#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

A partial genome assembly of the miniature parasitoid wasp, Megaphragma amalphitanum


Autoři: Fedor S. Sharko aff001;  Artem V. Nedoluzhko aff002;  Brandon M. Lê aff004;  Svetlana V. Tsygankova aff002;  Eugenia S. Boulygina aff002;  Sergey M. Rastorguev aff002;  Alexey S. Sokolov aff001;  Fernando Rodriguez aff004;  Alexander M. Mazur aff001;  Alexey A. Polilov aff005;  Richard Benton aff006;  Michael B. Evgen'ev aff007;  Irina R. Arkhipova aff004;  Egor B. Prokhortchouk aff001;  Konstantin G. Skryabin aff001
Působiště autorů: Institute of Bioengineering, Research Center of Biotechnology of the Russian Academy of Sciences, Moscow, Russia aff001;  National Research Center “Kurchatov Institute”, Moscow, Russia aff002;  Nord University, Faculty of Biosciences and Aquaculture, Bodø, Norway aff003;  Josephine Bay Paul Center for Comparative Molecular Biology and Evolution, Marine Biological Laboratory, Woods Hole, Massachusetts, United States of America aff004;  Lomonosov Moscow State University, Faculty of Biology, Moscow, Russia aff005;  Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, Lausanne, Switzerland aff006;  Institute of Molecular Biology RAS, Moscow, Russia aff007
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0226485

Souhrn

Body size reduction, also known as miniaturization, is an important evolutionary process that affects a number of physiological and phenotypic traits and helps animals conquer new ecological niches. However, this process is poorly understood at the molecular level. Here, we report genomic and transcriptomic features of arguably the smallest known insect–the parasitoid wasp, Megaphragma amalphitanum (Hymenoptera: Trichogrammatidae). In contrast to expectations, we find that the genome and transcriptome sizes of this parasitoid wasp are comparable to other members of the Chalcidoidea superfamily. Moreover, compared to other chalcid wasps the gene content of M. amalphitanum is remarkably conserved. Intriguingly, we observed significant changes in M. amalphitanum transposable element dynamics over time, in which an initial burst was followed by suppression of activity, possibly due to a recent reinforcement of the genome defense machinery. Overall, while the M. amalphitanum genomic data reveal certain features that may be linked to the unusual biological properties of this organism, miniaturization is not associated with a large decrease in genome complexity.

Klíčová slova:

Genome analysis – Comparative genomics – Insects – Genomic libraries – Genomic library construction – Transcriptome analysis – Genomics statistics – Invertebrate genomics


Zdroje

1. Hanken J, Wake DB. Miniaturization of Body-Size—Organismal Consequences and Evolutionary Significance. Annu Rev Ecol Syst. 1993;24:501–19. doi: 10.1146/annurev.es.24.110193.002441 ISI:A1993MJ37100018.

2. Polilov AA. Small is beautiful: features of the smallest insects and limits to miniaturization. Annu Rev Entomol. 2015;60:103–21. Epub 2014/10/24. doi: 10.1146/annurev-ento-010814-020924 25341106.

3. Bernardo U, Viggiani G. Biological data on Megaphragma amalphitanum Viggiani and Megaphragma mymaripenne Timberlake (Hymenoptera: Trichogrammatidae), egg-parasitoid of H. haemorrhoidalis Bouché) (Thysanoptera: Thripidae) in southern Italy. Bollettino del Laboratorio di Entomologia Agraria Filippo Silvestri. 2002;58:77–85.

4. Pintureau B, Lassabliere F, Khatchadourian C, Daumal J. Eggs parasitoids and symbionts of two European Thrips. Annales de la Société Entomologique de France. 1999;35:416–20. ISI:000085892500074.

5. Polilov AA. Anatomy of adult Megaphragma (Hymenoptera: Trichogrammatidae), one of the smallest insects, and new insight into insect miniaturization. PLoS One. 2017;12(5):e0175566. Epub 2017/05/04. doi: 10.1371/journal.pone.0175566 28467417

6. Branstetter MG, Danforth BN, Pitts JP, Faircloth BC, Ward PS, Buffington ML, et al. Phylogenomic Insights into the Evolution of Stinging Wasps and the Origins of Ants and Bees. Current Biology. 2017;27(7):1019–25. doi: 10.1016/j.cub.2017.03.027 ISI:000398061700023. 28376325

7. Nedoluzhko AV, Sharko FS, Boulygina ES, Tsygankova SV, Sokolov AS, Mazur AM, et al. Mitochondrial genome of Megaphragma amalphitanum (Hymenoptera: Trichogrammatidae). Mitochondrial DNA A DNA Mapp Seq Anal. 2016;27(6):4526–7. Epub 2015/12/01. doi: 10.3109/19401736.2015.1101546 26617282.

8. Owen AK, George J, Pinto JD, Heraty JM. A molecular phylogeny of the Trichogrammatidae (Hymenoptera: Chalcidoidea), with an evaluation of the utility of their male genitalia for higher level classification. Syst Entomol. 2007;32(2):227–51. doi: 10.1111/j.1365-3113.2006.00361.x ISI:000245745800003.

9. Heraty JM, Burks RA, Cruaud A, Gibson GAP, Liljeblad J, Munro J, et al. A phylogenetic analysis of the megadiverse Chalcidoidea (Hymenoptera). Cladistics. 2013;29(5):466–542. doi: 10.1111/cla.12006 ISI:000324622500003.

10. Peters RS, Niehuis O, Gunkel S, Blaser M, Mayer C, Podsiadlowski L, et al. Transcriptome sequence-based phylogeny of chalcidoid wasps (Hymenoptera: Chalcidoidea) reveals a history of rapid radiations, convergence, and evolutionary success. Mol Phylogenet Evol. 2018;120:286–96. Epub 2017/12/17. doi: 10.1016/j.ympev.2017.12.005 29247847

11. Schulz HN, Brinkhoff T, Ferdelman TG, Marine MH, Teske A, Jorgensen BB. Dense populations of a giant sulfur bacterium in Namibian shelf sediments. Science. 1999;284(5413):493–5. Epub 1999/04/16. doi: 10.1126/science.284.5413.493 10205058.

12. Standage DS, Berens AJ, Glastad KM, Severin AJ, Brendel VP, Toth AL. Genome, transcriptome and methylome sequencing of a primitively eusocial wasp reveal a greatly reduced DNA methylation system in a social insect. Mol Ecol. 2016;25(8):1769–84. Epub 2016/02/10. doi: 10.1111/mec.13578 26859767.

13. Makarova AA, Polilov AA. Peculiarities of the Brain Structure and Ultrastructure in Small Insects Related to Miniaturization. 1. The Smallest Coleoptera (Ptiliidae). Zool Zh. 2013;92(5):523–33. doi: 10.7868/S0044513413050073 ISI:000321472300003.

14. Polilov AA. The smallest insects evolve anucleate neurons. Arthropod Struct Dev. 2012;41(1):29–34. Epub 2011/11/15. doi: 10.1016/j.asd.2011.09.001 22078364.

15. Gregory TR. Synergy between sequence and size in large-scale genomics. Nat Rev Genet. 2005;6(9):699–708. Epub 2005/09/10. nrg1674 [pii] doi: 10.1038/nrg1674 16151375.

16. Gregory TR, Hebert PDN, Kolasa J. Evolutionary implications of the relationship between genome size and body size in flatworms and copepods. Heredity. 2000;84(2):201–8. doi: 10.1046/j.1365-2540.2000.00661.x ISI:000086196500009. 10762390

17. Erives AJ. Genes conserved in bilaterians but jointly lost with Myc during nematode evolution are enriched in cell proliferation and cell migration functions. Dev Genes Evol. 2015;225(5):259–73. Epub 2015/07/16. doi: 10.1007/s00427-015-0508-1 26173873; PubMed Central PMCID: PMC4568025.

18. Akif'ev AP, Grishanin AK, Degtiarev SV. [Chromatin diminution is a key process explaining the eukaryotic genome size paradox and some mechanisms of genetic isolation]. Genetika. 2002;38(5):595–606. Epub 2002/06/19. 12068542.

19. Wang J, Mitreva M, Berriman M, Thorne A, Magrini V, Koutsovoulos G, et al. Silencing of germline-expressed genes by DNA elimination in somatic cells. Dev Cell. 2012;23(5):1072–80. Epub 2012/11/06. doi: 10.1016/j.devcel.2012.09.020 23123092

20. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19(5):455–77. Epub 2012/04/18. doi: 10.1089/cmb.2012.0021 PubMed Central PMCID: PMC3342519. 22506599

21. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology. 2011;29(7):644–U130. doi: 10.1038/nbt.1883 ISI:000292595200023. 21572440

22. Bryant DM, Johnson K, DiTommaso T, Tickle T, Couger MB, Payzin-Dogru D, et al. A Tissue-Mapped Axolotl De Novo Transcriptome Enables Identification of Limb Regeneration Factors. Cell Rep. 2017;18(3):762–76. Epub 2017/01/19. doi: 10.1016/j.celrep.2016.12.063 28099853; PubMed Central PMCID: PMC5419050.

23. Flutre T, Duprat E, Feuillet C, Quesneville H. Considering transposable element diversification in de novo annotation approaches. PLoS One. 2011;6(1):e16526. Epub 2011/02/10. doi: 10.1371/journal.pone.0016526 21304975; PubMed Central PMCID: PMC3031573.

24. The i5K Initiative: advancing arthropod genomics for knowledge, human health, agriculture, and the environment. J Hered. 2013;104(5):595–600. Epub 2013/08/14. doi: 10.1093/jhered/est050 23940263; PubMed Central PMCID: PMC4046820.

25. Werren JH, Richards S, Desjardins CA, Niehuis O, Gadau J, Colbourne JK, et al. Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science. 2010;327(5963):343–8. Epub 2010/01/16. doi: 10.1126/science.1178028 20075255

26. Simao FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015;31(19):3210–2. Epub 2015/06/11. doi: 10.1093/bioinformatics/btv351 26059717.

27. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9(4):357–9. Epub 2012/03/06. doi: 10.1038/nmeth.1923 22388286; PubMed Central PMCID: PMC3322381.

28. Li L, Stoeckert CJ Jr., Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 2003;13(9):2178–89. Epub 2003/09/04. doi: 10.1101/gr.1224503 12952885; PubMed Central PMCID: PMC403725.

29. Lindsey ARI, Kelkar YD, Wu X, Sun D, Martinson EO, Yan Z, et al. Comparative genomics of the miniature wasp and pest control agent Trichogramma pretiosum. BMC Biol. 2018;16(1):54. Epub 2018/05/20. doi: 10.1186/s12915-018-0520-9 29776407; PubMed Central PMCID: PMC5960102.

30. Eisman RC, Kaufman TC. Probing the boundaries of orthology: the unanticipated rapid evolution of Drosophila centrosomin. Genetics. 2013;194(4):903–26. Epub 2013/06/12. doi: 10.1534/genetics.113.152546 23749319; PubMed Central PMCID: PMC3730919.

31. Feng Z, Caballe A, Wainman A, Johnson S, Haensele AFM, Cottee MA, et al. Structural Basis for Mitotic Centrosome Assembly in Flies. Cell. 2017;169(6):1078–89 e13. Epub 2017/06/03. doi: 10.1016/j.cell.2017.05.030 28575671

32. Yalgin C, Ebrahimi S, Delandre C, Yoong LF, Akimoto S, Tran H, et al. Centrosomin represses dendrite branching by orienting microtubule nucleation. Nat Neurosci. 2015;18(10):1437–45. Epub 2015/09/01. doi: 10.1038/nn.4099 26322925.

33. Basto R, Lau J, Vinogradova T, Gardiol A, Woods CG, Khodjakov A, et al. Flies without centrioles. Cell. 2006;125(7):1375–86. doi: 10.1016/j.cell.2006.05.025 ISI:000239104500019. 16814722

34. Zheng Z, Gao T, Hou Y, Zhou M. Involvement of the anucleate primary sterigmata protein FgApsB in vegetative differentiation, asexual development, nuclear migration, and virulence in Fusarium graminearum. FEMS Microbiol Lett. 2013;349(2):88–98. Epub 2013/10/15. doi: 10.1111/1574-6968.12297 24117691.

35. Veith D, Scherr N, Efimov VP, Fischer R. Role of the spindle-pole-body protein ApsB and the cortex protein ApsA in microtubule organization and nuclear migration in Aspergillus nidulans. J Cell Sci. 2005;118(Pt 16):3705–16. Epub 2005/08/18. doi: 10.1242/jcs.02501 16105883

36. Suelmann R, Sievers N, Galetzka D, Robertson L, Timberlake WE, Fischer R. Increased nuclear traffic chaos in hyphae of Aspergillus nidulans: molecular characterization of apsB and in vivo observation of nuclear behaviour. Mol Microbiol. 1998;30(4):831–42. Epub 1999/03/27. doi: 10.1046/j.1365-2958.1998.01115.x 10094631.

37. Benton R, Vannice KS, Gomez-Diaz C, Vosshall LB. Variant Ionotropic Glutamate Receptors as Chemosensory Receptors in Drosophila. Cell. 2009;136(1):149–62. doi: 10.1016/j.cell.2008.12.001 ISI:000262318400022. 19135896

38. Rytz R, Croset V, Benton R. Ionotropic Receptors (IRs): Chemosensory ionotropic glutamate receptors in Drosophila and beyond. Insect Biochem Molec. 2013;43(9):888–97. doi: 10.1016/j.ibmb.2013.02.007 ISI:000323801100011. 23459169

39. Knecht ZA, Silbering AF, Cruz J, Yang L, Croset V, Benton R, et al. Ionotropic Receptor-dependent moist and dry cells control hygrosensation in Drosophila. Elife. 2017;6. Epub 2017/06/18. doi: 10.7554/eLife.26654e26654 [pii] 28621663; PubMed Central PMCID: PMC5495567.

40. Knecht ZA, Silbering AF, Ni L, Klein M, Budelli G, Bell R, et al. Distinct combinations of variant ionotropic glutamate receptors mediate thermosensation and hygrosensation in Drosophila. Elife. 2016;5. Epub 2016/09/24. doi: 10.7554/eLife.17879e17879 [pii] 27656904; PubMed Central PMCID: PMC5052030.

41. Ni L, Klein M, Svec KV, Budelli G, Chang EC, Ferrer AJ, et al. The Ionotropic Receptors IR21a and IR25a mediate cool sensing in Drosophila. Elife. 2016;5. Epub 2016/04/30. doi: 10.7554/eLife.13254 27126188

42. Benton R. Multigene Family Evolution: Perspectives from Insect Chemoreceptors. Trends Ecol Evol. 2015;30(10):590–600. Epub 2015/09/29. doi: 10.1016/j.tree.2015.07.009 26411616

43. Croset V, Rytz R, Cummins SF, Budd A, Brawand D, Kaessmann H, et al. Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLoS Genet. 2010;6(8):e1001064. Epub 2010/09/03. doi: 10.1371/journal.pgen.1001064 20808886

44. Larsson MC, Domingos AI, Jones WD, Chiappe ME, Amrein H, Vosshall LB. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron. 2004;43(5):703–14. Epub 2004/09/02. doi: 10.1016/j.neuron.2004.08.019 15339651

45. Joseph RM, Carlson JR. Drosophila Chemoreceptors: A Molecular Interface Between the Chemical World and the Brain. Trends in Genetics. 2015;31(12):683–95. doi: 10.1016/j.tig.2015.09.005 ISI:000366346000002. 26477743

46. Miyamoto T, Slone J, Song XY, Amrein H. A Fructose Receptor Functions as a Nutrient Sensor in the Drosophila Brain. Cell. 2012;151(5):1113–25. doi: 10.1016/j.cell.2012.10.024 ISI:000311423500022. 23178127

47. Fujii S, Yavuz A, Slone J, Jagge C, Song X, Amrein H. Drosophila sugar receptors in sweet taste perception, olfaction, and internal nutrient sensing. Curr Biol. 2015;25(5):621–7. Epub 2015/02/24. doi: 10.1016/j.cub.2014.12.058 25702577

48. Robertson HM, Gadau J, Wanner KW. The insect chemoreceptor superfamily of the parasitoid jewel wasp Nasonia vitripennis. Insect Mol Biol. 2010;19 Suppl 1:121–36. Epub 2010/02/20. doi: 10.1111/j.1365-2583.2009.00979.x IMB979 [pii] 20167023.

49. Ahmed T, Zhang T, Wang Z, He K, Bai S. Gene set of chemosensory receptors in the polyembryonic endoparasitoid Macrocentrus cingulum. Sci Rep. 2016;6:24078. Epub 2016/04/20. doi: 10.1038/srep24078 27090020

50. Sheng S, Liao CW, Zheng Y, Zhou Y, Xu Y, Song WM, et al. Candidate chemosensory genes identified in the endoparasitoid Meteorus pulchricornis (Hymenoptera: Braconidae) by antennal transcriptome analysis. Comp Biochem Physiol Part D Genomics Proteomics. 2017;22:20–31. Epub 2017/02/12. doi: 10.1016/j.cbd.2017.01.002 28187311

51. Moreau SJM, Asgari S. Venom Proteins from Parasitoid Wasps and Their Biological Functions. Toxins. 2015;7(7):2385–412. doi: 10.3390/toxins7072385 ISI:000359191200004. 26131769

52. de Graaf DC, Aerts M, Brunain M, Desjardins CA, Jacobs FJ, Werren JH, et al. Insights into the venom composition of the ectoparasitoid wasp Nasonia vitripennis from bioinformatic and proteomic studies. Insect Mol Biol. 2010;19 Suppl 1:11–26. Epub 2010/02/20. doi: 10.1111/j.1365-2583.2009.00914.x 20167014

53. Paulson AR, Le CH, Dickson JC, Ehlting J, von Aderkas P, Perlman SJ. Transcriptome analysis provides insight into venom evolution in a seed-parasitic wasp, Megastigmus spermotrophus. Insect Molecular Biology. 2016;25(5):604–16. doi: 10.1111/imb.12247 ISI:000383345000008. 27286234

54. Universal Chalcidoidea Database. World Wide Web electronic publication. [Internet]. 2019. Available from: http://www.nhm.ac.uk/chalcidoids.

55. Peters RS. Host Range and Offspring Quantities in Natural Populations of Nasonia vitripennis (Walker, 1836) (Hymenoptera: Chalcidoidea: Pteromalidae). J Hymenopt Res. 2010;19(1):128–38. WOS:000285775800012.

56. Kapheim KM, Pan H, Li C, Salzberg SL, Puiu D, Magoc T, et al. Social evolution. Genomic signatures of evolutionary transitions from solitary to group living. Science. 2015;348(6239):1139–43. Epub 2015/05/16. doi: 10.1126/science.aaa4788 25977371

57. Patalano S, Vlasova A, Wyatt C, Ewels P, Camara F, Ferreira PG, et al. Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies. Proc Natl Acad Sci U S A. 2015;112(45):13970–5. Epub 2015/10/21. doi: 10.1073/pnas.1515937112 26483466

58. Bast J, Schaefer I, Schwander T, Maraun M, Scheu S, Kraaijeveld K. No Accumulation of Transposable Elements in Asexual Arthropods. Mol Biol Evol. 2016;33(3):697–706. Epub 2015/11/13. doi: 10.1093/molbev/msv261 26560353; PubMed Central PMCID: PMC4760076.

59. Petersen M, Armisen D, Gibbs RA, Hering L, Khila A, Mayer G, et al. Diversity and evolution of the transposable element repertoire in arthropods with particular reference to insects. BMC Evol Biol. 2019;19(1):11. Epub 2019/01/11. doi: 10.1186/s12862-018-1324-9 30626321; PubMed Central PMCID: PMC6327564.

60. Kraaijeveld K, Bast J. Transposable element proliferation as a possible side effect of endosymbiont manipulations. Mob Genet Elements. 2012;2(5):253–6. Epub 2013/04/04. doi: 10.4161/mge.22878 23550173; PubMed Central PMCID: PMC3575435.

61. Kraaijeveld K, Zwanenburg B, Hubert B, Vieira C, De Pater S, Van Alphen JJ, et al. Transposon proliferation in an asexual parasitoid. Mol Ecol. 2012;21(16):3898–906. Epub 2012/05/03. doi: 10.1111/j.1365-294X.2012.5582.x 22548357.

62. Nedoluzhko AV, Sharko FS, Tsygankova SV, Boulygina ES, Sokolov AS, Rastorguev SM, et al. Metagenomic analysis of microbial community of a parasitoid wasp Megaphragma amalphitanum. Genom Data. 2017;11:87–8. Epub 2017/01/10. doi: 10.1016/j.gdata.2016.12.007 28066711; PubMed Central PMCID: PMC5200880.

63. Lindsey AR, Werren JH, Richards S, Stouthamer R. Comparative Genomics of a Parthenogenesis-Inducing Wolbachia Symbiont. G3 (Bethesda). 2016;6(7):2113–23. Epub 2016/05/20. doi: 10.1534/g3.116.028449 27194801

64. Obbard DJ, Gordon KH, Buck AH, Jiggins FM. The evolution of RNAi as a defence against viruses and transposable elements. Philos Trans R Soc Lond B Biol Sci. 2009;364(1513):99–115. Epub 2008/10/18. doi: 10.1098/rstb.2008.0168 18926973; PubMed Central PMCID: PMC2592633.

65. Schaack S, Gilbert C, Feschotte C. Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution. Trends Ecol Evol. 2010;25(9):537–46. Epub 2010/07/02. doi: 10.1016/j.tree.2010.06.001 20591532

66. Tsutsui ND, Suarez AV, Spagna JC, Johnston JS. The evolution of genome size in ants. BMC Evol Biol. 2008;8:64. Epub 2008/02/28. doi: 10.1186/1471-2148-8-64 18302783; PubMed Central PMCID: PMC2268675.

67. Carroll SB. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell. 2008;134(1):25–36. Epub 2008/07/11. doi: 10.1016/j.cell.2008.06.030 18614008


Článok vyšiel v časopise

PLOS One


2019 Číslo 12
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#