Cephalic ganglia transcriptomics of the American cockroach Periplaneta americana (Blattodea: Blattidae).

Ilana Levy, Ryan Arvidson
Author Information
  1. Ilana Levy: Undergraduate Program in Biochemistry, Department of Biochemistry, Case Western Reserve University, Cleveland, OH, USA.
  2. Ryan Arvidson: Department of Biochemistry, Case Western Reserve University, Cleveland, OH, USA. ORCID

Abstract

The American cockroach Periplaneta americana (L.) (Blattodea, Blattidae) has been a model organism for biochemical and physiological study for almost a century, however, its use does not benefit from the genetic tools found in key model species such as Drosophila melanogaster. To facilitate the use of the cockroach as a model system in neuroscience and to serve as a foundation for functional and translational experimentation, a transcriptome of the cephalic ganglia was assembled and annotated, and differential expression profiles between these ganglia were assessed. The transcriptome assembly yielded >400 k transcripts, with >40 k putative coding sequences. Gene ontology and protein domain searches indicate the cerebral and gnathal ganglia (GNG) have distinct genetic expression profiles. The developmental Toll signaling pathway appears to be active in the adult central nervous system (CNS), which may suggest a separate role for this pathway besides innate immune activation or embryonic development. The catabolic glycolytic and citric acid cycle enzymes are well represented in both ganglia, but key enzymes are more highly expressed in the GNG. Both ganglia express gluconeogenic and trehaloneogenic enzymes, suggesting a larger role of the CNS in regulating hemolymph sugar homeostasis than previously appreciated. The annotation and quantification of the cephalic ganglia transcriptome reveal both canonical and novel pathways in signaling and metabolism in an adult insect and lay a foundation for future functional and genetic analysis.

Keywords

References

  1. J Toxicol. 2012;2012:143740 [PMID: 22666245]
  2. Genome Biol. 2006;7(8):232 [PMID: 16930467]
  3. Nat Methods. 2010 Nov;7(11):909-12 [PMID: 20935650]
  4. Development. 2009 Apr;136(7):1211-21 [PMID: 19270177]
  5. Cell Rep. 2024 Mar 26;43(3):113889 [PMID: 38416646]
  6. Adv Genet. 2011;73:1-50 [PMID: 21310293]
  7. Methods Mol Biol. 2016;1374:23-54 [PMID: 26519399]
  8. Dev Biol. 2001 Dec 15;240(2):611-26 [PMID: 11784087]
  9. Cold Spring Harb Perspect Biol. 2013 Jun 01;5(6): [PMID: 23732470]
  10. J Biol Chem. 2013 Feb 22;288(8):5660-72 [PMID: 23303188]
  11. Genome. 2017 Jan;60(1):1-7 [PMID: 27848260]
  12. J Exp Biol. 2011 Nov 15;214(Pt 22):3843-9 [PMID: 22031749]
  13. Cold Spring Harb Perspect Biol. 2014 Feb 01;6(2): [PMID: 24370848]
  14. Front Physiol. 2015 Jul 24;6:207 [PMID: 26257659]
  15. PLoS Biol. 2020 Dec 8;18(12):e3000703 [PMID: 33290404]
  16. Pharmacol Rev. 2011 Jun;63(2):411-36 [PMID: 21415126]
  17. Curr Biol. 2016 Oct 24;26(20):R1022-R1038 [PMID: 27780045]
  18. Int J Mol Sci. 2021 Jul 13;22(14): [PMID: 34299134]
  19. J Insect Physiol. 2004 Sep;50(9):821-30 [PMID: 15350502]
  20. Insect Biochem Mol Biol. 2012 Jun;42(6):396-403 [PMID: 22685715]
  21. Dev Cell. 2016 Oct 24;39(2):267-278 [PMID: 27780041]
  22. Annu Rev Cell Dev Biol. 1996;12:393-416 [PMID: 8970732]
  23. Mol Biol Evol. 2013 Apr;30(4):772-80 [PMID: 23329690]
  24. Front Physiol. 2020 Jan 08;10:1539 [PMID: 31969831]
  25. Nucleic Acids Res. 2021 Jan 8;49(D1):D899-D907 [PMID: 33219682]
  26. Front Physiol. 2022 Nov 11;13:1002183 [PMID: 36439265]
  27. Science. 2009 Dec 4;326(5958):1403-5 [PMID: 19965758]
  28. Genome Biol. 2011 Jun 24;12(6):224 [PMID: 21722353]
  29. PLoS One. 2009 May 21;4(5):e5651 [PMID: 19461966]
  30. Mol Neurobiol. 2014 Feb;49(1):303-15 [PMID: 23990374]
  31. Bioinformatics. 2014 May 1;30(9):1236-40 [PMID: 24451626]
  32. Cell Metab. 2015 Sep 1;22(3):437-47 [PMID: 26235423]
  33. Nucleic Acids Res. 2018 Jul 2;46(W1):W537-W544 [PMID: 29790989]
  34. Genome Biol. 2014;15(12):550 [PMID: 25516281]
  35. Nat Biotechnol. 2016 May;34(5):525-7 [PMID: 27043002]
  36. Genome Res. 2016 Aug;26(8):1134-44 [PMID: 27252236]
  37. Front Immunol. 2014 Sep 25;5:461 [PMID: 25309543]
  38. Am J Psychol. 1946 Jan;59:1-58 [PMID: 21015312]
  39. Genome Res. 2020 Nov;30(11):1559-1569 [PMID: 32973040]
  40. Exp Neurol. 2015 Dec;274(Pt A):58-71 [PMID: 26024860]
  41. Nucleic Acids Res. 2008 Jun;36(10):3420-35 [PMID: 18445632]
  42. Insect Biochem Mol Biol. 2019 Mar;106:64-78 [PMID: 30508629]
  43. Curr Biol. 2004 Jul 13;14(13):1208-13 [PMID: 15242619]
  44. Cell Death Differ. 2000 Nov;7(11):1075-80 [PMID: 11139281]
  45. Dev Biol. 2019 Oct 15;454(2):181-189 [PMID: 31207209]
  46. Proc Natl Acad Sci U S A. 2013 Dec 17;110(51):20461-6 [PMID: 24282309]
  47. Proc Natl Acad Sci U S A. 2005 Feb 22;102(8):2820-5 [PMID: 15703293]
  48. PLoS Genet. 2007 Dec 28;3(12):e234 [PMID: 18166084]
  49. Elife. 2021 Jun 21;10: [PMID: 34151772]
  50. Neuron. 2014 Feb 19;81(4):755-65 [PMID: 24559671]
  51. Cell Rep Methods. 2022 May 16;2(5):100215 [PMID: 35637909]
  52. Cell. 1994 Feb 25;76(4):677-88 [PMID: 8124709]
  53. Proc Natl Acad Sci U S A. 2013 Sep 3;110(36):14688-92 [PMID: 23959885]
  54. Cell Rep. 2015 May 12;11(6):866-874 [PMID: 25937282]
  55. PLoS One. 2015 Jul 13;10(7):e0133017 [PMID: 26168160]
  56. Protein Sci. 2009 Nov;18(11):2203-8 [PMID: 19672878]
  57. BMC Biol. 2018 Jan 30;16(1):18 [PMID: 29382341]
  58. Proc Natl Acad Sci U S A. 2015 Apr 21;112(16):5057-62 [PMID: 25848040]
  59. Cell. 2001 Oct 5;107(1):17-26 [PMID: 11595182]
  60. Cell Signal. 2013 Jun;25(6):1468-75 [PMID: 23524329]
  61. Int J Mol Sci. 2020 Jan 30;21(3): [PMID: 32019113]
  62. PLoS Biol. 2008 Nov 18;6(11):e284 [PMID: 19018662]
  63. BMC Genomics. 2013 May 30;14:361 [PMID: 23721482]
  64. Cell Rep. 2024 Jan 23;43(1):113640 [PMID: 38180839]
  65. Neuron. 2007 May 3;54(3):403-16 [PMID: 17481394]
  66. Genetics. 2015 Nov;201(3):815-42 [PMID: 26564900]
  67. Genes Dev. 1999 Apr 1;13(7):792-7 [PMID: 10197979]
  68. Curr Biol. 2019 Apr 22;29(8):1263-1272.e5 [PMID: 30930040]
  69. Dev Neurobiol. 2007 Feb 15;67(3):378-93 [PMID: 17443795]
  70. Physiol Rev. 2022 Oct 1;102(4):1587-1624 [PMID: 35468004]
  71. Bioinformatics. 2015 Oct 1;31(19):3210-2 [PMID: 26059717]
  72. J Biol Chem. 2010 Jun 18;285(25):19502-9 [PMID: 20378549]
  73. Front Endocrinol (Lausanne). 2012 Nov 30;3:151 [PMID: 23226142]
  74. Insect Biochem Mol Biol. 2004 Feb;34(2):113-20 [PMID: 14871607]
  75. Cell Rep. 2020 Feb 25;30(8):2627-2643.e5 [PMID: 32101741]
  76. EMBO J. 2004 Jan 14;23(1):100-10 [PMID: 14685264]
  77. Proc Natl Acad Sci U S A. 1993 May 1;90(9):4236-40 [PMID: 7683429]
  78. Nat Immunol. 2003 Aug;4(8):794-800 [PMID: 12872120]
  79. Open Biol. 2018 Oct 3;8(10): [PMID: 30282660]
  80. PLoS One. 2016 Aug 05;11(8):e0160531 [PMID: 27494326]
  81. Nat Cell Biol. 2014 Feb;16(2):157-66 [PMID: 24441527]
  82. J Exp Biol. 2015 Apr;218(Pt 7):1022-7 [PMID: 25687435]
  83. Development. 2018 Dec 4;145(23): [PMID: 30327326]
  84. J Mol Cell Biol. 2015 Jun;7(3):280-2 [PMID: 25801960]
  85. PLoS Genet. 2010 Sep 02;6(9):e1001087 [PMID: 20824130]
  86. Biomed Res Int. 2018 Apr 5;2018:5065190 [PMID: 29850527]
  87. Nucleic Acids Res. 1996 Jan 1;24(1):21-5 [PMID: 8594581]
  88. J Exp Biol. 2013 Mar 15;216(Pt 6):992-1002 [PMID: 23197098]
  89. Genome Biol. 2010;11(3):R25 [PMID: 20196867]
  90. Gen Comp Endocrinol. 2023 May 1;335:114233 [PMID: 36791825]
  91. Curr Opin Neurol. 2021 Aug 1;34(4):578-588 [PMID: 34010218]
  92. Cell Tissue Res. 2011 Feb;343(2):357-69 [PMID: 21174124]
  93. Fly (Austin). 2013 Oct-Dec;7(4):229-36 [PMID: 24022020]
  94. Neurobiol Dis. 2019 Dec;132:104535 [PMID: 31310802]
  95. Sci Rep. 2013 Sep 26;3:2765 [PMID: 24067446]
  96. Mol Biol Cell. 2003 Jan;14(1):241-50 [PMID: 12529440]
  97. Front Physiol. 2020 Feb 21;11:135 [PMID: 32153430]
  98. PLoS Biol. 2006 Oct;4(11):e348 [PMID: 17032066]
  99. Nat Rev Neurosci. 2011 May;12(5):269-83 [PMID: 21505516]
  100. Nucleic Acids Res. 2003 Jan 1;31(1):365-70 [PMID: 12520024]
  101. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2006 Sep;192(9):1003-20 [PMID: 16733727]
  102. Int J Mol Sci. 2018 Dec 07;19(12): [PMID: 30544507]
  103. J Cell Sci. 2014 Jan 1;127(Pt 1):101-10 [PMID: 24163435]
  104. Integr Comp Biol. 2009 Oct;49(4):380-92 [PMID: 21665828]
  105. Elife. 2024 Jun 21;12: [PMID: 38904987]
  106. Mol Biol Evol. 2020 May 1;37(5):1530-1534 [PMID: 32011700]
  107. Bioinformatics. 2012 Apr 15;28(8):1086-92 [PMID: 22368243]
  108. Nat Rev Cancer. 2013 Oct;13(10):685-700 [PMID: 24060861]
  109. Nat Commun. 2015 Oct 28;6:8759 [PMID: 26508274]
  110. Curr Biol. 2023 Feb 6;33(3):449-463.e5 [PMID: 36580915]
  111. Nat Rev Neurosci. 2021 Mar;22(3):137-151 [PMID: 33420412]
  112. Biol Open. 2018 Nov 2;7(11): [PMID: 30341100]
  113. Cell. 1996 Sep 20;86(6):973-83 [PMID: 8808632]
  114. Mol Biol Evol. 2018 Feb 1;35(2):518-522 [PMID: 29077904]
  115. J Mol Biol. 2001 Jan 19;305(3):567-80 [PMID: 11152613]
  116. Exp Gerontol. 2011 May;46(5):376-81 [PMID: 20849947]
  117. Science. 2016 Sep 30;353(6307):1553-1556 [PMID: 27708106]
  118. Neurobiol Dis. 2010 Oct;40(1):113-9 [PMID: 20211259]
  119. Fly (Austin). 2013 Jul-Sep;7(3):161-7 [PMID: 24047959]
  120. J Neurol. 2019 Feb;266(2):533-544 [PMID: 30284037]
  121. Dev Cell. 2022 Jul 11;57(13):1643-1660.e7 [PMID: 35654038]
  122. Front Physiol. 2016 Jun 23;7:244 [PMID: 27445837]
  123. J Comput Biol. 2013 Oct;20(10):714-37 [PMID: 24093227]
  124. J Insect Physiol. 2013 Feb;59(2):171-8 [PMID: 22664137]
  125. Proc Natl Acad Sci U S A. 2001 Apr 24;98(9):5055-60 [PMID: 11296245]
  126. J Exp Biol. 2010 Jul 1;213(Pt 13):2256-65 [PMID: 20543124]
  127. Cell. 1985 Oct;42(3):779-89 [PMID: 3931918]
  128. Insect Biochem Mol Biol. 2011 Aug;41(8):637-44 [PMID: 21536128]
  129. Nat Methods. 2017 Jun;14(6):587-589 [PMID: 28481363]
  130. Evol Dev. 2004 Sep-Oct;6(5):303-9 [PMID: 15330863]
  131. G3 (Bethesda). 2021 Mar 16;11(3): [PMID: 33729500]
  132. Nat Protoc. 2013 Aug;8(8):1494-512 [PMID: 23845962]
  133. J Biol Chem. 2003 Nov 7;278(45):44600-7 [PMID: 12941941]
  134. Proc Natl Acad Sci U S A. 2010 May 25;107(21):9747-52 [PMID: 20457924]
  135. Nat Neurosci. 2007 Sep;10(9):1160-7 [PMID: 17694052]
  136. Biomolecules. 2020 Jul 01;10(7): [PMID: 32630239]
  137. J Neurosci. 2013 Nov 6;33(45):17577-86 [PMID: 24198348]
  138. Sci Rep. 2024 Jun 21;14(1):14332 [PMID: 38906973]
  139. Curr Biol. 2010 Jun 22;20(12):1133-7 [PMID: 20605458]
  140. Cell Death Dis. 2023 Dec 8;14(12):805 [PMID: 38062036]
  141. Science. 2013 Apr 12;340(6129):157-61 [PMID: 23580521]
  142. PeerJ. 2019 Feb 1;7:e6374 [PMID: 30723633]
  143. Science. 2013 Apr 5;340(6128):91-5 [PMID: 23559253]
  144. Elife. 2017 Jul 25;6: [PMID: 28742021]
  145. Bioinformatics. 2014 Jun 15;30(12):1660-6 [PMID: 24532719]
  146. PLoS One. 2012;7(10):e47518 [PMID: 23082175]
  147. BMC Bioinformatics. 2009 Dec 15;10:421 [PMID: 20003500]
  148. Sci Rep. 2017 Sep 15;7(1):11730 [PMID: 28916758]
  149. Curr Biol. 2015 Nov 2;25(21):2795-2803 [PMID: 26592340]
  150. Nat Metab. 2023 Nov;5(11):2002-2019 [PMID: 37932430]

MeSH Term

Animals
Periplaneta
Transcriptome
Ganglia, Invertebrate
Female
Male
Gene Expression Profiling

Word Cloud

Created with Highcharts 10.0.0gangliacockroachmodelgenetictranscriptomeenzymesAmericanPeriplanetaamericanaBlattidaeusekeysystemfoundationfunctionalcephalicexpressionprofileskGNGsignalingpathwayadultCNSroleLBlattodeaorganismbiochemicalphysiologicalstudyalmostcenturyhoweverbenefittoolsfoundspeciesDrosophilamelanogasterfacilitateneuroscienceservetranslationalexperimentationassembledannotateddifferentialassessedassemblyyielded>400transcripts>40putativecodingsequencesGeneontologyproteindomainsearchesindicatecerebralgnathaldistinctdevelopmentalTollappearsactivecentralnervousmaysuggestseparatebesidesinnateimmuneactivationembryonicdevelopmentcatabolicglycolyticcitricacidcyclewellrepresentedhighlyexpressedexpressgluconeogenictrehaloneogenicsuggestinglargerregulatinghemolymphsugarhomeostasispreviouslyappreciatedannotationquantificationrevealcanonicalnovelpathwaysmetabolisminsectlayfutureanalysisCephalictranscriptomicsBlattodea:neurometabolismneurotranscriptomicssignaltransduction

Similar Articles

Cited By