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Proceedings of the National Academy of Sciences of the United States of America
08 08, 2017;114 (32): 8532-8537.

Conceptual framework of the eco-physiological phases of insect diapause development justified by transcriptomic profiling.

Vladimír Koštál, Tomáš Štětina, Rodolphe Poupardin, Jaroslava Korbelová, Alexander William Bruce
Author Information
  1. Vladimír Koštál: Biology Centre, Institute of Entomology, Academy of Sciences of the Czech Republic, 37005 Budweis, Czech Republic; kostal@entu.cas.cz. ORCID
  2. Tomáš Štětina: Biology Centre, Institute of Entomology, Academy of Sciences of the Czech Republic, 37005 Budweis, Czech Republic.
  3. Rodolphe Poupardin: Biology Centre, Institute of Entomology, Academy of Sciences of the Czech Republic, 37005 Budweis, Czech Republic.
  4. Jaroslava Korbelová: Biology Centre, Institute of Entomology, Academy of Sciences of the Czech Republic, 37005 Budweis, Czech Republic.
  5. Alexander William Bruce: Faculty of Science, University of South Bohemia, 37005 Budweis, Czech Republic.
PMID: 28720705 DOI: 10.1073/pnas.1707281114

Abstract

Insects often overcome unfavorable seasons in a hormonally regulated state of diapause during which their activity ceases, development is arrested, metabolic rate is suppressed, and tolerance of environmental stress is bolstered. Diapausing insects pass through a stereotypic succession of eco-physiological phases termed "diapause development." The phasing is varied in the literature, and the whole concept is sometimes criticized as being too artificial. Here we present the results of transcriptional profiling using custom microarrays representing 1,042 genes in the drosophilid fly, Fully grown, third-instar larvae programmed for diapause by a photoperiodic (short-day) signal were assayed as they traversed the diapause developmental program. When analyzing the gradual dynamics in the transcriptomic profile, we could readily distinguish distinct diapause developmental phases associated with induction/initiation, maintenance, cold acclimation, and termination by cold or by photoperiodic signal. Accordingly, each phase is characterized by a specific pattern of gene expression, supporting the physiological relevance of the concept of diapause phasing. Further, we have dissected in greater detail the changes in transcript levels of elements of several signaling pathways considered critical for diapause regulation. The phase of diapause termination is associated with enhanced transcript levels in several positive elements stimulating direct development (the 20-hydroxyecdysone pathway: , , ; the Wnt pathway: , ) that are countered by up-regulation in some negative elements (the insulin-signaling pathway: , , ; the target of rapamycin pathway: and ; the Wnt pathway: ). We speculate such up-regulations may represent the early steps linked to termination of diapause programming.

Keywords

development diapause insects microarrays transcriptomics

References

  1. BMC Ecol. 2010 Feb 01;10:3 [PMID: 20122138]
  2. Physiol Entomol. 2013 Jun;38(2):96-104 [PMID: 23894219]
  3. Aging Cell. 2016 Apr;15(2):196-207 [PMID: 26643314]
  4. PLoS One. 2010 Mar 05;5(3):e9574 [PMID: 20221437]
  5. J Nutr. 2001 Nov;131(11):2988S-93S [PMID: 11694634]
  6. Genetics. 1998 May;149(1):217-31 [PMID: 9584098]
  7. J Insect Physiol. 2010 Sep;56(9):1147-54 [PMID: 20230829]
  8. Dev Biol. 2000 May 15;221(2):404-18 [PMID: 10790335]
  9. Science. 2005 Oct 28;310(5748):667-70 [PMID: 16179433]
  10. Int J Biochem Cell Biol. 2009 May;41(5):1006-10 [PMID: 18992839]
  11. Cell Mol Life Sci. 2010 Jul;67(14):2405-24 [PMID: 20213274]
  12. Proc Biol Sci. 2013 Mar 20;280(1759):20130143 [PMID: 23516243]
  13. Science. 2012 May 4;336(6081):582-5 [PMID: 22556251]
  14. J Insect Physiol. 2000 Apr;46(4):417-428 [PMID: 12770205]
  15. Science. 2010 Mar 5;327(5970):1223-8 [PMID: 20203043]
  16. Proc Natl Acad Sci U S A. 2003 Nov 25;100(24):13773-8 [PMID: 14610274]
  17. Mol Cell Endocrinol. 2004 Jan 15;213(2):155-66 [PMID: 15062563]
  18. J Insect Physiol. 2007 Dec;53(12):1276-82 [PMID: 17681525]
  19. J Insect Physiol. 2011 Jun;57(6):840-50 [PMID: 21435341]
  20. Proc Natl Acad Sci U S A. 1989 Feb;86(4):1421-5 [PMID: 2493154]
  21. BMC Genomics. 2015 Sep 21;16:720 [PMID: 26391666]
  22. Annu Rev Entomol. 1986;31:239-64 [PMID: 3510585]
  23. PLoS Genet. 2010 Feb 26;6(2):e1000857 [PMID: 20195512]
  24. Dev Cell. 2008 Oct;15(4):568-77 [PMID: 18854141]
  25. J Exp Biol. 2016 Sep 1;219(Pt 17):2613-22 [PMID: 27312473]
  26. Proc Natl Acad Sci U S A. 2008 May 6;105(18):6777-81 [PMID: 18448677]
  27. J Insect Physiol. 2004 Nov;50(11):1053-64 [PMID: 15607508]
  28. Proc Natl Acad Sci U S A. 2005 Nov 1;102(44):15912-7 [PMID: 16247003]
  29. Novartis Found Symp. 2001;237:182-94; discussion 194-202 [PMID: 11444043]
  30. Antioxid Redox Signal. 2011 Feb 15;14(4):593-605 [PMID: 20618067]
  31. PLoS One. 2010 Feb 05;5(2):e9059 [PMID: 20140202]
  32. J Insect Physiol. 2005 Jun;51(6):631-40 [PMID: 15993127]
  33. Eur J Biochem. 1993 May 1;213(3):1125-31 [PMID: 8504807]
  34. Proc Natl Acad Sci U S A. 2010 Aug 17;107(33):14909-14 [PMID: 20668242]
  35. Biochem Soc Trans. 2015 Oct;43(5):1057-62 [PMID: 26517923]
  36. J Insect Physiol. 2006 Feb;52(2):113-27 [PMID: 16332347]
  37. Mol Cell. 2003 Jun;11(6):1457-66 [PMID: 12820960]
  38. Nucleic Acids Res. 2001 May 1;29(9):e45 [PMID: 11328886]
  39. Proc Natl Acad Sci U S A. 2015 Mar 24;112(12):3811-6 [PMID: 25775593]
  40. Nucleic Acids Res. 2015 Apr 20;43(7):e47 [PMID: 25605792]
  41. J Exp Biol. 2009 Jul;212(Pt 13):2075-84 [PMID: 19525434]
  42. J Exp Biol. 2016 Aug 1;219(Pt 15):2358-67 [PMID: 27489218]
  43. Proc Natl Acad Sci U S A. 2006 Oct 24;103(43):15911-5 [PMID: 17043223]
  44. Development. 1998 Dec;125(23):4709-17 [PMID: 9806919]
  45. Biochem J. 2009 Dec 14;425(1):13-26 [PMID: 20001959]
  46. PLoS One. 2007 Jan 31;2(1):e187 [PMID: 17264888]
  47. Science. 2001 Apr 6;292(5514):107-10 [PMID: 11292875]
  48. Dev Biol. 1993 Mar;156(1):117-35 [PMID: 8449364]
  49. Curr Opin Insect Sci. 2016 Oct;17 :49-54 [PMID: 27720073]
  50. Front Physiol. 2013 Sep 26;4:263 [PMID: 24133450]
  51. Genes Dev. 2001 Jun 1;15(11):1383-92 [PMID: 11390358]
  52. Biol Bull. 1946 Jun;90:234-43 [PMID: 20988208]
  53. Trends Biochem Sci. 2004 Feb;29(2):95-102 [PMID: 15102436]
  54. Curr Biol. 2002 Aug 6;12(15):1293-300 [PMID: 12176357]
  55. Gen Comp Endocrinol. 2005 Jul;142(3):347-56 [PMID: 15935161]
  56. Proc Natl Acad Sci U S A. 2011 Aug 9;108(32):13041-6 [PMID: 21788482]
  57. J Exp Biol. 2011 Dec 1;214(Pt 23):3948-59 [PMID: 22071185]
  58. Genetics. 2004 May;167(1):311-23 [PMID: 15166157]
  59. Trends Genet. 2009 May;25(5):217-25 [PMID: 19375812]
  60. Nucleic Acids Res. 2003 Jun 15;31(12):3057-62 [PMID: 12799432]
  61. Annu Rev Entomol. 2013;58:251-71 [PMID: 23072463]
  62. Front Physiol. 2013 Jul 22;4:189 [PMID: 23885240]
  63. Front Physiol. 2014 Mar 20;5:103 [PMID: 24688471]
  64. Genes Dev. 2007 Mar 15;21(6):632-7 [PMID: 17369395]
  65. Dev Cell. 2001 Oct;1(4):453-65 [PMID: 11703937]
  66. Science. 2012 May 4;336(6081):579-82 [PMID: 22556250]
  67. Trends Cell Biol. 2013 Jul;23(7):336-44 [PMID: 23587490]
  68. Insect Biochem Mol Biol. 2009 Dec;39(12):875-83 [PMID: 19879357]
  69. J Insect Physiol. 2011 May;57(5):628-34 [PMID: 21277308]
  70. Biochim Biophys Acta. 2011 Nov;1813(11):1965-70 [PMID: 21440577]
  71. Nat Rev Genet. 2006 Dec;7(12):907-16 [PMID: 17139322]

MeSH Term

Animals
Circadian Rhythm
Diapause
Diapause, Insect
Drosophilidae
Gene Expression Profiling
Gene Expression Regulation, Developmental
Insect Proteins
Insecta
Larva
Oligonucleotide Array Sequence Analysis
Photoperiod
Transcriptome

Chemicals

Insect Proteins
Journal Article Research Support, Non-U.S. Gov't
Article has an altmetric score of 2

Word Cloud

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