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

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          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.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12915-016-0321-y) contains supplementary material, which is available to authorized users.

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          Most cited references65

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          Top 10 plant viruses in molecular plant pathology.

          Many scientists, if not all, feel that their particular plant virus should appear in any list of the most important plant viruses. However, to our knowledge, no such list exists. The aim of this review was to survey all plant virologists with an association with Molecular Plant Pathology and ask them to nominate which plant viruses they would place in a 'Top 10' based on scientific/economic importance. The survey generated more than 250 votes from the international community, and allowed the generation of a Top 10 plant virus list for Molecular Plant Pathology. The Top 10 list includes, in rank order, (1) Tobacco mosaic virus, (2) Tomato spotted wilt virus, (3) Tomato yellow leaf curl virus, (4) Cucumber mosaic virus, (5) Potato virus Y, (6) Cauliflower mosaic virus, (7) African cassava mosaic virus, (8) Plum pox virus, (9) Brome mosaic virus and (10) Potato virus X, with honourable mentions for viruses just missing out on the Top 10, including Citrus tristeza virus, Barley yellow dwarf virus, Potato leafroll virus and Tomato bushy stunt virus. This review article presents a short review on each virus of the Top 10 list and its importance, with the intent of initiating discussion and debate amongst the plant virology community, as well as laying down a benchmark, as it will be interesting to see in future years how perceptions change and which viruses enter and leave the Top 10. © 2011 The Authors. Molecular Plant Pathology © 2011 BSPP and Blackwell Publishing Ltd.
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            Estimating maximum likelihood phylogenies with PhyML.

            Our understanding of the origins, the functions and/or the structures of biological sequences strongly depends on our ability to decipher the mechanisms of molecular evolution. These complex processes can be described through the comparison of homologous sequences in a phylogenetic framework. Moreover, phylogenetic inference provides sound statistical tools to exhibit the main features of molecular evolution from the analysis of actual sequences. This chapter focuses on phylogenetic tree estimation under the maximum likelihood (ML) principle. Phylogenies inferred under this probabilistic criterion are usually reliable and important biological hypotheses can be tested through the comparison of different models. Estimating ML phylogenies is computationally demanding, and careful examination of the results is warranted. This chapter focuses on PhyML, a software that implements recent ML phylogenetic methods and algorithms. We illustrate the strengths and pitfalls of this program through the analysis of a real data set. PhyML v3.0 is available from (http://atgc_montpellier.fr/phyml/).
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              Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes.

              Although common among bacteria, lateral gene transfer-the movement of genes between distantly related organisms-is thought to occur only rarely between bacteria and multicellular eukaryotes. However, the presence of endosymbionts, such as Wolbachia pipientis, within some eukaryotic germlines may facilitate bacterial gene transfers to eukaryotic host genomes. We therefore examined host genomes for evidence of gene transfer events from Wolbachia bacteria to their hosts. We found and confirmed transfers into the genomes of four insect and four nematode species that range from nearly the entire Wolbachia genome (>1 megabase) to short (<500 base pairs) insertions. Potential Wolbachia-to-host transfers were also detected computationally in three additional sequenced insect genomes. We also show that some of these inserted Wolbachia genes are transcribed within eukaryotic cells lacking endosymbionts. Therefore, heritable lateral gene transfer occurs into eukaryotic hosts from their prokaryote symbionts, potentially providing a mechanism for acquisition of new genes and functions.
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                Author and article information

                Contributors
                bill.wintermantel@ars.usda.gov
                kai.ling@ars.usda.gov
                zf25@cornell.edu
                Journal
                BMC Biol
                BMC Biol
                BMC Biology
                BioMed Central (London )
                1741-7007
                14 December 2016
                14 December 2016
                2016
                : 14
                : 110
                Affiliations
                [1 ]Boyce Thompson Institute, Cornell University, Ithaca, NY 14853 USA
                [2 ]US Department of Agriculture-Agricultural Research Service, US Vegetable Laboratory, Charleston, SC 29414 USA
                [3 ]US Department of Agriculture-Agricultural Research Service, Crop Improvement and Protection Research, Salinas, CA 93905 USA
                [4 ]Department of Entomology, The Volcani Center, Bet Dagan, 50250 Israel
                [5 ]EMBRAPA Rice and Beans, Santo Antônio de Goiás, GO 75375-000 Brazil
                [6 ]Department of Entomology, Cornell University, Ithaca, NY 14853 USA
                [7 ]Department of Biology, Lund University, Lund, SE-223 62 Sweden
                [8 ]Department of Plant Pathology and Plant-Microbe Biology, Cornell University, Ithaca, NY 14853 USA
                [9 ]Department of Plant Sciences, The University of Arizona, Tucson, AZ 85721 USA
                [10 ]Department of Microbiology, Immunology and Biochemistry, University of Tennessee Health Science Center, Memphis, TN 38163 USA
                [11 ]US Department of Agriculture-Agricultural Research Service, US Horticultural Laboratory, Fort Pierce, FL 34945 USA
                [12 ]US Department of Agriculture-Agricultural Research Service, Robert W. Holley Center for Agriculture and Health, Ithaca, NY 14853 USA
                Author information
                http://orcid.org/0000-0001-9684-1450
                Article
                321
                10.1186/s12915-016-0321-y
                5157087
                27974049
                2222286f-1f4d-4a3c-bba8-deef9c594390
                © Chen et al. 2016

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 2 September 2016
                : 28 October 2016
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000200, United States Agency for International Development;
                Award ID: IDOELPAG4799
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000154, Division of Integrative Organismal Systems;
                Award ID: IDOEZQAG4800
                Award ID: IDEOJUAG4801
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100005825, National Institute of Food and Agriculture;
                Award ID: IDOEFXAG4803
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100003977, Israel Science Foundation;
                Award ID: IDOERYAG4804
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2016

                Life sciences
                whitefly,bemisia tabaci,draft genome,virus transmission,polyphagy,insecticide resistance
                Life sciences
                whitefly, bemisia tabaci, draft genome, virus transmission, polyphagy, insecticide resistance

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