Jekyll or Hyde? The genome (and more) of Nesidiocoris tenuis, a zoophytophagous predatory bug that is both a biological control agent and a pest

. 2021 Apr ; 30 (2) : 188-209. [epub] 20201222

Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid33305885

Nesidiocoris tenuis (Reuter) is an efficient predatory biological control agent used throughout the Mediterranean Basin in tomato crops but regarded as a pest in northern European countries. From the family Miridae, it is an economically important insect yet very little is known in terms of genetic information and no genomic or transcriptomic studies have been published. Here, we use a linked-read sequencing strategy on a single female N. tenuis. From this, we assembled the 355 Mbp genome and delivered an ab initio, homology-based and evidence-based annotation. Along the way, the bacterial "contamination" was removed from the assembly. In addition, bacterial lateral gene transfer (LGT) candidates were detected in the N. tenuis genome. The complete gene set is composed of 24 688 genes; the associated proteins were compared to other hemipterans (Cimex lectularis, Halyomorpha halys and Acyrthosiphon pisum). We visualized the genome using various cytogenetic techniques, such as karyotyping, CGH and GISH, indicating a karyotype of 2n = 32. Additional analyses include the localization of 18S rDNA and unique satellite probes as well as pooled sequencing to assess nucleotide diversity and neutrality of the commercial population. This is one of the first mirid genomes to be released and the first of a mirid biological control agent.

Zobrazit více v PubMed

Abreo, E. and Altier, N. (2019) Pangenome of Serratia marcescens strains from nosocomial and environmental origins reveals different populations and the links between them. Scientific Reports, 9(1), 46. PubMed PMC

Acland, A. , Agarwala, R. , Barrett, T. , Beck, J. , Benson, D.A. , Bollin, C. PubMed PMC

Andrews, S. , Krueger, F. , Seconds‐Pichon, A. , Biggins, F. and Wingett, S. (2015) In: FastQC. A quality control tool for high throughput sequence data. Babraham Bioinformatics. Cambridge: Babraham Institute.

Arnó, J. , Castañé, C. , Riudavets, J. and Gabarra, R. (2010) Risk of damage to tomato crops by the generalist zoophytophagous predator PubMed

Banaei‐Moghaddam, A.M. , Meier, K. , Karimi‐Ashtiyani, R. and Houben, A. (2013) Formation and expression of pseudogenes on the B chromosome of rye. Plant Cell, 25(7), 2536–2544. PubMed PMC

Benoit, J.B. , Adelman, Z.N. , Reinhardt, K. , Dolan, A. , Poelchau, M. , Jennings, E.C. PubMed PMC

Benson, G. (1999) Tandem repeats finder: A program to analyze DNA sequences. Nucleic Acids Research, 27(2), 573–580. PubMed PMC

Biondi, A. , Zappalà, L. , Di Mauro, A. , Tropea Garzia, G. , Russo, A. , Desneux, N.

Blankenfeldt, W. , Kuzin, A.P. , Skarina, T. , Korniyenko, Y. , Tong, L. , Bayer, P. PubMed PMC

Bolger, A.M. , Lohse, M. and Usadel, B. (2014) Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics, 30(15), 2114–2120. PubMed PMC

Bouagga, S. , Urbaneja, A. , Depalo, L. , Rubio, L. and Pérez‐Hedo, M. (2020) Zoophytophagous predator‐induced defences restrict accumulation of the tomato spotted wilt virus. Pest Management Science, 76(2), 561–567. PubMed

Boutet, E. , Lieberherr, D. , Tognolli, M. , Schneider, M. and Bairoch, A. (2008) UniProtKB/Swiss‐Prot: The manually annotated section of the UniProt KnowledgeBase. Methods in Molecular Biology, 406(January 2014), 89–112.

Boyd, B.M. , Allen, J.M. , Koga, R. , Fukatsu, T. , Sweet, A.D. , Johnson, K.P. PubMed PMC

Bruton, B.D. , Mitchell, F. , Fletcher, J. , Pair, S.D. , Wayadande, A. , Melcher, U. PubMed

Calvo, J.F. , Bolckmans, K. , Stansly, P.a. and Urbaneja, A. (2009) Predation by

Camacho, J.P.M. , Sharbel, T.F. and Beukeboom, L.W. (2000) B‐chromosome evolution. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 355(1394), 163–178. PubMed PMC

Camacho, C. , Coulouris, G. , Avagyan, V. , Ma, N. , Papadopoulos, J. , Bealer, K. PubMed PMC

Carabajal Paladino, L.Z. , Provazníková, I. , Berger, M. , Bass, C. , Aratchige, N.S. , López, S.N. PubMed PMC

Caspi‐Fluger, A. , Inbar, M. , Steinberg, S. , Friedmann, Y. , Freund, M. , Mozes‐Daube, N. PubMed

Castañé, C. , Arnó, J. , Gabarra, R. and Alomar, O. (2011) Plant damage to vegetable crops by zoophytophagous mirid predators. Biological Control, 59(1), 22–29.

Charlesworth, B. and Charlesworth, D. (2000) The degeneration of Y chromosomes. Philosophical Transactions of the Royal Society B: Biological Sciences, 355(1403), 1563–1572. PubMed PMC

Chin, C.‐S. , Peluso, P. , Sedlazeck, F.J. , Nattestad, M. , Concepcion, G.T. , Clum, A. PubMed PMC

Chinchilla‐Ramírez, M. , Pérez‐Hedo, M. , Pannebakker, B.A. and Urbaneja, A. (2020) Genetic Variation in the Feeding Behavior of Isofemale Lines of PubMed PMC

Chinchilla‐Ramírez, M. , Garzo, E. , Fereres, A. , Gavara‐Vidal, J. , ten Broeke, C.J. , van Loon, J.J.A.

Conway, J.R. , Lex, A. and Gehlenborg, N. (2017) UpSetR: an R package for the visualization of intersecting sets and their properties. Bioinformatics, 33(18), 2938–2940. PubMed PMC

Costechareyre, D. , Balmand, S. , Condemine, G. and Rahbé, Y. (2012) Dickeya dadantii, a plant pathogenic bacterium producing cyt‐like entomotoxins, causes septicemia in the pea aphid PubMed DOI PMC

Dai, X. , Xun, H. , Chang, J. , Zhang, J. , Hu, B. , Li, H.

Dalíková, M. , Zrzavá, M. , Hladová, I. , Nguyen, P. , Šonský, I. , Flegrová, M. PubMed

Dalíková, M. , Zrzavá, M. , Kubíčková, S. and Marec, F. (2017b) W‐enriched satellite sequence in the Indian meal moth, PubMed

De Boer, J.G. , Ode, P.J. , Vet, L.E.M. , Whitfield, J.B. and Heimpel, G.E. (2007) Diploid males sire triploid daughters and sons in the parasitoid wasp PubMed

Doyle, J. and Doyle, J. (1990) Isolation of plant DNA from fresh tissue. Focus, 12(1), 13–15.

Dunning Hotopp, J.C. , Clark, M.E. , Oliveira, D.C.S.G. , Foster, J.M. , Fischer, P. , Muñoz Torres, M.C. PubMed

Ekblom, R. and Wolf, J.B.W. (2014) A field guide to whole‐genome sequencing, assembly and annotation. Evolutionary Applications, 7(7), 1026–1042. PubMed PMC

Ellegren, H. (2014) Genome sequencing and population genomics in non‐model organisms. Trends in Ecology & Evolution, Elsevier Ltd, 29(1), 51–63. PubMed

Frydrychová, R. , Grossmann, P. , Trubac, P. , Vítková, M. and Marec, F. (2004) Phylogenetic distribution of TTAGG telomeric repeats in insects. Genome, 47(1), 163–178. PubMed

Garantonakis, N. , Pappas, M.L. , Varikou, K. , Skiada, V. , Broufas, G.D. , Kavroulakis, N.

Gatto, K.P. , Mattos, J.V. , Seger, K.R. and Lourenço, L.B. (2018) Sex chromosome differentiation in the frog genus PubMed PMC

Gomez‐Rodriguez, V.M. , Rodriguez‐Garay, B. , Palomino, G. , Martínez, J. and Barba‐Gonzalez, R. (2013) Physical mapping of 5S and 18S ribosomal DNA in three species of Agave (Asparagales, Asparagaceae). Comparative Cytogenetics, 7(3), 191–203. PubMed PMC

Grozeva, S. , Kuznetsova, V.G. and Anokhin, B.A. (2011) Karyotypes, male meiosis and comparative FISH mapping of 18S ribosomal DNA and telomeric (TTAGG)n repeat in eight species of true bugs (Hemiptera, Heteroptera). Comparative Cytogenetics, 5(4), 97–116. PubMed PMC

Grozeva, S. , Anokhin, B.A. , Simov, N. and Kuznetsova, V.G. (2019) New evidence for the presence of the telomere motif (TTAGG)n in the family Reduviidae and its absence in the families Nabidae and Miridae (Hemiptera, Cimicomorpha). Comparative Cytogenetics, 13(3), 283–295. PubMed PMC

Gurevich, A. , Saveliev, V. , Vyahhi, N. and Tesler, G. (2013) QUAST: Quality assessment tool for genome assemblies. Bioinformatics, 29(8), 1072–1075. PubMed PMC

Haas, B.J. , Salzberg, S.L. , Zhu, W. , Pertea, M. , Allen, J.E. , Orvis, J. PubMed PMC

Hare, E.E. and Johnston, J.S. (2011) Molecular methods for evolutionary genetics. In: Orgogozo V., and Rockman M.V., (Eds.) Molecular Methods for Evolutionary Genetics. Totowa, NJ: Humana Press, pp. 3–12.

Husnik, F. and McCutcheon, J.P. (2018) Functional horizontal gene transfer from bacteria to eukaryotes. Nature Reviews Microbiology, 16(2), 67–79. PubMed

Itou, M. , Watanabe, M. , Watanabe, E. and Miura, K. (2013) Gut content analysis to study predatory efficacy of

Jang, E.B. and Nishijima, K.A. (1990) Identification and Attractancy of Bacteria Associated with

Jauset, A.M. , Edo‐Tena, E. , Castañé, C. , Agustí, N. , Alomar, O. and Grozeva, S. (2015) Comparative cytogenetic study of three PubMed PMC

Jetybayev, I.Y. , Bugrov, A.G. , Ünal, M. , Buleu, O.G. and Rubtsov, N.B. (2017) Molecular cytogenetic analysis reveals the existence of two independent neo‐XY sex chromosome systems in Anatolian Pamphagidae grasshoppers. BMC Evolutionary Biology, 17(Suppl 1), 1–12. PubMed PMC

Jones, R.N. and Rees, H. (1982) In: B Chromosomes. New York: Academic Press.

Jones, S. , Taylor, G. , Chan, S. , Warren, R. , Hammond, S. , Bilobram, S. PubMed PMC

Jung, S. and Lee, S. (2012) Molecular phylogeny of the plant bugs (Heteroptera: Miridae) and the evolution of feeding habits. Cladistics, 28(1), 50–79. PubMed

Kamber, T. , Smits, T.H.M. , Rezzonico, F. and Duffy, B. (2012) Genomics and current genetic understanding of

Kato, A. , Albert, P.S. , Vega, J.M. and Birchler, J.A. (2006) Sensitive fluorescence PubMed

Keeling, C.I. , Yuen, M.M.S. , Liao, N.Y. , Roderick Docking, T. , Chan, S.K. , Taylor, G.A. PubMed PMC

Keilwagen, J. , Wenk, M. , Erickson, J.L. , Schattat, M.H. , Grau, J. and Hartung, F. (2016) Using intron position conservation for homology‐based gene prediction. Nucleic Acids Research, 44(9), e89. 10.1093/nar/gkw092. PubMed DOI PMC

Kofler, R. , Orozco‐terWengel, P. , de Maio, N. , Pandey, R.V. , Nolte, V. , Futschik, A. PubMed DOI PMC

Kuznetsova, V. , Grozeva, S. , Nokkala, S. and Nokkala, C. (2011) Cytogenetics of the true bug infraorder Cimicomorpha (Hemiptera, Heteroptera): a review. ZooKeys, 154(December), 31–70. PubMed PMC

Lee, W. , Kang, J. , Jung, C. , Hoelmer, K. , Lee, S.H. and Lee, S. (2009) Complete mitochondrial genome of brown marmorated stink bug PubMed

Legeai, F. , Shigenobu, S. , Gauthier, J.P. , Colbourne, J. , Rispe, C. , Collin, O. PubMed PMC

van Lenteren, J.C. , Bolckmans, K. , Köhl, J. , Ravensberg, W.J. and Urbaneja, A. (2018) Biological control using invertebrates and microorganisms: plenty of new opportunities. BioControl, 63(1), 39–59.

Leung, K. , Ras, E. , Ferguson, K.B. , Ariëns, S. , Babendreier, D. , Bijma, P. PubMed DOI PMC

Li, H. , Handsaker, B. , Wysoker, A. , Fennell, T. , Ruan, J. , Homer, N. PubMed PMC

Lindsey, A.R.I. , Werren, J.H. , Richards, S. and Stouthamer, R. (2016) Comparative genomics of a parthenogenesis‐inducing PubMed PMC

Lindsey, A.R.I. , Kelkar, Y.D. , Wu, X. , Sun, D. , Martinson, E.O. , Yan, Z. PubMed PMC

Lowe‐Power, T.M. , Khokhani, D. and Allen, C. (2018) How PubMed

Majoros, W.H. , Pertea, M. and Salzberg, S.L. (2004) TigrScan and GlimmerHMM: Two open source ab initio eukaryotic gene‐finders. Bioinformatics, 20(16), 2878–2879. PubMed

Marçais, G. and Kingsford, C. (2011) A fast, lock‐free approach for efficient parallel counting of occurrences of k‐mers. Bioinformatics, 27(6), 764–770. PubMed PMC

Marec, F. and Shvedov, A.N. (1990) Yellow eye, a new pigment mutation in

Martínez‐García, H. , Román‐Fernández, L.R. , Sáenz‐Romo, M.G. , Pérez‐Moreno, I. and Marco‐Mancebón, V.S. (2016) Optimizing PubMed

May, C.M. , Heuvel, J. , Doroszuk, A. , Hoedjes, K.M. , Flatt, T. and Zwaan, B.J. (2019) Adaptation to developmental diet influences the response to selection on age at reproduction in the fruit fly. Journal of Evolutionary Biology, 32(5), 425–437. PubMed PMC

Mediouni, J. , Fuková, I. , Frydrychová, R. , Marec, F. , Fuková, I. , Marec, F.

Moerkens, R. , Pekas, A. , Bellinkx, S. , Hanssen, I. , Huysmans, M. , Bosmans, L.

Mollá, O. , Biondi, A. , Alonso‐Valiente, M. and Urbaneja, A. (2014) A comparative life history study of two mirid bugs preying on

Morgulis, A. , Gertz, E.M. , Schäffer, A.A. and Agarwala, R. (2006) A fast and symmetric DUST implementation to mask low‐complexity DNA sequences. Journal of Computational Biology, 13(5), 1028–1040. PubMed

Novák, P. , Neumann, P. , Pech, J. , Steinhaisl, J. and MacAs, J. (2013) RepeatExplorer: A Galaxy‐based web server for genome‐wide characterization of eukaryotic repetitive elements from next‐generation sequence reads. Bioinformatics, 29(6), 792–793. PubMed

Panfilio, K.A. and Angelini, D.R. (2018) By land, air, and sea: hemipteran diversity through the genomic lens. Current Opinion in Insect Science, 25, 106–115. PubMed

Panfilio, K.A. , Vargas Jentzsch, I.M. , Benoit, J.B. , Erezyilmaz, D. , Suzuki, Y. , Colella, S. PubMed PMC

Paspati, A. , Ferguson, K.B. , Verhulst, E.C. , Urbaneja, A. , González‐Cabrera, J. and Pannebakker, B.A. (2019) Effect of mass rearing on the genetic diversity of the predatory mite

Pérez‐Hedo, M. and Urbaneja, A. (2016) The zoophytophagous predator

Pérez‐Hedo, M. , Urbaneja‐Bernat, P. , Jaques, J.A. , Flors, V. and Urbaneja, A. (2015) Defensive plant responses induced by

Pérez‐Hedo, M. , Arias‐Sanguino, Á.M. and Urbaneja, A. (2018) Induced tomato plant resistance against PubMed PMC

Pérez‐Hedo, M. , Riahi, C. and Urbaneja, A. (2020) Use of zoophytophagous mirid bugs in horticultural crops: current challenges and future perspectives. Pest Management Science, ps.6043. 77(1), 33–42. PubMed

Pita, S. , Panzera, F. , Mora, P. , Vela, J. , Palomeque, T. and Lorite, P. (2016) The presence of the ancestral insect telomeric motif in kissing bugs (Triatominae) rules out the hypothesis of its loss in evolutionarily advanced Heteroptera (Cimicomorpha). Comparative Cytogenetics, 10(3), 427–437. PubMed PMC

Poelchau, M. , Childers, C. , Moore, G. , Tsavatapalli, V. , Evans, J. , Lee, C.Y. PubMed PMC

Prado, S.S. and Almeida, R.P.P. (2009) Phylogenetic placement of pentatomid stink bug gut symbionts. Current Microbiology, 58(1), 64–69. PubMed

Puentes, A. , Stephan, J.G. and Björkman, C. (2018) A systematic review on the effects of plant‐feeding by omnivorous arthropods: Time to catch‐up with the mirid‐tomato bias? Frontiers in Ecology and Evolution, 6(218). 10.3389/fevo.2018.00218. DOI

Rasmussen, L.B. , Jensen, K. , Sørensen, J.G. , Sverrisdóttir, E. , Nielsen, K.L. , Overgaard, J.

Reddiex, A.J. , Allen, S.L. and Chenoweth, S.F. (2018) A Genomic Reference Panel for PubMed PMC

Richards, S. and Murali, S.C. (2015) Best practices in insect genome sequencing: what works and what doesn't. Current Opinion in Insect Science, 7, 1–7. PubMed PMC

Richards, S. , Gibbs, R.A. , Gerardo, N.M. , Moran, N. , Nakabachi, A. , Stern, D. PubMed PMC

Sachman‐Ruiz, B. and Quiroz‐Castañeda, R.E. (2018) Genomics of Rickettsiaceae: An update. Quiroz‐Castañeda, R.E. , In: Farm Animals Diseases, Recent Omic Trends and New Strategies of Treatment, Vol. I London: InTechOpen, pp. 13.

Sahara, K. , Marec, F. and Traut, W. (1999) TTAGG telomeric repeats in chromosomes of some insects and other arthropods. Chromosome Research, 7(6), 449–460. PubMed

Sanchez, J.A. (2009) Density thresholds for

Santos‐Garcia, D. , Silva, F.J. , Morin, S. , Dettner, K. and Kuechler, S.M. (2017) The all‐rounder PubMed PMC

Schwarz, A. , Medrano‐Mercado, N. , Schaub, G.A. , Struchiner, C.J. , Bargues, M.D. , Levy, M.Z. PubMed PMC

Sember, A. , Bertollo, L.A.C. , Ráb, P. , Yano, C.F. , Hatanaka, T. , de Oliveira, E.A. PubMed PMC

Simão, F.A. , Waterhouse, R.M. , Ioannidis, P. , Kriventseva, E.V. and Zdobnov, E.M. (2015) BUSCO: Assessing genome assembly and annotation completeness with single‐copy orthologs. Bioinformatics, 31(19), 3210–3212. PubMed

Sobreira, T.J.P. , Durham, A.M. and Gruber, A. (2006) TRAP: Automated classification, quantification and annotation of tandemly repeated sequences. Bioinformatics, 22(3), 361–362. PubMed

Sochorová, J. , Garcia, S. , Gálvez, F. , Symonová, R. and Kovařík, A. (2018) Evolutionary trends in animal ribosomal DNA loci: introduction to a new online database. Chromosoma, 127(1), 141–150. PubMed PMC

Streito, J.C. , Clouet, C. , Hamdi, F. and Gauthier, N. (2017) Population genetic structure of the biological control agent PubMed

Sunnucks, P. and Hales, D.F. (1996) Numerous transposed sequences of mitochondrial cytochrome oxidase I‐II in aphids of the genus PubMed

Szűcs, M. , Vercken, E. , Bitume, E.V. and Hufbauer, R.A. (2019) The implications of rapid eco‐evolutionary processes for biological control—a review. Entomologia Experimentalis et Applicata, eea.12807. 167, 598–615.

Testa, A.C. , Hane, J.K. , Ellwood, S.R. and Oliver, R.P. (2015) CodingQuarry: highly accurate hidden Markov model gene prediction in fungal genomes using RNA‐seq transcripts. BMC Genomics, 16(1), 1–12. PubMed PMC

Thomas, G.W.C. , Dohmen, E. , Hughes, D.S.T. , Murali, S.C. , Poelchau, M. , Glastad, K. PubMed PMC

Tian, C. , Tek Tay, W. , Feng, H. , Wang, Y. , Hu, Y. and Li, G. (2015) Characterization of PubMed PMC

Trapnell, C. , Pachter, L. and Salzberg, S.L. (2009) TopHat: discovering splice junctions with RNA‐Seq. Bioinformatics, 25(9), 1105–1111. PubMed PMC

Trapnell, C. , Williams, B.A. , Pertea, G. , Mortazavi, A. , Kwan, G. , van Baren, M.J. PubMed PMC

Traut, W. (1976) Pachytene mapping in the female silkworm, PubMed

Traut, W. , Sahara, K. , Otto, T.D. and Marec, F. (1999) Molecular differentiation of sex chromosomes probed by comparative genomic hybridization. Chromosoma, 108(3), 173–180. PubMed

Traverse, K.L. and Pardue, M.L. (1988) A spontaneously opened ring chromosome of PubMed PMC

Urbaneja, A. , González‐Cabrera, J. , Arnó, J. and Gabarra, R. (2012) Prospects for the biological control of PubMed

Urbaneja‐Bernat, P. , Bru, P. , González‐Cabrera, J. , Urbaneja, A. and Tena, A. (2019) Reduced phytophagy in sugar‐provisioned mirids. Journal of Pest Science, 92(3), 1139–1148.

Vurture, G.W. , Sedlazeck, F.J. , Nattestad, M. , Schatz, M.C. , Gurtowski, J. , Underwood, C.J. PubMed PMC

Weisenfeld, N.I. , Kumar, V. , Shah, P. , Church, D.M. and Jaffe, D.B. (2017) Direct determination of diploid genome sequences. Genome Research, 27, 757–767. PubMed PMC

Wheeler, D. , Redding, A.J. and Werren, J.H. (2013) Characterization of an Ancient Lepidopteran Lateral Gene Transfer. PLoS One, 8(3), e59262. PubMed PMC

van Wilgenburg, E. , Driessen, G. and Beukeboom, L.W. (2006) Single locus complementary sex determination in Hymenoptera: an 'unintelligent' design? Frontiers in Zoology, 3, 1. PubMed PMC

Xu, L. , Dong, Z. , Fang, L. , Luo, Y. , Wei, Z. , Guo, H. PubMed PMC

Xu, P. , Lu, B. , Liu, J. , Chao, J. , Donkersley, P. , Holdbrook, R. PubMed PMC

Xun, H. , Li, H. , Li, S. , Wei, S. , Zhang, L. , Song, F. PubMed DOI PMC

Zhang, Y. and Qiu, S. (2015) Examining phylogenetic relationships of PubMed

Zhou, W. , Rousset, F. and O'Neill, S. (1998) Phylogeny and PCR‐based classification of PubMed PMC

Zrzavá, M. , Hladová, I. , Dalíková, M. , Šíchová, J. , Õunap, E. , Kubíčková, S. PubMed DOI PMC

Zobrazit více v PubMed

figshare
10.6084/m9.figshare.12073893

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...