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      The nuclear and mitochondrial genomes of Frieseomelitta varia – a highly eusocial stingless bee (Meliponini) with a permanently sterile worker caste

      research-article
      1 , 2 , 1 , 3 , 1 , 4 , 5 , 1 , 1 , 1 , 6 , 6 , 7 , 8 , 4 , 1 , 4 , 4 , 4 , 1 , 1 , 2 , 8 , 4 , 1 , 1 , 4 , 6 , 6 , 2 , 2 , 6 , , 8 , 8 , 7
      BMC Genomics
      BioMed Central
      Social insect, Meliponini, Illumina sequencing, Genome assembly, Synteny, Repetitive elements, Non-coding RNA, Reproductive process genes, Immunity genes

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          Abstract

          Background

          Most of our understanding on the social behavior and genomics of bees and other social insects is centered on the Western honey bee, Apis mellifera. The genus Apis, however, is a highly derived branch comprising less than a dozen species, four of which genomically characterized. In contrast, for the equally highly eusocial, yet taxonomically and biologically more diverse Meliponini, a full genome sequence was so far available for a single Melipona species only. We present here the genome sequence of Frieseomelitta varia, a stingless bee that has, as a peculiarity, a completely sterile worker caste.

          Results

          The assembly of 243,974,526 high quality Illumina reads resulted in a predicted assembled genome size of 275 Mb composed of 2173 scaffolds. A BUSCO analysis for the 10,526 predicted genes showed that these represent 96.6% of the expected hymenopteran orthologs. We also predicted 169,371 repetitive genomic components, 2083 putative transposable elements, and 1946 genes for non-coding RNAs, largely long non-coding RNAs. The mitochondrial genome comprises 15,144 bp, encoding 13 proteins, 22 tRNAs and 2 rRNAs. We observed considerable rearrangement in the mitochondrial gene order compared to other bees. For an in-depth analysis of genes related to social biology, we manually checked the annotations for 533 automatically predicted gene models, including 127 genes related to reproductive processes, 104 to development, and 174 immunity-related genes. We also performed specific searches for genes containing transcription factor domains and genes related to neurogenesis and chemosensory communication.

          Conclusions

          The total genome size for F. varia is similar to the sequenced genomes of other bees. Using specific prediction methods, we identified a large number of repetitive genome components and long non-coding RNAs, which could provide the molecular basis for gene regulatory plasticity, including worker reproduction. The remarkable reshuffling in gene order in the mitochondrial genome suggests that stingless bees may be a hotspot for mtDNA evolution. Hence, while being just the second stingless bee genome sequenced, we expect that subsequent targeting of a selected set of species from this diverse clade of highly eusocial bees will reveal relevant evolutionary signals and trends related to eusociality in these important pollinators.

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          Most cited references80

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          MRBAYES: Bayesian inference of phylogenetic trees.

          The program MRBAYES performs Bayesian inference of phylogeny using a variant of Markov chain Monte Carlo. MRBAYES, including the source code, documentation, sample data files, and an executable, is available at http://brahms.biology.rochester.edu/software.html.
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            Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads—a baiting and iterative mapping approach

            We present an in silico approach for the reconstruction of complete mitochondrial genomes of non-model organisms directly from next-generation sequencing (NGS) data—mitochondrial baiting and iterative mapping (MITObim). The method is straightforward even if only (i) distantly related mitochondrial genomes or (ii) mitochondrial barcode sequences are available as starting-reference sequences or seeds, respectively. We demonstrate the efficiency of the approach in case studies using real NGS data sets of the two monogenean ectoparasites species Gyrodactylus thymalli and Gyrodactylus derjavinoides including their respective teleost hosts European grayling (Thymallus thymallus) and Rainbow trout (Oncorhynchus mykiss). MITObim appeared superior to existing tools in terms of accuracy, runtime and memory requirements and fully automatically recovered mitochondrial genomes exceeding 99.5% accuracy from total genomic DNA derived NGS data sets in <24 h using a standard desktop computer. The approach overcomes the limitations of traditional strategies for obtaining mitochondrial genomes for species with little or no mitochondrial sequence information at hand and represents a fast and highly efficient in silico alternative to laborious conventional strategies relying on initial long-range PCR. We furthermore demonstrate the applicability of MITObim for metagenomic/pooled data sets using simulated data. MITObim is an easy to use tool even for biologists with modest bioinformatics experience. The software is made available as open source pipeline under the MIT license at https://github.com/chrishah/MITObim.
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              REAPR: a universal tool for genome assembly evaluation

              Methods to reliably assess the accuracy of genome sequence data are lacking. Currently completeness is only described qualitatively and mis-assemblies are overlooked. Here we present REAPR, a tool that precisely identifies errors in genome assemblies without the need for a reference sequence. We have validated REAPR on complete genomes or de novo assemblies from bacteria, malaria and Caenorhabditis elegans, and demonstrate that 86% and 82% of the human and mouse reference genomes are error-free, respectively. When applied to an ongoing genome project, REAPR provides corrected assembly statistics allowing the quantitative comparison of multiple assemblies. REAPR is available at http://www.sanger.ac.uk/resources/software/reapr/.
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                Author and article information

                Contributors
                flaviacpfreitas@gmail.com
                anete.lourenco@ufvjm.edu.br
                francis.nunes@ufscar.br
                paschoal@utfpr.edu.br
                fabiano.biotecnologia@gmail.com
                fabiobarbin@usp.br
                luanabataglia19@gmail.com
                carloscardoso.bio@usp.br
                mario_cervoni@hotmail.com
                saura.silva@unesp.br
                fernanda.04.06@hotmail.com
                dmdl@ufscar.br
                thiago_depintor@usp.br
                kamaferre@gmail.com
                paulinhagoria@gmail.com
                mcjusa@gmail.com
                denysecl@usp.br
                dlunalucena@gmail.com
                limoda@gmail.com
                leonardonascimento1106@gmail.com
                mat.pedrino@gmail.com
                franciene.rabico@gmail.com
                fernandasanches130@gmail.com
                santoseliasdouglas@gmail.com
                cgsbio@gmail.com
                joseanavieira@yahoo.com.br
                barchuk@unifal-mg.edu.br
                klaus@fmrp.usp.br
                zlpsimoe@usp.br
                mmgbit@usp.br
                dgpinheiro@gmail.com
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central (London )
                1471-2164
                3 June 2020
                3 June 2020
                2020
                : 21
                : 386
                Affiliations
                [1 ]GRID grid.11899.38, ISNI 0000 0004 1937 0722, Departamento de Genética, Faculdade de Medicina de Ribeirão Preto, , Universidade de São Paulo, ; Ribeirão Preto, SP Brazil
                [2 ]GRID grid.411180.d, ISNI 0000 0004 0643 7932, Departamento de Biologia Celular e do Desenvolvimento, Instituto de Ciências Biomédicas, , Universidade Federal de Alfenas, ; Alfenas, MG Brazil
                [3 ]GRID grid.411287.9, ISNI 0000 0004 0643 9823, Departamento de Ciências Biológicas, Faculdade de Ciências Biológicas e da Saúde, , Universidade Federal dos Vales do Jequitinhonha e Mucuri, ; Diamantina, MG Brazil
                [4 ]GRID grid.411247.5, ISNI 0000 0001 2163 588X, Departamento de Genética e Evolução, Centro de Ciências Biológicas e da Saúde, , Universidade Federal de São Carlos, ; São Carlos, SP Brazil
                [5 ]GRID grid.474682.b, ISNI 0000 0001 0292 0044, Universidade Tecnológica Federal do Paraná, ; Cornélio Procópio, PR Brazil
                [6 ]GRID grid.11899.38, ISNI 0000 0004 1937 0722, Departamento de Biologia Celular e Molecular e Bioagentes Patogênicos, Faculdade de Medicina de Ribeirão Preto, , Universidade de São Paulo, ; Av. Bandeirantes 3900, Ribeirão Preto, SP 14049-900 Brazil
                [7 ]GRID grid.410543.7, ISNI 0000 0001 2188 478X, Departamento de Tecnologia, Faculdade de Ciências Agrárias e Veterinárias, , Universidade Estadual Paulista “Júlio de Mesquita Filho”, ; Jaboticabal, SP Brazil
                [8 ]GRID grid.11899.38, ISNI 0000 0004 1937 0722, Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, , Universidade de São Paulo, ; Ribeirão Preto, SP Brazil
                Author information
                https://orcid.org/0000-0002-3162-4890
                https://orcid.org/0000-0001-6929-7277
                https://orcid.org/0000-0002-7769-3058
                https://orcid.org/0000-0002-8887-0582
                https://orcid.org/0000-0003-0112-2520
                https://orcid.org/0000-0001-7668-2851
                https://orcid.org/0000-0002-8408-738X
                https://orcid.org/0000-0002-5039-8358
                https://orcid.org/0000-0003-1178-6144
                https://orcid.org/0000-0002-6333-5268
                https://orcid.org/0000-0001-7594-758X
                https://orcid.org/0000-0002-3329-8953
                https://orcid.org/0000-0003-2610-867X
                https://orcid.org/0000-0003-1387-7066
                https://orcid.org/0000-0002-2654-6808
                https://orcid.org/0000-0001-9420-2137
                https://orcid.org/0000-0002-6585-4619
                https://orcid.org/0000-0002-1492-236X
                https://orcid.org/0000-0001-6381-7788
                https://orcid.org/0000-0003-0687-4692
                https://orcid.org/0000-0003-4382-9823
                https://orcid.org/0000-0002-3012-2709
                https://orcid.org/0000-0001-9850-4554
                https://orcid.org/0000-0001-8538-4303
                https://orcid.org/0000-0003-0476-7359
                https://orcid.org/0000-0001-8417-2763
                https://orcid.org/0000-0001-7981-8427
                https://orcid.org/0000-0003-2363-6178
                https://orcid.org/0000-0002-5619-6378
                https://orcid.org/0000-0001-7062-5936
                Article
                6784
                10.1186/s12864-020-06784-8
                7268684
                32493270
                bf2601c9-5d4d-4104-8b39-07be351686b4
                © The Author(s) 2020

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data.

                History
                : 18 November 2019
                : 14 May 2020
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
                Award ID: 454103/2014-0
                Funded by: FundRef http://dx.doi.org/10.13039/501100001807, Fundação de Amparo à Pesquisa do Estado de São Paulo;
                Award ID: 2015/06657-0
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2020

                Genetics
                social insect,meliponini,illumina sequencing,genome assembly,synteny,repetitive elements,non-coding rna,reproductive process genes,immunity genes

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