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Genome-wide investigation of transcription factors provides insights into transcriptional regulation in Plutella xylostella

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Abstract

Transcription factors (TFs), which play a vital role in regulating gene expression, are prevalent in all organisms and characterization of them may provide important clues for understanding regulation in vivo. The present study reports a genome-wide investigation of TFs in the diamondback moth, Plutella xylostella (L.), a worldwide pest of crucifers. A total of 940 TFs distributed among 133 families were identified. Phylogenetic analysis of insect species showed that some of these families were found to have expanded during the evolution of P. xylostella or Lepidoptera. RNA-seq analysis showed that some of the TF families, such as zinc fingers, homeobox, bZIP, bHLH, and MADF_DNA_bdg genes, were highly expressed in certain tissues including midgut, salivary glands, fat body, and hemocytes, with an obvious sex-biased expression pattern. In addition, a number of TFs showed significant differences in expression between insecticide susceptible and resistant strains, suggesting that these TFs play a role in regulating genes related to insecticide resistance. Finally, we identified an expansion of the HOX cluster in Lepidoptera, which might be related to Lepidoptera-specific evolution. Knockout of this cluster using CRISPR/Cas9 showed that the egg cannot hatch, indicating that this cluster may be related to egg development and maturation. This is the first comprehensive study on identifying and characterizing TFs in P. xylostella. Our results suggest that some TF families are expanded in the P. xylostella genome, and these TFs may have important biological roles in growth, development, sexual dimorphism, and resistance to insecticides. The present work provides a solid foundation for understanding regulation via TFs in P. xylostella and insights into the evolution of the P. xylostella genome.

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References

  • Aufauvre J, Misme-Aucouturier B, Viguès B, Texier C, Delbac F, Blot N (2014) Transcriptome analyses of the honeybee response to Nosema ceranae and insecticides. PLoS ONE 9(3): e91686. https://doi.org/10.1371/journal.pone.0091686

  • Benjamini Y DY (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188

    Article  Google Scholar 

  • Bhaskar V, Courey AJ (2002) The MADF-BESS domain factor Dip3 potentiates synergistic activation by Dorsal and Twist. Gene 299(1–2):173–184

    Article  CAS  PubMed  Google Scholar 

  • Bitra K, Palli SR (2010) The members of bHLH transcription factor superfamily are required for female reproduction in the red flour beetle, Tribolium castaneum. J Insect Physiol 56(10):1481–1489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Botas J (1993) Control of morphogenesis and differentiation by HOM/Hox genes. Curr Opin Cell Biol 5(6):1015–1022

    Article  CAS  PubMed  Google Scholar 

  • Chai CL, Zhang Z, Huang FF, Wang XY, Yu QY, Liu BB, Tian T, Xia QY, Lu C, Xiang ZH (2008) A genomewide survey of homeobox genes and identification of novel structure of the Hox cluster in the silkworm, Bombyx mori. Insect Biochem Mol Biol 38(12):1111–1120

    Article  CAS  PubMed  Google Scholar 

  • Chung HR, Schafer U, Jackle H, Bohm S (2002) Genomic expansion and clustering of ZAD-containing C2H2 zinc-finger genes in Drosophila. EMBO Rep 3(12):1158–1162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chung HR, Lohr U, Jackle H (2007) Lineage-specific expansion of the zinc finger associated domain ZAD. Mol Biol Evol 24(9):1934–1943

    Article  CAS  PubMed  Google Scholar 

  • Consortium THG (2012) Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487(7405):94–98

    Article  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27(8):1164–1165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Derelle R, Lopez P, Le Guyader H, Manuel M (2007) Homeodomain proteins belong to the ancestral molecular toolkit of eukaryotes. Evol Dev 9(3):212–219

    Article  CAS  PubMed  Google Scholar 

  • Dorn A, Affolter M, Gehring WJ, Leupin W (1994) Homeodomain proteins in development and therapy. Pharmacol Ther 61(1–2):155–184

    Article  CAS  PubMed  Google Scholar 

  • Duan J, Xia Q, Cheng D, Zha X, Zhao P, Xiang Z (2008) Species-specific expansion of C2H2 zinc-finger genes and their expression profiles in silkworm, Bombyx mori. Insect Biochem Mol Biol 38(12):1121–1129

    Article  CAS  PubMed  Google Scholar 

  • Duan J, Li R, Cheng D, Fan W, Zha X, Cheng T, Wu Y, Wang J, Mita K, Xiang Z, Xia Q (2009) SilkDB v2.0: a platform for silkworm (Bombyx mori) genome biology. Nucleic Acids Res 38(Database issue):D453-456

    Google Scholar 

  • Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14(9):755–763 pii]

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Englbrecht CC, Schoof H, Bohm S (2004) Conservation, diversification and expansion of C2H2 zinc finger proteins in the Arabidopsis thaliana genome. BMC Genomics 5(1):39

    Article  PubMed  PubMed Central  Google Scholar 

  • Ferguson L, Marletaz F, Carter J-M, Taylor WR, Gibbs M et al (2014) Ancient expansion of the hox cluster in lepidoptera generated four homeobox genes implicated in extra-embryonic tissue formation. PLoS Genet 10(10):e1004698. https://doi.org/10.1371/journal.pgen.1004698

    Article  PubMed  PubMed Central  Google Scholar 

  • Furlong MJ, Wright DJ, Dosdall LM (2013) Diamondback moth ecology and management: problems, progress, and prospects. Annu Rev Entomol 58:517–541

    Article  CAS  PubMed  Google Scholar 

  • Gao G, Zhong Y, Guo A, Zhu Q, Tang W, Zheng W, Gu X, Wei L, Luo J (2006) DRTF: a database of rice transcription factors. Bioinformatics 22(10):1286–1287

    Article  CAS  PubMed  Google Scholar 

  • Gehring WJ, Affolter M, Burglin T (1994) Homeodomain proteins. Annu Rev Biochem 63:487–526

    Article  CAS  PubMed  Google Scholar 

  • Guo AY, Chen X, Gao G, Zhang H, Zhu QH, Liu XC, Zhong YF, Gu X, He K, Luo J (2008) PlantTFDB: a comprehensive plant transcription factor database. Nucleic Acids Res 36(Database issue):D966-969

    Google Scholar 

  • Gupta BP, Sternberg PW (2002) Tissue-specific regulation of the LIM homeobox gene lin-11 during development of the Caenorhabditis elegans egg-laying system. Dev Biol 247(1):102–115

    Article  CAS  PubMed  Google Scholar 

  • He W, You M, Vasseur L, Yang G, Xie M, Cui K, Bai J, Liu C, Li X, Xu X, Huang S (2012) Developmental and insecticide-resistant insights from the de novo assembled transcriptome of the diamondback moth, Plutella xylostella. Genomics 99(3):169–177

    Article  CAS  PubMed  Google Scholar 

  • Hemingway J, Field L, Vontas J (2002) An overview of insecticide resistance. Science 298(5591):96–97

    Article  CAS  PubMed  Google Scholar 

  • Hsu HH, Chung KM, Chen TC, Chang BY (2006) Role of the sigma factor in transcription initiation in the absence of core RNA polymerase. Cell 127:317–327

    Article  CAS  PubMed  Google Scholar 

  • Huang L, Cheng T, Xu P, Fang T, Xia Q (2011) Bombyx mori transcription factors: genome-wide identification, expression profiles and response to pathogens by microarray analysis. J Insect Sci 12:40

    Google Scholar 

  • Huang Y, Chen Y, Zeng B, Wang Y, James AA, Gurr GM, Yang G, Lin X, Huang Y, You M (2016) CRISPR/Cas9 mediated knockout of the abdominal-A homeotic gene in the globla pest, diamondback moth (Plutella xylostella). Insect Biochem Mol Biol 75:98–106

    Article  CAS  PubMed  Google Scholar 

  • Jakoby M, Weisshaar B, Droge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7(3):106–111

    Article  CAS  PubMed  Google Scholar 

  • Jones S (2004) An overview of the basic helix-loop-helix proteins. Genome Biol 5(6):226

    Article  PubMed  PubMed Central  Google Scholar 

  • Junell A, Uvell H, Davis MM, Edlundh-Rose E, Antonsson A et al (2010) The POU transcription factor Drifter/Ventral veinless regulates expression of Drosophila immune defense genes. Mol Cell Bio 30:3672–3684

    Article  CAS  Google Scholar 

  • Kadesh T (1993) Consequences of heterodimeric interactions among helix-loop-helix proteins. cell growth differentiation 4:49–55

    Google Scholar 

  • Kang W, Katsuma S, Matsuda-Imai N, Kurihara M, Yoshiga T, Shimada T, Matsumoto S (2012) Identification and characterization of host factors interacting with Bombyx mori nucleopolyhedrovirus ORF8. J Microbiol 50(3):469–477

    Article  CAS  PubMed  Google Scholar 

  • Kappen C (2000) The homeodomain: an ancient evolutionary motif in animals and plants. Comput Chem 24(1):95–103

    Article  CAS  PubMed  Google Scholar 

  • Kingsley PD, Palis J (1994) GRP2 proteins contain both CCHC zinc fingers and a cold shock domain. Plant Cell 6(11):1522–1523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ladomery M, Dellaire G (2002) Multifunctional zinc finger proteins in development and disease. Ann Hum Genet 66(Pt 5–6):331–342

    Article  CAS  PubMed  Google Scholar 

  • Letunic I, Copley RR, Schmidt S, Ciccarelli FD, Doerks T, Schultz J, Ponting CP, Bork P (2004) SMART 4.0: towards genomic data integration. Nucleic Acids Res 32(Database issue):D142-144

    Google Scholar 

  • Li H, Baker BS (1998) Her, a gene required for sexual differentiation in Drosophila, encodes a zinc finger protein with characteristics of ZFY-like proteins and is expressed independently of the sex determination hierarchy. Development 125(2):225–235

    CAS  PubMed  Google Scholar 

  • Li D, Fu F, Zhang H, Song F (2015) Genome-wide systematic characterization of the bZIP transcriptional factor family in tomato (Solanum lycopersicum L.). BMC Genomics 16(1):771

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu X, Chu Z (2015) Genome-wide evolutionary characterization and analysis of bZIP transcription factors and their expression profiles in response to multiple abiotic stresses in Brachypodium distachyon. BMC Genomics 16:227

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu A, Wang Y, Dang C, Zhang D, Song H, Yao Q, Chen K (2012) A genome-wide identification and analysis of the basic helix-loop-helix transcription factors in the ponerine ant, Harpegnathos saltator. BMC Evol Biol 12:165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Chen N, Chen F, Cai B, Dal Santo S, Tornielli GB, Pezzotti M, Cheng ZM (2014) Genome-wide analysis and expression profile of the bZIP transcription factor gene family in grapevine (Vitis vinifera). BMC Genomics 15:281

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu XT, Wang Y, Wang XH, Tao XF, Yao Q, Chen KP (2015) A genome-wide identification and classification of basic helix-loop-helix genes in the jewel wasp, Nasonia vitripennis (Hymenoptera: Pteromalidae). Genome 57(10):525–536

    Article  Google Scholar 

  • Massari ME, Murre C (2000) Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol Cell Biol 20(2):429–440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Merkel DJ, Wells SB, Hilburn BC, Elazzouzi F, Perez-Alvarado GC, Lee BM (2013) The C-terminal region of cytoplasmic polyadenylation element binding protein is a ZZ domain with potential for protein-protein interactions. J Mol Biol 425(11):2015–2026

    Article  CAS  PubMed  Google Scholar 

  • Mihailovich M, Militti C, Gabaldon T, Gebauer F (2010) Eukaryotic cold shock domain proteins: highly versatile regulators of gene expression. Bioessays 32(2):109–118

    Article  CAS  PubMed  Google Scholar 

  • Miller J, McLachlan AD, Klug A (1985) Repetitive zinc-binding domains in the protein transcription factor IIIA from Xenopus oocytes. EMBO J 4(6):1609–1614

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moehren U, Eckey M, Baniahmad A (2004) Gene repression by nuclear hormone receptors. Essays Biochem 40:89–104

    Article  CAS  PubMed  Google Scholar 

  • Munoz-Descalzo S, Terol J, Paricio N (2005) Cabut, a C2H2 zinc finger transcription factor, is required during Drosophila dorsal closure downstream of JNK signaling. Dev Biol 287(1):168–179

    Article  CAS  PubMed  Google Scholar 

  • Munoz-Torres MC, Reese JT, Childers CP, Bennett AK, Sundaram JP, Childs KL, Anzola JM, Milshina N, Elsik CG (2011) Hymenoptera Genome Database: integrated community resources for insect species of the order Hymenoptera. Nucleic Acids Res 39(Database issue):D658-662

    Google Scholar 

  • Murre C MP, Vaessin H, Caudy M, Jan LY, Jan YN, Cabrera CV, Buskin JN HS, Lassar AB et al (1989) Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell 58(3):537–544

    Article  CAS  PubMed  Google Scholar 

  • Musser RO, Hum-Musser SM, Eichenseer H, Peiffer M, Ervin G, Murphy JB, Felton GW (2002) Herbivory: caterpillar saliva beats plant defences. Nature 416(6881):599–600

    Article  CAS  PubMed  Google Scholar 

  • Nabel G, Baltimore D (1987) An inducible transcription factor activates expression of human immunodeficiency virus in T cells. Nature 326(6114):711–713

    Article  CAS  PubMed  Google Scholar 

  • Nijhawan A, Jain M, Tyagi AK, Khurana JP (2008) Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice. Plant Physiol 146(2):333–350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Padmalatha KV, Dhandapani G, Kanakachari M, Kumar S, Dass A, Patil DP, Rajamani V, Kumar K, Pathak R, Rawat B, Leelavathi S, Reddy PS, Jain N, Powar KN, Hiremath V, Katageri IS, Reddy MK, Solanke AU, Reddy VS, Kumar PA (2012) Genome-wide transcriptomic analysis of cotton under drought stress reveal significant down-regulation of genes and pathways involved in fibre elongation and up-regulation of defense responsive genes. Plant Mol Biol 78(3):223–246

    Article  CAS  PubMed  Google Scholar 

  • Perezgasga L, Jiang J, Bolival B Jr, Hiller M, Benson E, Fuller MT, White-Cooper H (2004) Regulation of transcription of meiotic cell cycle and terminal differentiation genes by the testis-specific Zn-finger protein matotopetli. Development 131(8):1691–1702

    Article  CAS  PubMed  Google Scholar 

  • Pollard SL, Holland PW, Retnakaran A, Krell P, Feng Q, Arif B (2000) Evidence for 14 homeobox gene clusters in human genome ancestry. Curr Biol 10(17):1059–1062 2(4 :187–199.

    Article  CAS  PubMed  Google Scholar 

  • Riechmann JL, Ratcliffe OJ (2000) A genomic perspective on plant transcription factors. Curr Opin Plant Biol 3(5):423–434

    Article  CAS  PubMed  Google Scholar 

  • Riechmann JL, Heard J, Martin G, Reuber L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu G (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290(5499):2105–2110

    Article  CAS  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Saibo NJ, Lourenco T, Oliveira MM (2009) Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses. Ann Bot 103(4):609–623

    Article  CAS  PubMed  Google Scholar 

  • Schweizer F, Fernandez-Calvo P, Zander M, Diez-Diaz M, Fonseca S, Glauser G, Lewsey MG, Ecker JR, Solano R, Reymond P (2013) Arabidopsis basic helix-loop-helix transcription factors MYC2, MYC3, and MYC4 regulate glucosinolate biosynthesis, insect performance, and feeding behavior. Plant Cell 25(8):3117–3132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi X, Kachirskaia I, Walter KL, Kuo JH, Lake A, Davrazou F, Chan SM, Martin DG, Fingerman IM, Briggs SD, Howe L, Utz PJ, Kutateladze TG, Lugovskoy AA, Bedford MT, Gozani O (2007) Proteome-wide analysis in Saccharomyces cerevisiae identifies several PHD fingers as novel direct and selective binding modules of histone H3 methylated at either lysine 4 or lysine 36. J Biol Chem 282(4):2450–2455

    Article  CAS  PubMed  Google Scholar 

  • Simionato E, Ledent V, Richards G, Thomas-Chollier M, Kerner P, Coornaert D, Degnan BM, Vervoort M (2007) Origin and diversification of the basic helix-loop-helix gene family in metazoans: insights from comparative genomics. BMC Evol Biol 7:33

    Article  PubMed  PubMed Central  Google Scholar 

  • Sourmeli S, Papantonis A, Lecanidou R (2005) A novel role for the Bombyx SIbo homologue, BmC/EBP, in insect choriogenesis. Biochem Bioph Res Co 337(2):713–719

    Article  CAS  Google Scholar 

  • Stathopoulos A, Levine M (2002) Dorsal gradient networks in the Drosophila embryo. Dev Biol 246(1):57–67

    Article  CAS  PubMed  Google Scholar 

  • Sun W, Yu H, Shen Y, Banno Y, Xiang Z, Zhang Z (2012) Phylogeny and evolutionary history of the silkworm. Sci China Life Sci 55(6):483–496. https://doi.org/10.1007/s11427-012-4334-7

    Article  PubMed  Google Scholar 

  • Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-SEq. Bioinformatics 25(9):1105–1111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7(3):562–578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ureña E, Manjón C, Franch-Marro X, Martín D (2014) Transcription factor E93 specifies adult metamorphosis in hemimetabolous and holometabolous insects. PNAS 111(19):7024–7029

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Chen K, Yao Q, Wang W, Zhu Z (2007) The basic helix-loop-helix transcription factor family in Bombyx mori. Dev Genes Evol 217(10):715–723

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Chen K, Yao Q, Wang W, Zhu Z (2008) The basic helix-loop-helix transcription factor family in the honey bee, Apis mellifera. J Insect Sci 8(1):40

    PubMed Central  Google Scholar 

  • Wang J, Zhou J, Zhang B, Vanitha J, Ramachandran S, Jiang SY (2011) Genome-wide expansion and expression divergence of the basic leucine zipper transcription factors in higher plants with an emphasis on sorghum. J Integr Plant Biol 53(3):212–231

    Article  CAS  PubMed  Google Scholar 

  • Weatherbee SD, Halder G, Kim J, Hudson A, Carroll S (1998) Ultrabithorax regulates genes at several levels of the wing-patterning hierarchy to shape the development of the Drosophila haltere. Genes Dev 12:1474–1482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson D, Charoensawan V, Kummerfeld SK, Teichmann SA (2008) DBD–taxonomically broad transcription factor predictions: new content and functionality. Nucleic Acids Res 36(Database issue):D88-92

    PubMed  Google Scholar 

  • Wysocka J, Swigut T, Xiao H, Milne TA, Kwon SY, Landry J, Kauer M, Tackett AJ, Chait BT, Badenhorst P, Wu C, Allis CD (2006) A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 442(7098):86–90

    Article  CAS  PubMed  Google Scholar 

  • Xia Q, Cheng D, Duan J, Wang G, Cheng T, Zha X, Liu C, Zhao P, Dai F, Zhang Z, He N, Zhang L, Xiang Z (2007) Microarray-based gene expression profiles in multiple tissues of the domesticated silkworm, Bombyx mori. Genome Biol 8(8):R162

    Article  PubMed  PubMed Central  Google Scholar 

  • Yilmaz A, Nishiyama MY Jr, Fuentes BG, Souza GM, Janies D, Gray J, Grotewold E (2009) GRASSIUS: a platform for comparative regulatory genomics across the grasses. Plant Physiol 149(1):171–180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • You M, Yue Z, He W, Yang X, Yang G, Xie M, Zhan D, Baxter SW, Vasseur L, Gurr GM, Douglas CJ, Bai J, Wang P, Cui K, Huang S, Li X, Zhou Q, Wu Z, Chen Q, Liu C, Wang B, Xu X, Lu C, Hu M, Davey JW, Smith SM, Chen M, Xia X, Tang W, Ke F, Zheng D, Hu Y, Song F, You Y, Ma X, Peng L, Zheng Y, Liang Y, Chen Y, Yu L, Zhang Y, Liu Y, Li G, Fang L, Li J, Zhou X, Luo Y, Gou C, Wang J, Yang H (2013) A heterozygous moth genome provides insights into herbivory and detoxification. Nat Genet 45(2):220–225

    Article  CAS  PubMed  Google Scholar 

  • Zhan S, Reppert SM (2012) MonarchBase: the monarch butterfly genome database. Nucleic Acids Res 41(Database issue):D758-763

    Google Scholar 

  • Zhan S, Merlin C, Boore JL, Reppert SM (2011) The monarch butterfly genome yields insights into long-distance migration. Cell 147(5):1171–1185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Lu YX, Liu J, Yang C, Feng QL, Xu WH (2013) A regulatory pathway, ecdysone-transcription factor relish-cathepsin L, is involved in insect fat body dissociation. Plos Genet 9(2):e1003273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou J, Ng SB, Chng WJ (2013) LIN28/LIN28B: an emerging oncogenic driver in cancer stem cells. Int J Biochem Cell Biol 45(5):973–978

    Article  CAS  PubMed  Google Scholar 

  • Zhu QH GA, Gao G, Zhong YF, Xu M, Huang M, Luo J (2007) DPTF: a database of poplar transcription factors. Bioinformatics 23:1307–1308

    Article  CAS  PubMed  Google Scholar 

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Funding

This work was funded by the National Natural Science Foundation of China (Grant numbers 31230061 and 31320103922) and Fujian Provincial Key Project of Agricultural Science and Technology (2018NZ01010013).

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  1. Qian Zhao and Dongna Ma made equal contribution to this work.

Authors and Affiliations

  1. State Key Laboratory for Ecological Pest Control of Fujian - Taiwan Crops and Institute of Applied Ecology, Fujian Agriculture and Forestry University, Fuzhou, 350002, People’s Republic of China

    Qian Zhao, Dongna Ma, Yuping Huang, Weiyi He, Yiying Li, Liette Vasseur & Minsheng You

  2. Fujian-Taiwan Joint Centre for Ecological Control of Crop Pests, Fujian Agriculture and Forestry University, Fuzhou, 350002, People’s Republic of China

    Qian Zhao, Dongna Ma, Yuping Huang, Weiyi He, Yiying Li & Minsheng You

  3. Joint International Research Laboratory of Ecological Pest Control, Ministry of Education, Fuzhou, 350002, People’s Republic of China

    Qian Zhao, Dongna Ma, Yuping Huang, Weiyi He & Minsheng You

  4. Department of Biological Sciences, Brock University, 500 Glenridge Avenue, St. Catharines, ON, L2S 3A1, Canada

    Liette Vasseur

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Contributions

QZ designed and performed the genome-wide analyses, interpreted the data, and drafted the manuscript. DM and YH helped to collect the data and performed the experiment validation. WH and WZ provided advice for the data analysis. LV and DM provided help in the data analysis and revised the manuscript. MY supervised the study. QZ and LV critically revised the manuscript. All authors read and approved the final manuscript.

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Correspondence to Minsheng You.

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All the authors declare that they have no conflict of interests.

Ethical approval

P. xylostella is not protected under any legislation in China since it is considered as pests, no permit for specimen collection and animal care clearance were required.

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Communicated by S. Hohmann.

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Zhao, Q., Ma, D., Huang, Y. et al. Genome-wide investigation of transcription factors provides insights into transcriptional regulation in Plutella xylostella . Mol Genet Genomics 293, 435–449 (2018). https://doi.org/10.1007/s00438-017-1389-y

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