Key molecular processes of the diapause to post-diapause quiescence transition in the alfalfa leafcutting bee Megachile rotundata identified by comparative transcriptome analysis

Physiological Entomology

Volumn 40, Issue 2, 2015, Pages 103-112

  Yocum, George D ^a   Rinehart, Joseph P ^a   Horvath, David P ^a   Kemp, William P ^a   Bosch, Jordi ^b   Alroobi, Rami ^c   Salem, Saeed ^c  

^a USDA ARS Red River Valley Agricultural Research Center   (United States)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^c North Dakota State University   (United States)

Author keywords

Development; Diapause; Gene expression; KEGG pathways; Pollinator

Indexed keywords

ALFALFA; BEE; DIAPAUSE; GENE EXPRESSION; GROWTH RESPONSE; LIFE CYCLE; MOLECULAR ANALYSIS; REPRODUCTIVE BEHAVIOR; SEASONAL VARIATION;

HEXAPODA; MEGACHILE ROTUNDATA;

EID: 84929511587     PISSN: 03076962     EISSN: 13653032     Source Type: Journal    
DOI: 10.1111/phen.12093     Document Type: Article

References (79)

1. Amero, S.A., Elgin, S.C.R. & Beyer, A.L. (1991) A unique zinc finger protein is associated preferentially with active ecdysone-responsive loci in Drosophila. Genes and Development, 5, 188-200.
2. Aronova, S., Wedaman, K., Aronov, P.A. etal. (2008) Regulation of ceramide biosynthesis by TOR complex 2. Cell Metabolism, 7, 148-158.
3. Ashburner, M. (1972) Patterns of puffing activity in the salivary gland chromosomes in Drosophila. Chromosoma, 38, 255-281.
4. Ashburner, M. (1974) Sequential gene activation by ecdysone in polytene chromosomes of Drosophila melanogaster. Developmental Biology, 39, 141-157.
5. Bartel, D.P. (2009) MicroRNAs: target recognition and regulatory functions. Cell, 136, 215-233.
6. Buday, L. & Downward, J. (2008) Many faces of Ras activation. Biochimica et Biophysica Acta, 1786, 178-187.
7. Burtis, K.C., Thummel, C.S., Jones, C.W. etal. (1990) The Drosophila 74EF early puff contains E74, a complex ecdysone-inducible gene that encodes two ets-related proteins. Cell, 61, 85-99.
8. Conesa, A., Götz, S., García-Gómez, J.M. etal. (2005) Blast2go: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 21, 3674-3676.
9. Danks, H.V. (1987) Insect Dormancy: An Ecological Perspective. Biological Survey of Canada, Canada.
10. Denlinger, D.L., Yocum, G.D. & Rinehart, J.P. (2005) Hormonal control of diapause. Comprehensive Molecular Insect Science (ed. by L. Gilbert, K. Iatrou and S. Gill), pp. 615-650. Elsevier Press, The Netherlands.
11. Denlinger, D.L., Yocum, G.D. & Rinehart, J.P. (2011) Hormonal control of diapause. Insect Endocrinology (ed. by L. Gilbert), pp. 430-463. Academic Press, The Netherlands.
12. Dongen, S.V. (2008) Graph clustering via a discrete uncoupling process. SIAM Journal on Matrix Analysis and Applications, 30, 121-141.
13. Flannagan, R.D., Tammariello, S.P., Joplin, K.H. etal. (1998) Diapause-specific gene expression in pupae of the flesh fly, Sarcophaga crassipalpis. Proceedings of the National Academy of Sciences of the United States of America, 95, 5616-5620.
14. Fujiwara, Y. & Denlinger, D.L. (2007) High temperature and hexane break pupal diapause in the flesh fly, Sarcophaga crassipalpis, by activating ERK/MAPK. Journal of Experimental Biology, 210, 3295-3300.
15. Fujiwara, H., Jindra, M., Newitt, R. etal. (1995) Cloning of an ecdysone receptor homolog from Manduca sexta and the developmental profile of its mRNA in wings. Insect Biochemistry and Molecular Biology, 25, 845-856.
16. Fujiwara, Y., Tanaka, Y., Iwatac, K.I. etal. (2006) ERK/MAPK regulates ecdysteroid and sorbitol metabolism for embryonic diapause termination in the silkworm, Bombyx mori. Journal of Insect Physiology, 52, 569-575.
17. Hahn, D.A. & Denlinger, D.L. (2011) Energetics of insect diapause. Annual Review of Entomology, 56, 103-121.
18. Hamann, S. & Strätling, W.H. (1998) Specific binding of Drosophila nuclear protein PEP (protein on ecdysone puffs) to hsp70 and RNA. Nucleic Acids Research, 26, 4108-4115.
19. Hayward, S.A.L., Pavlides, S.C., Tammariello, S.P. etal. (2005) Temporal expression patterns of diapause-associated genes in flesh fly pupae from the onset of diapause through post-diapause quiescence. Journal of Insect Physiology, 51, 631-640.
20. He, L. & Hannon, G.J. (2004) MicroRNAs: small RNAs with a big role in gene regulation. Nature Reviews Genetics, 5, 522-532.
21. Henrich, V.C. & Brown, N.E. (1995) Insect nuclear receptors: a developmental and comparative perspective. Insect Biochemistry and Molecular Biology, 25, 881-987.
22. Hobbs, G.A. & Richards, K.W. (1976) Selection for a univoltine strain of Megachile (Euthricharea) pacifica (Hymenoptera: Megachilidae). Canadian Entomologist, 108, 165-167.
23. Huang, D.W., Sherman, B.T. & Lempicki, R.A. (2008) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols, 4, 44-57.
24. Imhof, M.O., Rusconi, S. & Lezzi, M. (1993) Cloning of a Chronomus tentans cDNA encoding a protein (cEcRH) homologous to the Drosophila melanogaster ecdysome receptor (dEcR). Insect Biochemistry and Molecular Biology, 23, 115-124.
25. Johansen, C.A. & Eves, J.D. (1973) Effect of chilling, humidity and seasonal conditions on emergence of the alfalfa leafcutting bee. Environmental Entomology, 2, 23-26.
26. Kawaguchi, T., Veech, R.L. & Uyeda, K. (2001) Regulation of energy metabolism in macrophages during hypoxia: roles of fructose 2, 6-bisphosphate and ribose 1, 5-bisphosphate. Journal of Biological Chemistry, 276, 28554-28561.
27. Kemp, W.P. & Bosch, J. (2001) Postcocooning temperatures and diapause in the alfalfa pollinator Megachile rotundata (Hymenoptera: Megachilidae). Annals of the Entomological Society of America, 94, 244-250.
28. Kemp, W.P., Bosch, J. & Dennis, B. (2004) Oxygen consumption during the life cycles of the prepupae-wintering bee Megachile rotundata and the adult-wintering bee Osmia lignaria (Hymenoptera: Megachilidae). Annals of the Entomological Society of America, 97, 161-170.
29. Kennison, J.A. (1995) The polycomb and trithorax group proteins of Drosophila: trans-regulators of homeotic gene function. Annual Review of Genetics, 29, 289-303.
30. Kidokoro, K., Iwata, K.I., Takeda, M. & Fujiwara, Y. (2006) Involvement of ERK/MAPK in regulation of diapause intensity in the false melon beetle, Atrachya menetriesi. Journal of Insect Physiology, 52, 1189-1193.
31. Koštál, V. (2006) Eco-physiological phases of insect diapause. Journal of Insect Physiology, 52, 113-127.
32. Koštál, V., Simunkova, P., Kobelkova, A. & Shimada, K. (2009) Cell cycle arrest as a hallmark of insect diapause: changes in gene transcription during diapause induction in the drosophilid fly (Chymomyza costata). Insect Biochemistry and Molecular Biology, 39, 875-883.
33. Krunic, M.D. (1972) Voltinism in Megachile rotundata (Megachilidae: Hymenoptera) in Southern Alberta. Canadian Entomologist, 104, 185-188.
34. 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.
35. Lee, K.Y. & Denlinger, D.L. (1997) A role for ecdysteriods in the induction and maintenance of the pharate first instar diapause of the gypsy moth, Lymantria dispar. Journal of Insect Physiology, 43, 289-296.
36. Lu, Y.X., Denlinger, D.L. & Xu, W.-H. (2013) Polycomb repressive complex (PRC2) protein ESC regulates insect development timing by mediating H3K27me3 and activation prothoracicotropic hormone gene expression. Journal of Biological Chemistry, 288, 23554-23564.
37. Nakagaki, M., Takei, R., Nagashima, E. & Yaginuma, T. (1991) Cell cycles in embryos of the silkworm, Bombyx mori: G2-arrest at diapause stage. Developmental Biology, 200, 223-229.
38. O'Neill, K.M., O'Neill, R.P., Kemp, W.P. & Delphia, C.M. (2011) Effect of temperature on post-wintering development and total lipid content of alfalfa leafcutting bees. Environmental Entomology, 40, 917-930.
39. O'Shea, J.J., Gadina, M. & Schreiber, R.D. (2002) Cytokine signaling in 2002: new surprises in the Jak/Stat pathway. Cell, 109, S121-S131.
40. Palli, S.R., Kothapalli, R., Feng, Q. etal. (2001) Molecular analysis of overwintering diapause. Insect Timing: Circadian Rhythmicity to Seasonality (ed. by D. Denlinger, J. Giebultowicz and D. Saunders), pp. 133-144. Elsevier Science Inc., The Netherlands.
41. Parisi, F., Riccardo, S., Daniel, M. etal. (2011) Drosophila insulin and target of rapamycin (TOR) pathways regulate GSK3 beta activity to control Myc stability and determine Myc expression in vivo. BMC Biology, 9, 65.
42. Pitts-Singer, T.L. & Cane, J.H. (2011) The alfalfa leafcutting bee, Megchile rotundata: the world's most intensively managed solitary bee. Annual Review of Entomology, 56, 221-237.
43. Poelchau, M.F., Reynolds, J.A., Denlinger, D.L. etal. (2011) A de novo transcriptome of the Asian tiger mosquito, Aedes albopictus, to identity candidate transcripts for diapause preparation. BMC Genomics, 12, 619.
44. Poelchau, M.F., Reynolds, J.A., Elsik, C.G. etal. (2013a) Deep sequencing reveals complex mechanisms of diapause preparation in the invasive mosquito, Aedes albopictus. Proceedings of the Royal Society of London Series B, 280, 20130143.
45. Poelchau, M.F., Reynolds, J.A., Elsik, C.G. etal. (2013b) RNA-Seq revels early distinctions and late convergence of gene expression between diapause and quiescence in the Asia tiger mosquito, Aedes albopictus. Journal of Experimental Biology, 216, 4082-4090.
46. Polioudakis, D., Bhinge, A.A., Killion, P.J. etal. (2013) A Myc-microRNA network promotes exit from quiescence by suppressing the interferon response and cell-cycle arrest genes. Nucleic Acids Research, 41, 2239-2254.
47. Ragland, G.J., Denlinger, D.L. & Hahn, D.A. (2010) Mechanisms of suspended animation are revealed by transcript profiling in the flesh fly. Proceedings of the National Academy of Sciences of the United States of America, 107, 14909-14914.
48. Ragland, G.J., Egan, S.P., Feder, J.L. etal. (2011) Developmental trajectories of gene expression reveal candidates for diapause termination: a key life-history transition in the apple maggot fly Rhagoletis pomonella. Journal of Experimental Biology, 214, 3948-3959.
49. Reynolds, J.A., Clark, J., Diakoff, S.J. & Denlinger, D.L. (2013) Transcriptional evidence for small RNA regulation of pupal diapause in the flesh fly, Sarcophaga bullata. Insect Biochemistry and Molecular Biology, 43, 982-989.
50. Richards, K.W., Whitfield, G.H. & Schaalje, G.B. (1987) Effects of temperature and duration of winter storage and period of emergence for the alfalfa leafcutting bee (Hymenoptera: Megachilidae). Journal of the Kansas Entomological Society, 60, 70-76.
51. Rinehart, J.P., Cikra-Ireland, R.A., Flannagan, R.D. & Denlinger, D.L. (2001) Expression of ecdysone receptor is unaffected by pupal diapause in the flesh fly, Sarcophaga crassipalpis, while its dimerization partner, UPS, is downregulated. Journal of Insect Physiology, 47, 915-921.
52. Rinehart, J.P., Li, A., Yocum, G.D. etal. (2006) Insect overwintering: upregulation of heat shock proteins is essential for cold survival. Proceedings of the National Academy of Sciences of the United States of America, 104, 11130-11137.
53. Rinehart, J.P., Yocum, G.D., Kemp, W.P. & Greenlee, K.J. (2013) A fluctuating thermal regime improves long-term survival of quiescent prepupal Megachile rotundata (Hymenoptera: Megachilidae). Journal of Economic Entomology, 106, 1081-1088.
54. Ringrose, L. & Paro, R. (2004) Epigenetic regulation of cellular memory by the polycomb and trithorax group proteins. Annual Review of Genetics, 38, 414-443.
55. van Rooij, E. (2011) The art of microRNA research. Circulation Research, 108, 219-234.
56. Schwartz, Y.B. & Pirrotta, V. (2007) Polycomb silencing mechanisms and the management of genomic programmes. Nature Review Genetics, 8, 9-22.
57. Seiyama, A., Kosaka, H., Maeda, N. etal. (1996) Effect of hypothermia on skeletal muscle metabolism in perfused rat hindlimb. Cryobiology, 33, 338-346.
58. Seth, A. & Watson, D.K. (2005) ETS transcription factors and their emerging roles in human cancer. European Journal of Cancer, 41, 2462-2478.
59. Sharrocks, A.D., Brown, A.L., Ling, Y. & Yates, R.R. (1997) The ETS-domain transcription factor family. International Journal of Biochemistry and Cell Biology, 29, 1371-1387.
60. 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.
61. Sim, C. & Denlinger, D.L. (2009) 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.
62. Sláma, K. (1980) Homeostatic biosynthesis and inactivation in ecdysis and oviposition. Acta Entomologica Bohemoslovaca, 77, 145-168.
63. Steelman, L.S., Chappell, W.H., Abrams, S.L. etal. (2011) Roles of the Raf/MEK/ERK and PI3K/PTEN/Akt/mTOR in controlling growth and sensitivity to therapy-implications for cancer and aging. Aging, 3, 192-222.
64. Tammariello, S.P. & Denlinger, D.L. (1998) G0/G1 cell cycle arrest in the brain of Sarcophaga crassipalpis during pupal diapause and the expression of the cell cycle regulator, proliferating cell nuclear antigen. Insect Biochemistry and Molecular Biology, 28, 83-89.
65. Taséi, J.N. & Masure, M.M. (1978) Sur quelques facteurs influencant le developpement de Megachile pacifica Panz. (Hymenoptera: Megachilidae). Apidologie, 9, 273-290.
66. Tatun, N., Singtripop, T. & Sakurai, S. (2008) Dual control of midgut trehalase activity by 20-hydroxyecdysone and an inhibitory factor in the bamboo borer Omphisa fuscidentalis Hampson. Journal of Insect Physiology, 54, 351-357.
67. Tauber, M.J., Tauber, C.A. & Masaki, S. (1986) Seasonal Adaptations in Insects. Oxford Press, U.K.
68. Tootle, T.L. & Rebay, I. (2005) Post-translational modifications influences transcription factor activity: a view from the ETS superfamily. BioEssays, 27, 285-298.
69. Torchio, P.F. & Bosch, J. (1992) Biology of Tricrania stansburyi, a meloid beetle cleptoparasite of the bee Osmia lignaria propinqua (Hymenoptera: Megachilidae). Annals of the Entomological Society of America, 85, 713-721.
70. Trapnell, C., Pachter, L. & Salzberg, S.L. (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics, 25, 1105-1111.
71. Trapnell, C., Williams, B.A., Pertea, G. etal. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology, 28, 511-515.
72. Truman, J.W. (1981) Interaction between ecdysteroids, eclosion hormone and bursicon titers in Manduca sexta. American Zoologist, 21, 655-661.
73. Truman, J.W., Roundtree, D.B., Reiss, S.E. etal. (1983) Ecdysteroids regulate the release and action of eclosion hormone in the tobacco hornworn, Manduca sexta (L). Journal of Insect Physiology, 29, 895-900.
74. Williams, K.D., Busto, M., Suster, M.L. etal. (2006) Natural variation in Drosophila melanogaster diapause due to insulin-regulated PI3-kinase. Proceedings of the National Academy of Sciences of the United States of America, 103, 15911-15915.
75. Yocum, G.D., Kemp, W.P., Bosch, J. & Knoblet, J.N. (2005) Temporal variation in overwintering gene expression and respiration in the solitary bee Megachile rotundata. Journal of Insect Physiology, 51, 621-629.
76. Yocum, G.D., Kemp, W.P., Bosch, J. & Knoblet, J.N. (2006) Thermal history influences diapause development in the solitary bee Megachile rotundata. Journal of Insect Physiology, 52, 1113-1120.
77. Žďárek, J. & Denlinger, D.L. (1987) Pupal ecdysis in flies: the role of ecdysteroids in its regulation. Journal of Insect Physiology, 33, 123-128.
78. Zeeberg, B.R., Feng, W., Wang, G. etal. (2003) GoMiner: a resource for biological interpretation of genomic and proteomic data. Genome Biology, 4, R28.
79. Zhang, H., Bosch-Marce, M., Shimoda, L.A. etal. (2008) Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. Journal of Biological Chemistry, 283, 10892-10903.