. Entomol. 55, 207-225.
4. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T. et al. (2000). Gene Ontology: tool for the unification of biology. Nat. Genet. 25, 25-29.
5. Bai, H., Ramaseshadri, P. and Palli, S. R. (2007). Identification and characterization of juvenile hormone esterase gene from the yellow fever mosquito, Aedes aegypti. Insect Biochem. Mol. Biol. 37, 829-837.
6. Baker, D. A. and Russell, S. (2009). Gene expression during Drosophila melanogaster egg development before and after reproductive diapause. BMC Genomics 10, 242.
7. Bao, B. and Xu, W. H. (2011). Identification of gene expression changes associated with the initiation of diapause in the brain of the cotton bollworm, Helicoverpa armigera. BMC Genomics 12, 224.
8. Benedict, M. Q., Levine, R. S., Hawley, W. A. and Lounibos, L. P. (2007). Spread of the tiger: global risk of invasion by the mosquito Aedes albopictus. Vector Borne Zoonotic Dis. 7, 76-85.
9. Brody, T. (1999). The Interactive Fly: gene networks, development and the Internet. Trends Genet. 15, 333-334.
10. Bullard, J. H., Purdom, E., Hansen, K. D. and Dudoit, S. (2010). Evaluation of statistical methods for normalization and differential expression in mRNA-Seq experiments. BMC Bioinformatics 11, 94.
11. Burmester, T. (1999). Evolution and function of the insect hexamerins. Eur. J. Entomol. 96, 213-225.
12. Chaplin, S. B. and Wells, P. H. (1982). Energy reserves and metabolic expenditures of monarch butterflies overwintering in Southern California. Ecol. Entomol. 7, 249-256.
13. Danks, H. V. (1987). Insect Dormancy: An Ecological Perspective. Ottowa, ON: Biological Survey of Canada (Terrestrial Arthropods).
14. Denlinger, D. L. (2002). Regulation of diapause. Annu. Rev. Entomol. 47, 93-122.
15. Denlinger, D. L., Wilis, J. H. and Fraenkel, G. (1972). Rates and cycles of oxygen consumption during pupal diapause in Sarcophaga flesh flies. J. Insect Physiol. 18, 871-882.
16. Denlinger, D. L., Yocum, G. D. and Rinehart, J. L. (2005). Hormonal control of diapause. In Comprehensive Molecular Insect Science (ed. L. Gilbert, K. Iatrou and S. Gill), pp. 615-650. Amsterdam: Elsevier Press.
17. Emerson, K. J., Uyemura, A. M., McDaniel, K. L., Schmidt, P. S., Bradshaw, W. E. and Holzapfel, C. M. (2009). Environmental control of ovarian dormancy in natural populations of Drosophila melanogaster. J. Comp. Physiol. A 195, 825-829.
18. Emerson, K. J., Bradshaw, W. E. and Holzapfel, C. M. (2010). Microarrays reveal early transcriptional events during the termination of larval diapause in natural populations of the mosquito, Wyeomyia smithii. PLoS ONE 5, e9574.
19. Feliú, J. E., Hue, L. and Hers, H. G. (1976). Hormonal control of pyruvate kinase activity and of gluconeogenesis in isolated hepatocytes. Proc. Natl. Acad. Sci. USA 73, 2762-2766.
20. Feng, L., Liu, H., Liu, Y., Lu, Z., Guo, G., Guo, S., Zheng, H., Gao, Y., Cheng, S., Wang, J. et al. (2010). Power of deep sequencing and agilent microarray for gene expression profiling study. Mol. Biotechnol. 45, 101-110.
21. Fraenkel, G. S. (1935). A hormone causing pupation in the blowfly Calliphora erythrocephala. Proc. R. Soc. B 118, 1-12.
22. Fu, X., Fu, N., Guo, S., Yan, Z., Xu, Y., Hu, H., Menzel, C., Chen, W., Li, Y., Zeng, R. et al. (2009). Estimating accuracy of RNA-Seq and microarrays with proteomics. BMC Genomics 10, 161.
23. Gerisch, B., Weitzel, C., Kober-Eisermann, C., Rottiers, V. and Antebi, A. (2001). A hormonal signaling pathway influencing C. elegans metabolism, reproductive development, and life span. Dev. Cell 1, 841-851.
24. Guittard, E., Blais, C., Maria, A., Parvy, J. P., Pasricha, S., Lumb, C., Lafont, R., Daborn, P. J. and Dauphin-Villemant, C. (2011). CYP18A1, a key enzyme of Drosophila steroid hormone inactivation, is essential for metamorphosis. Dev. Biol. 349, 35-45.
25. Hahn, D. A. and Denlinger, D. L. (2007). Meeting the energetic demands of insect diapause: nutrient storage and utilization. J. Insect Physiol. 53, 760-773.
26. Hahn, D. A. and Denlinger, D. L. (2011). Energetics of insect diapause. Annu. Rev. Entomol. 56, 103-121.
27. Haider, S., Ballester, B., Smedley, D., Zhang, J. J., Rice, P. and Kasprzyk, A. (2009). BioMart Central Portal - unified access to biological data. Nucleic Acids Res. 37, W23-W27.
28. Hand, S. C. and Podrabsky, J. E. (2000). Bioenergetics of diapause and quiescence in aquatic animals. Thermochim. Acta 349, 31-42.
29. Hand, S. C., Menze, M. A., Borcar, A., Patil, Y., Covi, J. A., Reynolds, J. A. and Toner, M. (2011). Metabolic restructuring during energy-limited states: insights from Artemia franciscana embryos and other animals. J. Insect Physiol. 57, 584-594.
30. Hawley, W. A. (1988). The biology of Aedes albopictus. J. Am. Mosq. Control Assoc. 1, Suppl., 1-39.
31. Hayward, S. A. L., Pavlides, S. C., Tammariello, S. P., Rinehart, J. P. and Denlinger, D. L. (2005). Temporal expression patterns of diapause-associated genes in flesh fly pupae from the onset of diapause through post-diapause quiescence. J. Insect Physiol. 51, 631-640.
32. Hodek, I. (1996). Diapause development, diapause termination and the end of diapause. Eur. J. Entomol. 93, 475-487.
33. Jia, K., Albert, P. S. and Riddle, D. L. (2002). DAF-9, a cytochrome P450 regulating C. elegans larval development and adult longevity. Development 129, 221-231.
34. Kanehisa, M. and Goto, S. (2000). KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27-30.
35. Kanehisa, M., Goto, S., Sato, Y., Furumichi, M. and Tanabe, M. (2012). KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 40, D109-D114.
36. Klowden, M. J. (2007). Physiological Systems in Insects. Burlington, MA: Academic Press.
37. Koštál, V. (2006). Eco-physiological phases of insect diapause. J. Insect Physiol. 52, 113-127.
38. Lee, K. and Denlinger, D. L. (1997). A role for ecdysteroids in the induction and maintenance of the pharate first instar diapause of the gypsy moth, Lymantria dispar. J. Insect Physiol. 43, 289-296.
39. Lee, K., Valaitis, A. P. and Denlinger, D. L. (1997). Further evidence that diapause in the gypsy moth, Lymantria dispar, is regulated by ecdysteroids: a comparison of diapause and nondiapause strains. J. Insect Physiol. 43, 897-903.
40. Li, B. and Dewey, C. N. (2011). RSEM: accurate transcript quantification from RNASeq data with or without a reference genome. BMC Bioinformatics 12, 323.
41. Llorente, P., Marco, R. and Sols, A. (1970). Regulation of liver pyruvate kinase and the phosphoenolpyruvate crossroads. Eur. J. Biochem. 13, 45-54.
42. MacRae, T. H. (2010). Gene expression, metabolic regulation and stress tolerance during diapause. Cell. Mol. Life Sci. 67, 2405-2424.
43. McElwee, J. J., Schuster, E., Blanc, E., Thornton, J. and Gems, D. (2006). Diapause-associated metabolic traits reiterated in long-lived daf-2 mutants in the nematode Caenorhabditis elegans. Mech. Ageing Dev. 127, 458-472.
44. Michaud, M. R. and Denlinger, D. L. (2007). Shifts in the carbohydrate, polyol, and amino acid pools during rapid cold-hardening and diapause-associated coldhardening in flesh flies (Sarcophaga crassipalpis): a metabolomic comparison. J. Comp. Physiol. B 177, 753-763.
45. Miller, W. L. (1988). Molecular biology of steroid hormone synthesis. Endocr. Rev. 9, 295-318.
46. Morgan, T. D. and Chippendale, G. M. (1983). Free amino acids of the hemolymph of the Southwestern corn borer and the European corn borer in relation to their diapause. J. Insect Physiol. 29, 735-740.
47. Mori, A., Oda, T. and Wada, Y. (1981). Studies on the egg diapause and overwintering of Aedes albopictus in Nagasaki. Tropical Medicine 23, 79-90.
48. Nene, V., Wortman, J. R., Lawson, D., Haas, B., Kodira, C., Tu, Z. J., Loftus, B., Xi, Z., Megy, K., Grabherr, M. et al. (2007). Genome sequence of Aedes aegypti, a major arbovirus vector. Science 316, 1718-1723.
49. Poelchau, M. F., Reynolds, J. A., Denlinger, D. L., Elsik, C. G. and Armbruster, P. A. (2011). A de novo transcriptome of the Asian tiger mosquito, Aedes albopictus, to identify candidate transcripts for diapause preparation. BMC Genomics 12, 619.
50. Poelchau, M. F., Reynolds, J. A., Elsik, C. G., Denlinger, D. L. and Armbruster, P. A. (2013a). Transcriptome sequencing as a platform to elucidate molecular components of the diapause response in the Asian tiger mosquito, Aedes albopictus. Physiol. Entomol. 38, 173-181.
51. Poelchau, M. F., Reynolds, J. A., Elsik, C. G., Denlinger, D. L. and Armbruster, P. A. (2013b). Deep sequencing reveals complex mechanisms of diapause preparation in the invasive mosquito, Aedes albopictus. Proc. Biol. Sci. 280, 20130143.
52. Pumpuni, C. B. (1989). Factors influencing photoperiodic control of egg diapause in Aedes albopictus (Skuse). PhD thesis, Department of Biological Sciences, University of Notre Dame, IN, USA.
53. Ragland, G. J., Denlinger, D. L. and Hahn, D. A. (2010). Mechanisms of suspended animation are revealed by transcript profiling of diapause in the flesh fly. Proc. Natl. Acad. Sci. USA 107, 14909-14914.
54. Ragland, G. J., Egan, S. P., Feder, J. L., Berlocher, S. H. and Hahn, D. A. (2011). Developmental trajectories of gene expression reveal candidates for diapause termination: a key life-history transition in the apple maggot fly Rhagoletis pomonella. J. Exp. Biol. 214, 3948-3959.
55. Readio, J., Chen, M. H. and Meola, R. (1999). Juvenile hormone biosynthesis in diapausing and nondiapausing Culex pipiens (Diptera: Culicidae). J. Med. Entomol. 36, 355-360.
56. Reynolds, J. A. and Hand, S. C. (2009a). Decoupling development and energy flow during embryonic diapause in the cricket, Allonemobius socius. J. Exp. Biol. 212, 2065-2074.
57. Reynolds, J. A. and Hand, S. C. (2009b). Embryonic diapause highlighted by differential expression of mRNAs for ecdysteroidogenesis, transcription and lipid sparing in the cricket Allonemobius socius. J. Exp. Biol. 212, 2075-2084.
58. Reynolds, J. A., Poelchau, M. F., Rahman, Z., Armbruster, P. A. and Denlinger, D. L. (2012). Transcript profiling reveals mechanisms for lipid conservation during diapause in the mosquito, Aedes albopictus. J. Insect Physiol. 58, 966-973.
59. Riddiford, L. M. (1994). Cellular and molecular actions of juvenile hormone. I. General considerations and premetamorphic actions. In Advances in Insect Physiology (ed. P. D. Evans), pp. 213-274. San Diego, CA: Academic Press.
60. Rinehart, J. P., Robich, R. M. and Denlinger, D. L. (2006). Enhanced cold and desiccation tolerance in diapausing adults of Culex pipiens, and a role for Hsp70 in response to cold shock but not as a component of the diapause program. J. Med. Entomol. 43, 713-722.
61. Rinehart, J. P., Li, A., Yocum, G. D., Robich, R. M., Hayward, S. A. and Denlinger, D. L. (2007). Up-regulation of heat shock proteins is essential for cold survival during insect diapause. Proc. Natl. Acad. Sci. USA 104, 11130-11137.
62. Robinson, M. D. and Oshlack, A. (2010). A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 11, R25.
63. Robinson, M. D., McCarthy, D. J. and Smyth, G. K. (2010). edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140.
64. Schmidt, P. S., Matzkin, L., Ippolito, M. and Eanes, W. F. (2005). Geographic variation in diapause incidence, life-history traits, and climatic adaptation in Drosophila melanogaster. Evolution 59, 1721-1732.
65. Schulz, M. H., Zerbino, D. R., Vingron, M. and Birney, E. (2012). Oases: robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics 28, 1086-1092.
66. Sim, C. and Denlinger, D. L. (2009). Transcription profiling and regulation of fat metabolism genes in diapausing adults of the mosquito Culex pipiens. Physiol. Genomics 39, 202-209.
67. Smyth, G. K. (2004). Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, e3.
68. Smyth, G. K. (2005). Limma: linear models for microarray data. In Bioinformatics and Computational Biology Solutions Using R and Bioconductor (ed. R. Gentleman, V. Carey, S. Dudoit, R. Irizarry and W. Huber), pp. 397-420. New York, NY: Springer.
69. Spielman, A. (1974). Effect of synthetic juvenile hormone on ovarian diapause of Culex pipiens mosquitoes. J. Med. Entomol. 11, 223-225.
70. Tauber, M. J. and Tauber, C. A. (1976). Insect seasonality: diapause maintenance, termination, and postdiapause development. Annu. Rev. Entomol. 21, 81-107.
71. Tauber, M. J., Tauber, C. A. and Masaki, S. (1986). Seasonal Adaptations of Insects. New York, NY: Oxford University Press.
72. Trpis, M. (1970). A new bleaching and decalcifying method for general use in zoology. Can. J. Zool. 48, 892-893.
73. Truman, J. W., Hiruma, K., Allee, J. P., Macwhinnie, S. G., Champlin, D. T. and Riddiford, L. M. (2006). Juvenile hormone is required to couple imaginal disc formation with nutrition in insects. Science 312, 1385-1388.
74. Urbanski, J. M., Benoit, J. B., Michaud, M. R., Denlinger, D. L. and Armbruster, P. A. (2010). The molecular physiology of increased egg desiccation resistance during diapause in the invasive mosquito, Aedes albopictus. Proc. Biol. Sci. 277, 2683-2692.
75. Urbanski, J. M., Mogi, M., O'Donnell, D. L., DeCotiis, M., Toma, T. and Armbruster, P. A. (2012). Rapid adaptive evolution of photoperiodic response during invasion and range expansion across a climatic gradient. Am. Nat. 179, 490-500.
76. Van Handel, E. (1993). Fuel metabolism of the mosquito Culex quinquefasciatus embryo. J. Insect Physiol. 39, 831-833.
77. Wang, R. L. (1966). Observations on the influence of photoperiod on egg diapause in Aedes albopictus Skuse. Acta Entomologica Sinica 15, 75-77.
78. Wigglesworth, V. B. (1934). The physiology of ecdysis in Rhodnius prolixus. II. Factors controlling moulting and metamorphosis. Q. J. Microsc. Sci. 77, 191-222.
79. Williams, K. D., Schmidt, P. S. and Sokolowski, M. B. (2010). Photoperiodism in insects: molecular basis and consequences of diapause. In Photoperiodism: The Biological Calendar (ed. R. J. Nelson, D. L. Denlinger and D. E. Somers), pp. 287-317. New York, NY: Oxford University Press.
80. Wu, Q. and Brown, M. R. (2006). Signaling and function of insulin-like peptides in insects. Annu. Rev. Entomol. 51, 1-24.
81. Young, M. D., Wakefield, M. J., Smyth, G. K. and Oshlack, A. (2010). Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol. 11, R14.
82. Zerbino, D. R. and Birney, E. (2008). Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18, 821-829.
83. Zhou, G. and Miesfeld, R. L. (2009). Energy metabolism during diapause in Culex pipiens mosquitoes. J. Insect Physiol. 55, 40-46.