A near-chromosome level genome assembly of the European hoverfly, Sphaerophoria rueppellii (Diptera: Syrphidae), provides comparative insights into insecticide resistance-related gene family evolution.
Beneficial predator
Comparative genomics
Crop pests
Diptera
Hi-C
Hoverfly
Illumina
Insecticide resistance
PacBio
Sphaerophoria rueppellii
Syrphidae
Whole genome sequencing
Journal
BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258
Informations de publication
Date de publication:
12 Mar 2022
12 Mar 2022
Historique:
received:
04
11
2021
accepted:
11
02
2022
entrez:
13
3
2022
pubmed:
14
3
2022
medline:
16
3
2022
Statut:
epublish
Résumé
Sphaerophoria rueppellii, a European species of hoverfly, is a highly effective beneficial predator of hemipteran crop pests including aphids, thrips and coleopteran/lepidopteran larvae in integrated pest management (IPM) programmes. It is also a key pollinator of a wide variety of important agricultural crops. No genomic information is currently available for S. rueppellii. Without genomic information for such beneficial predator species, we are unable to perform comparative analyses of insecticide target-sites and genes encoding metabolic enzymes potentially responsible for insecticide resistance, between crop pests and their predators. These metabolic mechanisms include several gene families - cytochrome P450 monooxygenases (P450s), ATP binding cassette transporters (ABCs), glutathione-S-transferases (GSTs), UDP-glycosyltransferases (UGTs) and carboxyl/choline esterases (CCEs). In this study, a high-quality near-chromosome level de novo genome assembly (as well as a mitochondrial genome assembly) for S. rueppellii has been generated using a hybrid approach with PacBio long-read and Illumina short-read data, followed by super scaffolding using Hi-C data. The final assembly achieved a scaffold N50 of 87Mb, a total genome size of 537.6Mb and a level of completeness of 96% using a set of 1,658 core insect genes present as full-length genes. The assembly was annotated with 14,249 protein-coding genes. Comparative analysis revealed gene expansions of CYP6Zx P450s, epsilon-class GSTs, dietary CCEs and multiple UGT families (UGT37/302/308/430/431). Conversely, ABCs, delta-class GSTs and non-CYP6Zx P450s showed limited expansion. Differences were seen in the distributions of resistance-associated gene families across subfamilies between S. rueppellii and some hemipteran crop pests. Additionally, S. rueppellii had larger numbers of detoxification genes than other pollinator species. This assembly is the first published genome for a predatory member of the Syrphidae family and will serve as a useful resource for further research into selectivity and potential tolerance of insecticides by beneficial predators. Furthermore, the expansion of some gene families often linked to insecticide resistance and selectivity may be an indicator of the capacity of this predator to detoxify IPM selective insecticides. These findings could be exploited by targeted insecticide screens and functional studies to increase effectiveness of IPM strategies, which aim to increase crop yields by sustainably and effectively controlling pests without impacting beneficial predator populations.
Sections du résumé
BACKGROUND
BACKGROUND
Sphaerophoria rueppellii, a European species of hoverfly, is a highly effective beneficial predator of hemipteran crop pests including aphids, thrips and coleopteran/lepidopteran larvae in integrated pest management (IPM) programmes. It is also a key pollinator of a wide variety of important agricultural crops. No genomic information is currently available for S. rueppellii. Without genomic information for such beneficial predator species, we are unable to perform comparative analyses of insecticide target-sites and genes encoding metabolic enzymes potentially responsible for insecticide resistance, between crop pests and their predators. These metabolic mechanisms include several gene families - cytochrome P450 monooxygenases (P450s), ATP binding cassette transporters (ABCs), glutathione-S-transferases (GSTs), UDP-glycosyltransferases (UGTs) and carboxyl/choline esterases (CCEs).
METHODS AND FINDINGS
RESULTS
In this study, a high-quality near-chromosome level de novo genome assembly (as well as a mitochondrial genome assembly) for S. rueppellii has been generated using a hybrid approach with PacBio long-read and Illumina short-read data, followed by super scaffolding using Hi-C data. The final assembly achieved a scaffold N50 of 87Mb, a total genome size of 537.6Mb and a level of completeness of 96% using a set of 1,658 core insect genes present as full-length genes. The assembly was annotated with 14,249 protein-coding genes. Comparative analysis revealed gene expansions of CYP6Zx P450s, epsilon-class GSTs, dietary CCEs and multiple UGT families (UGT37/302/308/430/431). Conversely, ABCs, delta-class GSTs and non-CYP6Zx P450s showed limited expansion. Differences were seen in the distributions of resistance-associated gene families across subfamilies between S. rueppellii and some hemipteran crop pests. Additionally, S. rueppellii had larger numbers of detoxification genes than other pollinator species.
CONCLUSION AND SIGNIFICANCE
CONCLUSIONS
This assembly is the first published genome for a predatory member of the Syrphidae family and will serve as a useful resource for further research into selectivity and potential tolerance of insecticides by beneficial predators. Furthermore, the expansion of some gene families often linked to insecticide resistance and selectivity may be an indicator of the capacity of this predator to detoxify IPM selective insecticides. These findings could be exploited by targeted insecticide screens and functional studies to increase effectiveness of IPM strategies, which aim to increase crop yields by sustainably and effectively controlling pests without impacting beneficial predator populations.
Identifiants
pubmed: 35279098
doi: 10.1186/s12864-022-08436-5
pii: 10.1186/s12864-022-08436-5
pmc: PMC8917705
doi:
Substances chimiques
Insecticides
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
198Informations de copyright
© 2022. The Author(s).
Références
Genetics. 2007 Nov;177(3):1363-75
pubmed: 18039872
Int J Mol Sci. 2019 Jul 25;20(15):
pubmed: 31349586
PLoS One. 2011;6(12):e29418
pubmed: 22242119
Curr Opin Insect Sci. 2018 Jun;27:97-102
pubmed: 30025642
Mol Biol Evol. 2018 Jun 1;35(6):1547-1549
pubmed: 29722887
Philos Trans R Soc Lond B Biol Sci. 1998 Oct 29;353(1376):1707-11
pubmed: 10021771
Insect Mol Biol. 2010 Mar;19 Suppl 2:155-64
pubmed: 20482647
BMC Evol Biol. 2019 Jan 9;19(1):11
pubmed: 30626321
Mol Ecol Resour. 2020 Jul;20(4):1110-1125
pubmed: 32421889
Nucleic Acids Res. 2016 Jul 8;44(W1):W160-5
pubmed: 27079975
Front Genet. 2020 Nov 19;11:592595
pubmed: 33329739
Int J Mol Sci. 2019 Oct 09;20(20):
pubmed: 31600879
BMC Biol. 2016 Dec 14;14(1):110
pubmed: 27974049
Nucleic Acids Res. 2002 Jul 15;30(14):3059-66
pubmed: 12136088
BMC Genomics. 2017 Apr 26;18(1):330
pubmed: 28446145
Hum Genomics. 2009 Oct;4(1):59-65
pubmed: 19951895
BMC Genomics. 2012 Nov 10;13:609
pubmed: 23140097
Mol Biol Evol. 2013 Apr;30(4):772-80
pubmed: 23329690
Science. 2017 Apr 7;356(6333):92-95
pubmed: 28336562
Sci Rep. 2018 Dec 14;8(1):17847
pubmed: 30552348
Nat Biotechnol. 2011 May 15;29(7):644-52
pubmed: 21572440
Chromosome Res. 2011 Aug;19(6):809-23
pubmed: 21877225
Cell Syst. 2016 Jul;3(1):95-8
pubmed: 27467249
Wellcome Open Res. 2021 Oct 29;6:292
pubmed: 36873714
Comp Biochem Physiol B Biochem Mol Biol. 2009 Dec;154(4):427-34
pubmed: 19737624
Mol Phylogenet Evol. 2013 Nov;69(2):313-9
pubmed: 22982435
Bioinformatics. 2013 Oct 1;29(19):2487-9
pubmed: 23842809
BMC Bioinformatics. 2011 Dec 22;12:491
pubmed: 22192575
Mol Phylogenet Evol. 2011 Dec;61(3):924-32
pubmed: 21930223
BMC Genomics. 2011 Oct 07;12:491
pubmed: 21981826
BMC Genomics. 2003 Aug 13;4(1):35
pubmed: 12914673
PLoS One. 2012;7(5):e36544
pubmed: 22574182
Bioinformatics. 2014 Aug 1;30(15):2114-20
pubmed: 24695404
Pestic Biochem Physiol. 2019 Feb;154:23-31
pubmed: 30765053
Bioinformatics. 2014 May 1;30(9):1312-3
pubmed: 24451623
Malar J. 2019 Mar 7;18(1):62
pubmed: 30845961
Nucleic Acids Res. 2008 Jun;36(10):3420-35
pubmed: 18445632
Insect Biochem Mol Biol. 2007 Oct;37(10):1026-35
pubmed: 17785190
Annu Rev Entomol. 1999;44:507-33
pubmed: 9990722
J Insect Physiol. 2014 Dec;71:177-90
pubmed: 25450567
Nucleic Acids Res. 2016 Nov 2;44(19):e147
pubmed: 27458204
Pest Manag Sci. 2018 Mar;74(3):695-704
pubmed: 29027758
Mol Biol Evol. 2008 Jul;25(7):1307-20
pubmed: 18367465
Oecologia. 2008 Jul;156(4):819-23
pubmed: 18438687
Nat Rev Genet. 2003 Nov;4(11):889-99
pubmed: 14634636
Nature. 2008 Apr 24;452(7190):949-55
pubmed: 18362917
Curr Opin Insect Sci. 2015 Aug;10:51-58
pubmed: 29588014
Nucleic Acids Res. 2005 Nov 28;33(20):6494-506
pubmed: 16314312
Curr Opin Insect Sci. 2019 Feb;31:131-138
pubmed: 31109666
Proc Biol Sci. 2020 May 27;287(1927):20200508
pubmed: 32429807
PLoS Genet. 2010 Jun 24;6(6):e1000999
pubmed: 20585623
Genome Biol Evol. 2020 Feb 1;12(2):3857-3872
pubmed: 31971586
Biochem Soc Trans. 2006 Dec;34(Pt 6):1252-5
pubmed: 17073796
Bioinformatics. 2015 Oct 1;31(19):3210-2
pubmed: 26059717
Pestic Biochem Physiol. 2016 Sep;132:118-24
pubmed: 27521922
Gigascience. 2021 Feb 16;10(2):
pubmed: 33590861
Nat Biotechnol. 2019 May;37(5):540-546
pubmed: 30936562
BMC Bioinformatics. 2018 Nov 29;19(1):460
pubmed: 30497373
Nat Biotechnol. 2015 Mar;33(3):290-5
pubmed: 25690850
Curr Biol. 2018 Apr 2;28(7):1137-1143.e5
pubmed: 29576476
Pest Manag Sci. 2010 Nov;66(11):1171-80
pubmed: 20672339
Pest Manag Sci. 2020 Jun;76(6):1973-1979
pubmed: 32115861
Front Physiol. 2018 Apr 03;9:322
pubmed: 29670540
BMC Genomics. 2019 Dec 19;20(1):996
pubmed: 31856729
Int J Mol Sci. 2019 Mar 01;20(5):
pubmed: 30823656
Int J Mol Sci. 2020 Nov 11;21(22):
pubmed: 33187355
Science. 2010 Jan 15;327(5963):343-8
pubmed: 20075255
Genome Biol. 2014;15(10):466
pubmed: 25315136
Genome Res. 2017 May;27(5):722-736
pubmed: 28298431
Proc Natl Acad Sci U S A. 2011 Apr 5;108(14):5690-5
pubmed: 21402926
Proc Natl Acad Sci U S A. 2021 Feb 9;118(6):
pubmed: 33547243
Mol Ecol Resour. 2020 Jul;20(4):995-1006
pubmed: 32220045
Pestic Biochem Physiol. 2020 Jul;167:104558
pubmed: 32527432
Nucleic Acids Res. 2014 Jan;42(Database issue):D222-30
pubmed: 24288371
Insect Biochem Mol Biol. 2014 Feb;45:89-110
pubmed: 24291285
Cell Syst. 2016 Jul;3(1):99-101
pubmed: 27467250
Comp Biochem Physiol Part D Genomics Proteomics. 2018 Mar;25:1-8
pubmed: 29121518
Insect Biochem Mol Biol. 1999 Sep;29(9):757-77
pubmed: 10510498
Nat Commun. 2020 Mar 18;11(1):1432
pubmed: 32188846
Genome Biol. 2019 Nov 14;20(1):238
pubmed: 31727128
Int J Mol Sci. 2019 Mar 20;20(6):
pubmed: 30897799
Biochem J. 2001 Jul 1;357(Pt 1):65-72
pubmed: 11415437
Insect Mol Biol. 2006 Oct;15(5):687-701
pubmed: 17069640
G3 (Bethesda). 2020 Sep 2;10(9):3047-3060
pubmed: 32601059
Insect Mol Biol. 2000 Dec;9(6):655-60
pubmed: 11122475
Nat Methods. 2020 Feb;17(2):155-158
pubmed: 31819265
Science. 2012 Sep 28;337(6102):1612-4
pubmed: 23019637
BMC Genomics. 2015 Nov 14;16:939
pubmed: 26573457
BMC Biol. 2020 Oct 19;18(1):142
pubmed: 33070780
Nat Biotechnol. 2011 Jan;29(1):24-6
pubmed: 21221095
Nat Plants. 2017 Mar 01;3:17008
pubmed: 28248316
J Med Entomol. 2013 Mar;50(2):352-61
pubmed: 23540124
Sci Rep. 2016 Aug 30;6:31900
pubmed: 27573208
Insect Biochem Mol Biol. 2008 Jun;38(6):634-44
pubmed: 18510975
Insect Biochem Mol Biol. 1999 Dec;29(12):1065-73
pubmed: 10612041
BMC Genomics. 2013 Dec 12;14:874
pubmed: 24330608
Proc Natl Acad Sci U S A. 2019 Aug 20;116(34):16817-16822
pubmed: 31383752
Annu Rev Entomol. 2000;45:371-91
pubmed: 10761582
PLoS One. 2014 Nov 19;9(11):e112963
pubmed: 25409509
BMC Genomics. 2020 Jul 6;21(1):463
pubmed: 32631258
Nat Methods. 2015 Apr;12(4):357-60
pubmed: 25751142
Bioinformatics. 2011 Mar 15;27(6):764-70
pubmed: 21217122
Insect Mol Biol. 2001 Apr;10(2):139-46
pubmed: 11422509
Genome Biol. 2008 Jan 11;9(1):R7
pubmed: 18190707
BMC Genomics. 2014 Nov 25;15:1018
pubmed: 25421852
Genome Biol Evol. 2016 Jun 27;8(6):1762-75
pubmed: 26951779
Curr Biol. 2019 Jul 8;29(13):2167-2173.e5
pubmed: 31204159
Biochem J. 1995 Jan 15;305 ( Pt 2):651-8
pubmed: 7530448
Annu Rev Entomol. 2020 Jan 7;65:391-407
pubmed: 31610136
Mitochondrial DNA B Resour. 2021 Feb 11;6(2):519-521
pubmed: 33628911
Toxicol Lett. 2002 Mar 10;128(1-3):215-28
pubmed: 11869832
BMC Genomics. 2022 Jan 11;23(1):45
pubmed: 35012450
Int J Mol Sci. 2015 Jan 19;16(1):2078-98
pubmed: 25607733
Pest Manag Sci. 2011 Aug;67(8):886-90
pubmed: 21538802
Parasit Vectors. 2018 Apr 4;11(1):225
pubmed: 29618373
Nucleic Acids Res. 2004 Jul 1;32(Web Server issue):W309-12
pubmed: 15215400
Nat Commun. 2019 Apr 12;10(1):1702
pubmed: 30979905
Z Naturforsch C J Biosci. 2013 Nov-Dec;68(11-12):509-21
pubmed: 24601089
Insect Biochem Mol Biol. 2011 Mar;41(3):203-9
pubmed: 21195177
Bioinformation. 2014 Nov 27;10(11):679-83
pubmed: 25512683
Curr Opin Insect Sci. 2018 Apr;26:25-33
pubmed: 29764657
Insect Biochem Mol Biol. 2020 Dec;127:103490
pubmed: 33169702
Bioinformatics. 2013 Nov 15;29(22):2933-5
pubmed: 24008419
Nat Commun. 2018 Sep 21;9(1):3843
pubmed: 30242156
Insect Mol Biol. 2006 Oct;15(5):615-36
pubmed: 17069637
Proc Natl Acad Sci U S A. 2016 Dec 27;113(52):E8396-E8405
pubmed: 27956617
PLoS One. 2012;7(2):e31051
pubmed: 22319603
BMC Genomics. 2009 Apr 29;10:202
pubmed: 19402892
Front Physiol. 2021 Mar 17;12:648481
pubmed: 33815151
Annu Rev Entomol. 2004;49:219-42
pubmed: 14651463