The draft genome of whitefly Bemisia tabaci MEAM1, a global crop pest, provides novel insights into virus transmission, host adaptation, and insecticide resistance

Wenbo Chen, Daniel K. Hasegawa, Navneet Kaur, Adi Kliot, Patricia Valle Pinheiro, Junbo Luan, Marcus C. Stensmyr, Yi Zheng, Wenli Liu, Honghe Sun, Yimin Xu, Yuan Luo, Angela Kruse, Xiaowei Yang, Svetlana Kontsedalov, Galina Lebedev, Tonja W. Fisher, David R. Nelson, Wayne B. Hunter, Judith K BrownGeorg Jander, Michelle Cilia, Angela E. Douglas, Murad Ghanim, Alvin M. Simmons, William M. Wintermantel, Kai Shu Ling, Zhangjun Fei

Research output: Contribution to journalArticle

65 Citations (Scopus)

Abstract

Background: The whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) is among the 100 worst invasive species in the world. As one of the most important crop pests and virus vectors, B. tabaci causes substantial crop losses and poses a serious threat to global food security. Results: We report the 615-Mb high-quality genome sequence of B. tabaci Middle East-Asia Minor 1 (MEAM1), the first genome sequence in the Aleyrodidae family, which contains 15,664 protein-coding genes. The B. tabaci genome is highly divergent from other sequenced hemipteran genomes, sharing no detectable synteny. A number of known detoxification gene families, including cytochrome P450s and UDP-glucuronosyltransferases, are significantly expanded in B. tabaci. Other expanded gene families, including cathepsins, large clusters of tandemly duplicated B. tabaci-specific genes, and phosphatidylethanolamine-binding proteins (PEBPs), were found to be associated with virus acquisition and transmission and/or insecticide resistance, likely contributing to the global invasiveness and efficient virus transmission capacity of B. tabaci. The presence of 142 horizontally transferred genes from bacteria or fungi in the B. tabaci genome, including genes encoding hopanoid/sterol synthesis and xenobiotic detoxification enzymes that are not present in other insects, offers novel insights into the unique biological adaptations of this insect such as polyphagy and insecticide resistance. Interestingly, two adjacent bacterial pantothenate biosynthesis genes, panB and panC, have been co-transferred into B. tabaci and fused into a single gene that has acquired introns during its evolution. Conclusions: The B. tabaci genome contains numerous genetic novelties, including expansions in gene families associated with insecticide resistance, detoxification and virus transmission, as well as numerous horizontally transferred genes from bacteria and fungi. We believe these novelties likely have shaped B. tabaci as a highly invasive polyphagous crop pest and efficient vector of plant viruses. The genome serves as a reference for resolving the B. tabaci cryptic species complex, understanding fundamental biological novelties, and providing valuable genetic information to assist the development of novel strategies for controlling whiteflies and the viruses they transmit.

Original languageEnglish (US)
Article number110
JournalBMC Biology
Volume14
Issue number1
DOIs
StatePublished - Dec 14 2016
Externally publishedYes

Fingerprint

Insecticide Resistance
crop pest
plant pests
whitefly
Hemiptera
Middle East
Far East
insecticide resistance
virus transmission
Bemisia tabaci
Insecticides
Aleyrodidae
Viruses
East Asia
Crops
insecticide
virus
genome
Genes
Genome

Keywords

  • Bemisia tabaci
  • Draft genome
  • Insecticide resistance
  • Polyphagy
  • Virus transmission
  • Whitefly

ASJC Scopus subject areas

  • Biotechnology
  • Structural Biology
  • Physiology
  • Ecology, Evolution, Behavior and Systematics
  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)
  • Plant Science
  • Developmental Biology
  • Cell Biology

Cite this

The draft genome of whitefly Bemisia tabaci MEAM1, a global crop pest, provides novel insights into virus transmission, host adaptation, and insecticide resistance. / Chen, Wenbo; Hasegawa, Daniel K.; Kaur, Navneet; Kliot, Adi; Pinheiro, Patricia Valle; Luan, Junbo; Stensmyr, Marcus C.; Zheng, Yi; Liu, Wenli; Sun, Honghe; Xu, Yimin; Luo, Yuan; Kruse, Angela; Yang, Xiaowei; Kontsedalov, Svetlana; Lebedev, Galina; Fisher, Tonja W.; Nelson, David R.; Hunter, Wayne B.; Brown, Judith K; Jander, Georg; Cilia, Michelle; Douglas, Angela E.; Ghanim, Murad; Simmons, Alvin M.; Wintermantel, William M.; Ling, Kai Shu; Fei, Zhangjun.

In: BMC Biology, Vol. 14, No. 1, 110, 14.12.2016.

Research output: Contribution to journalArticle

Chen, W, Hasegawa, DK, Kaur, N, Kliot, A, Pinheiro, PV, Luan, J, Stensmyr, MC, Zheng, Y, Liu, W, Sun, H, Xu, Y, Luo, Y, Kruse, A, Yang, X, Kontsedalov, S, Lebedev, G, Fisher, TW, Nelson, DR, Hunter, WB, Brown, JK, Jander, G, Cilia, M, Douglas, AE, Ghanim, M, Simmons, AM, Wintermantel, WM, Ling, KS & Fei, Z 2016, 'The draft genome of whitefly Bemisia tabaci MEAM1, a global crop pest, provides novel insights into virus transmission, host adaptation, and insecticide resistance', BMC Biology, vol. 14, no. 1, 110. https://doi.org/10.1186/s12915-016-0321-y
Chen, Wenbo ; Hasegawa, Daniel K. ; Kaur, Navneet ; Kliot, Adi ; Pinheiro, Patricia Valle ; Luan, Junbo ; Stensmyr, Marcus C. ; Zheng, Yi ; Liu, Wenli ; Sun, Honghe ; Xu, Yimin ; Luo, Yuan ; Kruse, Angela ; Yang, Xiaowei ; Kontsedalov, Svetlana ; Lebedev, Galina ; Fisher, Tonja W. ; Nelson, David R. ; Hunter, Wayne B. ; Brown, Judith K ; Jander, Georg ; Cilia, Michelle ; Douglas, Angela E. ; Ghanim, Murad ; Simmons, Alvin M. ; Wintermantel, William M. ; Ling, Kai Shu ; Fei, Zhangjun. / The draft genome of whitefly Bemisia tabaci MEAM1, a global crop pest, provides novel insights into virus transmission, host adaptation, and insecticide resistance. In: BMC Biology. 2016 ; Vol. 14, No. 1.
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T1 - The draft genome of whitefly Bemisia tabaci MEAM1, a global crop pest, provides novel insights into virus transmission, host adaptation, and insecticide resistance

AU - Chen, Wenbo

AU - Hasegawa, Daniel K.

AU - Kaur, Navneet

AU - Kliot, Adi

AU - Pinheiro, Patricia Valle

AU - Luan, Junbo

AU - Stensmyr, Marcus C.

AU - Zheng, Yi

AU - Liu, Wenli

AU - Sun, Honghe

AU - Xu, Yimin

AU - Luo, Yuan

AU - Kruse, Angela

AU - Yang, Xiaowei

AU - Kontsedalov, Svetlana

AU - Lebedev, Galina

AU - Fisher, Tonja W.

AU - Nelson, David R.

AU - Hunter, Wayne B.

AU - Brown, Judith K

AU - Jander, Georg

AU - Cilia, Michelle

AU - Douglas, Angela E.

AU - Ghanim, Murad

AU - Simmons, Alvin M.

AU - Wintermantel, William M.

AU - Ling, Kai Shu

AU - Fei, Zhangjun

PY - 2016/12/14

Y1 - 2016/12/14

N2 - Background: The whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) is among the 100 worst invasive species in the world. As one of the most important crop pests and virus vectors, B. tabaci causes substantial crop losses and poses a serious threat to global food security. Results: We report the 615-Mb high-quality genome sequence of B. tabaci Middle East-Asia Minor 1 (MEAM1), the first genome sequence in the Aleyrodidae family, which contains 15,664 protein-coding genes. The B. tabaci genome is highly divergent from other sequenced hemipteran genomes, sharing no detectable synteny. A number of known detoxification gene families, including cytochrome P450s and UDP-glucuronosyltransferases, are significantly expanded in B. tabaci. Other expanded gene families, including cathepsins, large clusters of tandemly duplicated B. tabaci-specific genes, and phosphatidylethanolamine-binding proteins (PEBPs), were found to be associated with virus acquisition and transmission and/or insecticide resistance, likely contributing to the global invasiveness and efficient virus transmission capacity of B. tabaci. The presence of 142 horizontally transferred genes from bacteria or fungi in the B. tabaci genome, including genes encoding hopanoid/sterol synthesis and xenobiotic detoxification enzymes that are not present in other insects, offers novel insights into the unique biological adaptations of this insect such as polyphagy and insecticide resistance. Interestingly, two adjacent bacterial pantothenate biosynthesis genes, panB and panC, have been co-transferred into B. tabaci and fused into a single gene that has acquired introns during its evolution. Conclusions: The B. tabaci genome contains numerous genetic novelties, including expansions in gene families associated with insecticide resistance, detoxification and virus transmission, as well as numerous horizontally transferred genes from bacteria and fungi. We believe these novelties likely have shaped B. tabaci as a highly invasive polyphagous crop pest and efficient vector of plant viruses. The genome serves as a reference for resolving the B. tabaci cryptic species complex, understanding fundamental biological novelties, and providing valuable genetic information to assist the development of novel strategies for controlling whiteflies and the viruses they transmit.

AB - Background: The whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) is among the 100 worst invasive species in the world. As one of the most important crop pests and virus vectors, B. tabaci causes substantial crop losses and poses a serious threat to global food security. Results: We report the 615-Mb high-quality genome sequence of B. tabaci Middle East-Asia Minor 1 (MEAM1), the first genome sequence in the Aleyrodidae family, which contains 15,664 protein-coding genes. The B. tabaci genome is highly divergent from other sequenced hemipteran genomes, sharing no detectable synteny. A number of known detoxification gene families, including cytochrome P450s and UDP-glucuronosyltransferases, are significantly expanded in B. tabaci. Other expanded gene families, including cathepsins, large clusters of tandemly duplicated B. tabaci-specific genes, and phosphatidylethanolamine-binding proteins (PEBPs), were found to be associated with virus acquisition and transmission and/or insecticide resistance, likely contributing to the global invasiveness and efficient virus transmission capacity of B. tabaci. The presence of 142 horizontally transferred genes from bacteria or fungi in the B. tabaci genome, including genes encoding hopanoid/sterol synthesis and xenobiotic detoxification enzymes that are not present in other insects, offers novel insights into the unique biological adaptations of this insect such as polyphagy and insecticide resistance. Interestingly, two adjacent bacterial pantothenate biosynthesis genes, panB and panC, have been co-transferred into B. tabaci and fused into a single gene that has acquired introns during its evolution. Conclusions: The B. tabaci genome contains numerous genetic novelties, including expansions in gene families associated with insecticide resistance, detoxification and virus transmission, as well as numerous horizontally transferred genes from bacteria and fungi. We believe these novelties likely have shaped B. tabaci as a highly invasive polyphagous crop pest and efficient vector of plant viruses. The genome serves as a reference for resolving the B. tabaci cryptic species complex, understanding fundamental biological novelties, and providing valuable genetic information to assist the development of novel strategies for controlling whiteflies and the viruses they transmit.

KW - Bemisia tabaci

KW - Draft genome

KW - Insecticide resistance

KW - Polyphagy

KW - Virus transmission

KW - Whitefly

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