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Funding for the project was provided by a grant to RG from the National Human Genome Research Institute, National Institutes of Health (NHGRI, NIH) U54 HG003273. Contributions from members of the CGE lab were supported by Agriculture and Food Research Initiative Competitive grant no. 2010-65205-20407 from the USDA National Institute of Food Agriculture. AKB was supported by a Clare Luce Booth Fellowship at Georgetown University. The authors are grateful for the HGSC sequence production teams (Patil, S., Gubbala, S., Aqrawi, P., Arias, F., Bess, C., Blankenburg, K. B., Brocchini, M., Buhay, C., Challis, D., Chang, K., Chen, D., Coleman, P., Drummond, J., English, A., Evani, U., Francisco, L., Fu, Q., Goodspeed, R., Haessly, T. H., Hale, W., Han, H., Holder, M., Hu, Y., Jackson, L., Jakkamsetti, A., Jayaseelan, J. C., Kakkar, N., Kalra, D., Kandadi, H., Lee, S., Li, H., Liu, Y., Macmil, S., Mandapat, C. M., Mata, R., Mathew, T., Matskevitch, T., Munidasa, M., Nagaswamy, U., Najjar, R., Nguyen, N., Niu, J., Opheim, D., Palculict, T., Paul, S., Pellon, M., Perales, L., Pham, C., Pham, P., Pu, L.-L., Qi, S., Qu, J., Ren, Y., Ruth, R.T., Saada, N., Sabo, A., San Lucas, F., Sershen, C., Shafer, J., Shah, N., Shelton, R., Song, X.-Z., Tabassum, N., Tang, L., Taylor, A., Taylor, M., Velamala, V., Wan, Z., Wang, L., Wang, Y., Warren, J., Weissenberger, G., Wilczek-Boney, K. B., Yao, J., Yin, B., Yu, J., Zhang, J., Zhang, L., Zhou, C., Zhu, D., Zhu, Y., and Zou, X.), and the input of other members of the HGSC genome assembly team.

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Article

Finding the missing honey bee genes: lessons learned from a genome upgrade

Publicated to:Bmc Genomics. 15 86- - 2014-01-30 15(), DOI: 10.1186/1471-2164-15-86

Authors: Elsik, CG; Worley, KC; Bennett, AK; Beye, M; Camara, F; Childers, CP; de Graaf, DC; Debyser, G; Deng, JX; Devreese, B; Elhaik, E; Evans, JD; Foster, LJ; Graur, D; Guigo, R; Hoff, KJ; Holder, ME; Hudson, ME; Hunt, GJ; Jiang, HY; Joshi, V; Khetani, RS; Kosarev, P; Kovar, CL; Ma, J; Maleszka, R; Moritz, RFA; Munoz-Torres, MC; Murphy, TD; Muzny, DM; Newsham, IF; Reese, JT; Robertson, HM; Robinson, GE; Rueppell, O; Solovyev, V; Stanke, M; Stolle, E; Tsuruda, JM; Van Vaerenbergh, M; Waterhouse, RM; Weaver, DB; Whitfield, CW; Wu, YQ; Zdobnov, EM; Zhang, L; Zhu, DH; Gibbs, RA

Affiliations

Abstract

The first generation of genome sequence assemblies and annotations have had a significant impact upon our understanding of the biology of the sequenced species, the phylogenetic relationships among species, the study of populations within and across species, and have informed the biology of humans. As only a few Metazoan genomes are approaching finished quality (human, mouse, fly and worm), there is room for improvement of most genome assemblies. The honey bee (Apis mellifera) genome, published in 2006, was noted for its bimodal GC content distribution that affected the quality of the assembly in some regions and for fewer genes in the initial gene set (OGSv1.0) compared to what would be expected based on other sequenced insect genomes.Here, we report an improved honey bee genome assembly (Amel_4.5) with a new gene annotation set (OGSv3.2), and show that the honey bee genome contains a number of genes similar to that of other insect genomes, contrary to what was suggested in OGSv1.0. The new genome assembly is more contiguous and complete and the new gene set includes ~5000 more protein-coding genes, 50% more than previously reported. About 1/6 of the additional genes were due to improvements to the assembly, and the remaining were inferred based on new RNAseq and protein data.Lessons learned from this genome upgrade have important implications for future genome sequencing projects. Furthermore, the improvements significantly enhance genomic resources for the honey bee, a key model for social behavior and essential to global ecology through pollination.

Keywords

AnnotationApis melliferaApis-melliferaClassification-systemDomain databaseDraft genomeEvolutionExpressionFamiliesGc contentGene annotationGene predictionGenome assemblyGenome improvementGenome sequencingRepetitive dnaSequenceTandem repeatsTranscriptome

Quality index

Bibliometric impact. Analysis of the contribution and dissemination channel

The work has been published in the journal Bmc Genomics due to its progression and the good impact it has achieved in recent years, according to the agency WoS (JCR), it has become a reference in its field. In the year of publication of the work, 2014, it was in position 26/163, thus managing to position itself as a Q1 (Primer Cuartil), in the category Biotechnology & Applied Microbiology.

From a relative perspective, and based on the normalized impact indicator calculated from World Citations provided by WoS (ESI, Clarivate), it yields a value for the citation normalization relative to the expected citation rate of: 7.5. This indicates that, compared to works in the same discipline and in the same year of publication, it ranks as a work cited above average. (source consulted: ESI Nov 14, 2024)

This information is reinforced by other indicators of the same type, which, although dynamic over time and dependent on the set of average global citations at the time of their calculation, consistently position the work at some point among the top 50% most cited in its field:

  • Field Citation Ratio (FCR) from Dimensions: 33.76 (source consulted: Dimensions May 2025)

Specifically, and according to different indexing agencies, this work has accumulated citations as of 2025-05-31, the following number of citations:

  • WoS: 312
  • Europe PMC: 198
  • OpenCitations: 361

Impact and social visibility

From the perspective of influence or social adoption, and based on metrics associated with mentions and interactions provided by agencies specializing in calculating the so-called "Alternative or Social Metrics," we can highlight as of 2025-05-31:

  • The use, from an academic perspective evidenced by the Altmetric agency indicator referring to aggregations made by the personal bibliographic manager Mendeley, gives us a total of: 383.
  • The use of this contribution in bookmarks, code forks, additions to favorite lists for recurrent reading, as well as general views, indicates that someone is using the publication as a basis for their current work. This may be a notable indicator of future more formal and academic citations. This claim is supported by the result of the "Capture" indicator, which yields a total of: 382 (PlumX).

With a more dissemination-oriented intent and targeting more general audiences, we can observe other more global scores such as:

  • The Total Score from Altmetric: 29.9.
  • The number of mentions on the social network Facebook: 2 (Altmetric).
  • The number of mentions on the social network X (formerly Twitter): 19 (Altmetric).

It is essential to present evidence supporting full alignment with institutional principles and guidelines on Open Science and the Conservation and Dissemination of Intellectual Heritage. A clear example of this is:

  • The work has been submitted to a journal whose editorial policy allows open Open Access publication.

Leadership analysis of institutional authors

This work has been carried out with international collaboration, specifically with researchers from: Australia; Belgium; Canada; Germany; Saudi Arabia; Switzerland; Timor-Leste; United States of America.