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

Insect diapause (dormancy) synchronizes an insect's life cycle to seasonal changes in the abiotic and biotic resources required for development and reproduction. Transcription analysis of diapause to post‐diapause quiescent transition in the alfalfa leafcutting bee Megachile rotundata Fabricius identifies 643 post‐diapause up‐regulated gene transcripts and 242 post‐diapause down‐regulated transcripts. The log2 fold change in gene expression levels ranges from −5 to 7. Transcripts from several pivotal diapause‐related processes, including chromatin remodelling, cellular signalling pathways, microRNA processing, anaerobic glycolysis, cell cycle arrest and neuroendocrine control, are identified as being differentially expressed during the diapause to post‐diapause transition. In conjunction with studies from other insect species, the data indicate that there are several common mechanisms of diapause control and maintenance.

[1]  Monica F. Poelchau,et al.  RNA-Seq reveals early distinctions and late convergence of gene expression between diapause and quiescence in the Asian tiger mosquito, Aedes albopictus , 2013, Journal of Experimental Biology.

[2]  Jennifer I. Clark,et al.  Transcriptional evidence for small RNA regulation of pupal diapause in the flesh fly, Sarcophaga bullata. , 2013, Insect biochemistry and molecular biology.

[3]  D. Denlinger,et al.  Polycomb Repressive Complex 2 (PRC2) Protein ESC Regulates Insect Developmental Timing by Mediating H3K27me3 and Activating Prothoracicotropic Hormone Gene Expression* , 2013, The Journal of Biological Chemistry.

[4]  J. Rinehart,et al.  A Fluctuating Thermal Regime Improves Long-Term Survival of Quiescent Prepupal Megachile rotundata (Hymenoptera: Megachilidae) , 2013, Journal of economic entomology.

[5]  Monica F. Poelchau,et al.  Deep sequencing reveals complex mechanisms of diapause preparation in the invasive mosquito, Aedes albopictus , 2013, Proceedings of the Royal Society B: Biological Sciences.

[6]  Nathan S. Abell,et al.  A Myc–microRNA network promotes exit from quiescence by suppressing the interferon response and cell-cycle arrest genes , 2013, Nucleic acids research.

[7]  Monica F. Poelchau,et al.  A de novo transcriptome of the Asian tiger mosquito, Aedes albopictus, to identify candidate transcripts for diapause preparation , 2011, BMC Genomics.

[8]  J. Feder,et al.  Developmental trajectories of gene expression reveal candidates for diapause termination: a key life-history transition in the apple maggot fly Rhagoletis pomonella , 2011, Journal of Experimental Biology.

[9]  E. Tabak,et al.  Drosophila insulin and target of rapamycin (TOR) pathways regulate GSK3 beta activity to control Myc stability and determine Myc expression in vivo , 2011, BMC Biology.

[10]  K. M. O'Neill,et al.  Effect of Temperature on Post-Wintering Development and Total Lipid Content of Alfalfa Leafcutting Bees , 2011, Environmental entomology.

[11]  Stephen L. Abrams,et al.  Roles of the Raf/MEK/ERK and PI3K/PTEN/Akt/mTOR pathways in controlling growth and sensitivity to therapy-implications for cancer and aging , 2011, Aging.

[12]  E. Rooij,et al.  The Art of MicroRNA Research , 2011 .

[13]  D. Denlinger,et al.  Mechanisms of suspended animation are revealed by transcript profiling of diapause in the flesh fly , 2010, Proceedings of the National Academy of Sciences.

[14]  Cole Trapnell,et al.  Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. , 2010, Nature biotechnology.

[15]  V. Košťál,et al.  Cell cycle arrest as a hallmark of insect diapause: changes in gene transcription during diapause induction in the drosophilid fly, Chymomyza costata. , 2009, Insect biochemistry and molecular biology.

[16]  C. Sim,et al.  A shut‐down in expression of an insulin‐like peptide, ILP‐1, halts ovarian maturation during the overwintering diapause of the mosquito Culex pipiens , 2009, Insect molecular biology.

[17]  Lior Pachter,et al.  Sequence Analysis , 2020, Definitions.

[18]  Cole Trapnell,et al.  Ultrafast and memory-efficient alignment of short DNA sequences to the human genome , 2009, Genome Biology.

[19]  D. Bartel MicroRNAs: Target Recognition and Regulatory Functions , 2009, Cell.

[20]  J. Downward,et al.  Many faces of Ras activation. , 2008, Biochimica et biophysica acta.

[21]  C. Sim,et al.  Insulin signaling and FOXO regulate the overwintering diapause of the mosquito Culex pipiens , 2008, Proceedings of the National Academy of Sciences.

[22]  G. Semenza,et al.  Mitochondrial Autophagy Is an HIF-1-dependent Adaptive Metabolic Response to Hypoxia* , 2008, Journal of Biological Chemistry.

[23]  Ted Powers,et al.  Regulation of ceramide biosynthesis by TOR complex 2. , 2008, Cell metabolism.

[24]  Stijn van Dongen,et al.  Graph Clustering Via a Discrete Uncoupling Process , 2008, SIAM J. Matrix Anal. Appl..

[25]  S. Sakurai,et al.  Dual control of midgut trehalase activity by 20-hydroxyecdysone and an inhibitory factor in the bamboo borer Omphisa fuscidentalis Hampson. , 2008, Journal of insect physiology.

[26]  D. Denlinger,et al.  High temperature and hexane break pupal diapause in the flesh fly, Sarcophaga crassipalpis, by activating ERK/MAPK. , 2007, Journal of insect physiology.

[27]  D. Denlinger,et al.  p38 MAPK is a likely component of the signal transduction pathway triggering rapid cold hardening in the flesh fly Sarcophaga crassipalpis , 2007, Journal of Experimental Biology.

[28]  D. Denlinger,et al.  Up-regulation of heat shock proteins is essential for cold survival during insect diapause , 2007, Proceedings of the National Academy of Sciences.

[29]  J. Bosch,et al.  Thermal history influences diapause development in the solitary bee Megachile rotundata. , 2006, Journal of insect physiology.

[30]  Y. Fujiwara,et al.  Involvement of ERK/MAPK in regulation of diapause intensity in the false melon beetle, Atrachya menetriesi. , 2006, Journal of insect physiology.

[31]  M. Suster,et al.  Natural variation in Drosophila melanogaster diapause due to the insulin-regulated PI3-kinase , 2006, Proceedings of the National Academy of Sciences.

[32]  Yoshiaki Tanaka,et al.  ERK/MAPK regulates ecdysteroid and sorbitol metabolism for embryonic diapause termination in the silkworm, Bombyx mori. , 2006, Journal of insect physiology.

[33]  V. Košťál Eco-physiological phases of insect diapause. , 2006, Journal of insect physiology.

[34]  A. Seth,et al.  ETS transcription factors and their emerging roles in human cancer. , 2005, European journal of cancer.

[35]  Juan Miguel García-Gómez,et al.  BIOINFORMATICS APPLICATIONS NOTE Sequence analysis Manipulation of FASTQ data with Galaxy , 2005 .

[36]  D. Denlinger,et al.  Temporal expression patterns of diapause-associated genes in flesh fly pupae from the onset of diapause through post-diapause quiescence. , 2005, Journal of insect physiology.

[37]  J. Bosch,et al.  Temporal variation in overwintering gene expression and respiration in the solitary bee Megachile rotundata. , 2005, Journal of insect physiology.

[38]  I. Rebay,et al.  Post‐translational modifications influence transcription factor activity: A view from the ETS superfamily , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[39]  Lin He,et al.  MicroRNAs: small RNAs with a big role in gene regulation , 2004, Nature Reviews Genetics.

[40]  May D. Wang,et al.  GoMiner: a resource for biological interpretation of genomic and proteomic data , 2003, Genome Biology.

[41]  Massimo Gadina,et al.  Cytokine Signaling in 2002 New Surprises in the Jak/Stat Pathway , 2002, Cell.

[42]  A. Sharrocks The ETS-domain transcription factor family , 2001, Nature Reviews Molecular Cell Biology.

[43]  K. Uyeda,et al.  Regulation of Energy Metabolism in Macrophages during Hypoxia , 2001, The Journal of Biological Chemistry.

[44]  Ronald D. Flannagan,et al.  Expression of ecdysone receptor is unaffected by pupal diapause in the flesh fly, Sarcophaga crassipalpis, while its dimerization partner, USP, is downregulated , 2001 .

[45]  J. Bosch,et al.  Postcocooning Temperatures and Diapause in the Alfalfa Pollinator Megachile rotundata (Hymenoptera: Megachilidae) , 2001 .

[46]  W. Strätling,et al.  Specific binding of Drosophila nuclear protein PEP (protein on ecdysone puffs) to hsp70 DNA and RNA. , 1998, Nucleic acids research.

[47]  Ronald D. Flannagan,et al.  Diapause-specific gene expression in pupae of the flesh fly Sarcophaga crassipalpis. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[48]  D. Denlinger,et al.  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. , 1998, Insect biochemistry and molecular biology.

[49]  D. Denlinger,et al.  A Role for Ecdysteroids in the Induction and Maintenance of the Pharate First Instar Diapause of the Gypsy Moth, Lymantria dispar. , 1997, Journal of insect physiology.

[50]  A. Seiyama,et al.  Effect of hypothermia on skeletal muscle metabolism in perfused rat hindlimb. , 1996, Cryobiology.

[51]  V. Henrich,et al.  Insect nuclear receptors: a developmental and comparative perspective. , 1995, Insect biochemistry and molecular biology.

[52]  L. Riddiford,et al.  Cloning of an ecdysone receptor homolog from Manduca sexta and the developmental profile of its mRNA in wings. , 1995, Insect biochemistry and molecular biology.

[53]  J. Bosch,et al.  Biology of Tricrania stansburyi, a Meloid Beetle Cleptoparasite of the Bee Osmia lignaria propinqua (Hymenoptera: Megachilidae) , 1992 .

[54]  M. Nakagaki,et al.  Cell cycles in embryos of the silkworm, Bombyx mori: G2-arrest at diapause stage , 1991, Roux's archives of developmental biology.

[55]  A. Beyer,et al.  A unique zinc finger protein is associated preferentially with active ecdysone-responsive loci in Drosophila. , 1991, Genes & development.

[56]  D. Hogness,et al.  The Drosophila 74EF early puff contains E74, a complex ecdysone-inducible gene that encodes two ets-related proteins , 1990, Cell.

[57]  W. J. Bell,et al.  Seasonal adaptations of insects. , 1987 .

[58]  J. Truman Interaction Between Ecdysteroid, Eclosion Hormone, and Bursicon Titers inManduca sexta , 1981 .

[59]  K. Richards,et al.  SELECTION FOR A UNIVOLTINE STRAIN OF MEGACHILE (EUTRICHARAEA) PACIFICA (HYMENOPTERA: MEGACHILIDAE) , 1976, The Canadian Entomologist.

[60]  M. Ashburner Sequential gene activation by ecdysone in polytene chromosomes of Drosophila melanogaster. I. Dependence upon ecdysone concentration. , 1973, Developmental biology.

[61]  C. Johansen,et al.  Effects of Chilling, Humidity and Seasonal Conditions on Emergence of the Alfalfa Leafcutting Bee , 1973 .

[62]  M. Krunić VOLTINISM IN MEGACHILE ROTUNDATA (MEGACHILIDAE: HYMENOPTERA) IN SOUTHERN ALBERTA , 1972, The Canadian Entomologist.

[63]  D. Denlinger,et al.  10 – Hormonal Control of Diapause , 2012 .

[64]  T. Pitts‐Singer,et al.  The alfalfa leafcutting bee, Megachile rotundata: the world's most intensively managed solitary bee. , 2011, Annual review of entomology.

[65]  D. Denlinger,et al.  Energetics of insect diapause. , 2011, Annual review of entomology.

[66]  Brad T. Sherman,et al.  Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources , 2008, Nature Protocols.

[67]  Jo Handelsman,et al.  EPIGENETIC REGULATION OF CELLULAR MEMORY BY THE POLYCOMB AND TRITHORAX GROUP PROTEINS , 2008 .

[68]  Vincenzo Pirrotta,et al.  Polycomb silencing mechanisms and the management of genomic programmes , 2007, Nature Reviews Genetics.

[69]  D. Denlinger 3.12 – Hormonal Control of Diapause , 2005 .

[70]  M. Ashburner Patterns of puffing activity in the salivary gland chromosomes of Drosophila , 2004, Chromosoma.

[71]  B. Dennis,et al.  Oxygen Consumption During the Life Cycles of the Prepupa-Wintering Bee Megachile rotundata and the Adult-Wintering Bee Osmia lignaria (Hymenoptera: Megachilidae) , 2004 .

[72]  S. R. Palli,et al.  Molecular analysis of overwintering diapause , 2001 .

[73]  J. Kennison The Polycomb and trithorax group proteins of Drosophila: trans-regulators of homeotic gene function. , 1995, Annual review of genetics.

[74]  M. Imhof,et al.  Cloning of a Chironomus tentans cDNA encoding a protein (cEcRH) homologous to the Drosophila melanogaster ecdysteroid receptor (dEcR). , 1993, Insect biochemistry and molecular biology.

[75]  D. Denlinger,et al.  Pupal ecdysis in flies: The role of ecdysteroids in its regulation , 1987 .

[76]  H. Danks Insect dormancy: an ecological perspective. , 1987 .

[77]  J. Truman,et al.  Ecdysteroids regulate the release and action of eclosion hormone in the tobacco hornworm, Manduca sexta (L.) , 1983 .

[78]  K. Slăma Homeostatic function of ecdysteroids in ecdysis and oviposition. , 1980 .

[79]  J. Tasei,et al.  SUR QUELQUES FACTEURS INFLUENÇANT LE DÉVELOPPEMENT DE MEGACHILE PACIFICA PANZ (HYMENOPTERA, MEGACHILIDAE) , 1978 .