Genomic innovations, transcriptional plasticity and gene loss underlying the evolution and divergence of two highly polyphagous and invasive Helicoverpa pest species

S L Pearce; D F Clarke; P D East; S Elfekih; K H J Gordon; L S Jermiin; A McGaughran; J G Oakeshott; A Papanikolaou; O P Perera; R V Rane; S Richards; W T Tay; T K Walsh; A Anderson; C J Anderson; S Asgari; P G Board; A Bretschneider; P M Campbell; T Chertemps; J T Christeller; C W Coppin; S J Downes; G Duan; C A Farnsworth; R T Good; L B Han; Y C Han; K Hatje; I Horne; Y P Huang; D S T Hughes; E Jacquin-Joly; W James; S Jhangiani; M Kollmar; S S Kuwar; S Li; N-Y Liu; M T Maibeche; J R Miller; N Montagne; T Perry; J Qu; S V Song; G G Sutton; H Vogel; B P Walenz; W Xu; H-J Zhang; Z Zou; P Batterham; O R Edwards; Rene Feyereisen; R A Gibbs; D G Heckel; A McGrath; C Robin; S E Scherer; K C Worley; Y D Wu

doi:10.1186/s12915-017-0402-6

Genomic innovations, transcriptional plasticity and gene loss underlying the evolution and divergence of two highly polyphagous and invasive Helicoverpa pest species

S L Pearce, D F Clarke, P D East, S Elfekih, K H J Gordon, L S Jermiin, A McGaughran, J G Oakeshott, A Papanikolaou, O P Perera, R V Rane, S Richards, W T Tay, T K Walsh, A Anderson, C J Anderson, S Asgari, P G Board, A Bretschneider, P M CampbellT Chertemps, J T Christeller, C W Coppin, S J Downes, G Duan, C A Farnsworth, R T Good, L B Han, Y C Han, K Hatje, I Horne, Y P Huang, D S T Hughes, E Jacquin-Joly, W James, S Jhangiani, M Kollmar, S S Kuwar, S Li, N-Y Liu, M T Maibeche, J R Miller, N Montagne, T Perry, J Qu, S V Song, G G Sutton, H Vogel, B P Walenz, W Xu, H-J Zhang, Z Zou, P Batterham, O R Edwards, Rene Feyereisen, R A Gibbs, D G Heckel, A McGrath, C Robin, S E Scherer, K C Worley, Y D Wu

Plantebiokemi

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Abstract

BACKGROUND: Helicoverpa armigera and Helicoverpa zea are major caterpillar pests of Old and New World agriculture, respectively. Both, particularly H. armigera, are extremely polyphagous, and H. armigera has developed resistance to many insecticides. Here we use comparative genomics, transcriptomics and resequencing to elucidate the genetic basis for their properties as pests.

RESULTS: We find that, prior to their divergence about 1.5 Mya, the H. armigera/H. zea lineage had accumulated up to more than 100 more members of specific detoxification and digestion gene families and more than 100 extra gustatory receptor genes, compared to other lepidopterans with narrower host ranges. The two genomes remain very similar in gene content and order, but H. armigera is more polymorphic overall, and H. zea has lost several detoxification genes, as well as about 50 gustatory receptor genes. It also lacks certain genes and alleles conferring insecticide resistance found in H. armigera. Non-synonymous sites in the expanded gene families above are rapidly diverging, both between paralogues and between orthologues in the two species. Whole genome transcriptomic analyses of H. armigera larvae show widely divergent responses to different host plants, including responses among many of the duplicated detoxification and digestion genes.

CONCLUSIONS: The extreme polyphagy of the two heliothines is associated with extensive amplification and neofunctionalisation of genes involved in host finding and use, coupled with versatile transcriptional responses on different hosts. H. armigera's invasion of the Americas in recent years means that hybridisation could generate populations that are both locally adapted and insecticide resistant.

Originalsprog	Engelsk
Artikelnummer	63
Tidsskrift	BMC Biology
Vol/bind	15
Udgave nummer	1
Antal sider	30
ISSN	1741-7007
DOI	https://doi.org/10.1186/s12915-017-0402-6
Status	Udgivet - 31 jul. 2017

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10.1186/s12915-017-0402-6

Genomic innovations, transcriptional plasticity and gene loss underlying the evolution and divergence of two highly polyphagous and invasive Helicoverpa pest speciesForlagets udgivne version, 2,31 MB

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Pearce, S. L., Clarke, D. F., East, P. D., Elfekih, S., Gordon, K. H. J., Jermiin, L. S., McGaughran, A., Oakeshott, J. G., Papanikolaou, A., Perera, O. P., Rane, R. V., Richards, S., Tay, W. T., Walsh, T. K., Anderson, A., Anderson, C. J., Asgari, S., Board, P. G., Bretschneider, A., ... Wu, Y. D. (2017). Genomic innovations, transcriptional plasticity and gene loss underlying the evolution and divergence of two highly polyphagous and invasive Helicoverpa pest species. BMC Biology, 15(1), [63]. https://doi.org/10.1186/s12915-017-0402-6

Pearce, SL, Clarke, DF, East, PD, Elfekih, S, Gordon, KHJ, Jermiin, LS, McGaughran, A, Oakeshott, JG, Papanikolaou, A, Perera, OP, Rane, RV, Richards, S, Tay, WT, Walsh, TK, Anderson, A, Anderson, CJ, Asgari, S, Board, PG, Bretschneider, A, Campbell, PM, Chertemps, T, Christeller, JT, Coppin, CW, Downes, SJ, Duan, G, Farnsworth, CA, Good, RT, Han, LB, Han, YC, Hatje, K, Horne, I, Huang, YP, Hughes, DST, Jacquin-Joly, E, James, W, Jhangiani, S, Kollmar, M, Kuwar, SS, Li, S, Liu, N-Y, Maibeche, MT, Miller, JR, Montagne, N, Perry, T, Qu, J, Song, SV, Sutton, GG, Vogel, H, Walenz, BP, Xu, W, Zhang, H-J, Zou, Z, Batterham, P, Edwards, OR, Feyereisen, R, Gibbs, RA, Heckel, DG, McGrath, A, Robin, C, Scherer, SE, Worley, KC & Wu, YD 2017, 'Genomic innovations, transcriptional plasticity and gene loss underlying the evolution and divergence of two highly polyphagous and invasive Helicoverpa pest species', BMC Biology, bind 15, nr. 1, 63. https://doi.org/10.1186/s12915-017-0402-6

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abstract = "BACKGROUND: Helicoverpa armigera and Helicoverpa zea are major caterpillar pests of Old and New World agriculture, respectively. Both, particularly H. armigera, are extremely polyphagous, and H. armigera has developed resistance to many insecticides. Here we use comparative genomics, transcriptomics and resequencing to elucidate the genetic basis for their properties as pests.RESULTS: We find that, prior to their divergence about 1.5 Mya, the H. armigera/H. zea lineage had accumulated up to more than 100 more members of specific detoxification and digestion gene families and more than 100 extra gustatory receptor genes, compared to other lepidopterans with narrower host ranges. The two genomes remain very similar in gene content and order, but H. armigera is more polymorphic overall, and H. zea has lost several detoxification genes, as well as about 50 gustatory receptor genes. It also lacks certain genes and alleles conferring insecticide resistance found in H. armigera. Non-synonymous sites in the expanded gene families above are rapidly diverging, both between paralogues and between orthologues in the two species. Whole genome transcriptomic analyses of H. armigera larvae show widely divergent responses to different host plants, including responses among many of the duplicated detoxification and digestion genes.CONCLUSIONS: The extreme polyphagy of the two heliothines is associated with extensive amplification and neofunctionalisation of genes involved in host finding and use, coupled with versatile transcriptional responses on different hosts. H. armigera's invasion of the Americas in recent years means that hybridisation could generate populations that are both locally adapted and insecticide resistant.",

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T1 - Genomic innovations, transcriptional plasticity and gene loss underlying the evolution and divergence of two highly polyphagous and invasive Helicoverpa pest species

AU - Pearce, S L

AU - Clarke, D F

AU - East, P D

AU - Elfekih, S

AU - Gordon, K H J

AU - Jermiin, L S

AU - McGaughran, A

AU - Oakeshott, J G

AU - Papanikolaou, A

AU - Perera, O P

AU - Rane, R V

AU - Richards, S

AU - Tay, W T

AU - Walsh, T K

AU - Anderson, A

AU - Anderson, C J

AU - Asgari, S

AU - Board, P G

AU - Bretschneider, A

AU - Campbell, P M

AU - Chertemps, T

AU - Christeller, J T

AU - Coppin, C W

AU - Downes, S J

AU - Duan, G

AU - Farnsworth, C A

AU - Good, R T

AU - Han, L B

AU - Han, Y C

AU - Hatje, K

AU - Horne, I

AU - Huang, Y P

AU - Hughes, D S T

AU - Jacquin-Joly, E

AU - James, W

AU - Jhangiani, S

AU - Kollmar, M

AU - Kuwar, S S

AU - Li, S

AU - Liu, N-Y

AU - Maibeche, M T

AU - Miller, J R

AU - Montagne, N

AU - Perry, T

AU - Qu, J

AU - Song, S V

AU - Sutton, G G

AU - Vogel, H

AU - Walenz, B P

AU - Xu, W

AU - Zhang, H-J

AU - Zou, Z

AU - Batterham, P

AU - Edwards, O R

AU - Feyereisen, Rene

AU - Gibbs, R A

AU - Heckel, D G

AU - McGrath, A

AU - Robin, C

AU - Scherer, S E

AU - Worley, K C

AU - Wu, Y D

PY - 2017/7/31

Y1 - 2017/7/31

N2 - BACKGROUND: Helicoverpa armigera and Helicoverpa zea are major caterpillar pests of Old and New World agriculture, respectively. Both, particularly H. armigera, are extremely polyphagous, and H. armigera has developed resistance to many insecticides. Here we use comparative genomics, transcriptomics and resequencing to elucidate the genetic basis for their properties as pests.RESULTS: We find that, prior to their divergence about 1.5 Mya, the H. armigera/H. zea lineage had accumulated up to more than 100 more members of specific detoxification and digestion gene families and more than 100 extra gustatory receptor genes, compared to other lepidopterans with narrower host ranges. The two genomes remain very similar in gene content and order, but H. armigera is more polymorphic overall, and H. zea has lost several detoxification genes, as well as about 50 gustatory receptor genes. It also lacks certain genes and alleles conferring insecticide resistance found in H. armigera. Non-synonymous sites in the expanded gene families above are rapidly diverging, both between paralogues and between orthologues in the two species. Whole genome transcriptomic analyses of H. armigera larvae show widely divergent responses to different host plants, including responses among many of the duplicated detoxification and digestion genes.CONCLUSIONS: The extreme polyphagy of the two heliothines is associated with extensive amplification and neofunctionalisation of genes involved in host finding and use, coupled with versatile transcriptional responses on different hosts. H. armigera's invasion of the Americas in recent years means that hybridisation could generate populations that are both locally adapted and insecticide resistant.

AB - BACKGROUND: Helicoverpa armigera and Helicoverpa zea are major caterpillar pests of Old and New World agriculture, respectively. Both, particularly H. armigera, are extremely polyphagous, and H. armigera has developed resistance to many insecticides. Here we use comparative genomics, transcriptomics and resequencing to elucidate the genetic basis for their properties as pests.RESULTS: We find that, prior to their divergence about 1.5 Mya, the H. armigera/H. zea lineage had accumulated up to more than 100 more members of specific detoxification and digestion gene families and more than 100 extra gustatory receptor genes, compared to other lepidopterans with narrower host ranges. The two genomes remain very similar in gene content and order, but H. armigera is more polymorphic overall, and H. zea has lost several detoxification genes, as well as about 50 gustatory receptor genes. It also lacks certain genes and alleles conferring insecticide resistance found in H. armigera. Non-synonymous sites in the expanded gene families above are rapidly diverging, both between paralogues and between orthologues in the two species. Whole genome transcriptomic analyses of H. armigera larvae show widely divergent responses to different host plants, including responses among many of the duplicated detoxification and digestion genes.CONCLUSIONS: The extreme polyphagy of the two heliothines is associated with extensive amplification and neofunctionalisation of genes involved in host finding and use, coupled with versatile transcriptional responses on different hosts. H. armigera's invasion of the Americas in recent years means that hybridisation could generate populations that are both locally adapted and insecticide resistant.

KW - Journal Article

U2 - 10.1186/s12915-017-0402-6

DO - 10.1186/s12915-017-0402-6

M3 - Journal article

C2 - 28756777

SN - 1741-7007

VL - 15

JO - B M C Biology

JF - B M C Biology

IS - 1

M1 - 63

ER -

Genomic innovations, transcriptional plasticity and gene loss underlying the evolution and divergence of two highly polyphagous and invasive Helicoverpa pest species

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