Skip to main content Accessibility help
×
Home

Functional genome annotation of Drosophila seminal fluid proteins using transcriptional genetic networks

  • JULIEN F. AYROLES (a1) (a2), BROOKE A. LAFLAMME (a3), ERIC A. STONE (a1) (a2), MARIANA F. WOLFNER (a3) and TRUDY F. C. MACKAY (a1) (a2)...

Summary

Predicting functional gene annotations remains a significant challenge, even in well-annotated genomes such as yeast and Drosophila. One promising, high-throughput method for gene annotation is to use correlated gene expression patterns to annotate target genes based on the known function of focal genes. The Drosophila melanogaster transcriptome varies genetically among wild-derived inbred lines, with strong genetic correlations among the transcripts. Here, we leveraged the genetic correlations in gene expression among known seminal fluid protein (SFP) genes and the rest of the genetically varying transcriptome to identify 176 novel candidate SFPs (cSFPs). We independently validated the correlation in gene expression between seven of the cSFPs and a known SFP gene, as well as expression in male reproductive tissues. We argue that this method can be extended to other systems for which information on genetic variation in gene expression is available.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Functional genome annotation of Drosophila seminal fluid proteins using transcriptional genetic networks
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Functional genome annotation of Drosophila seminal fluid proteins using transcriptional genetic networks
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Functional genome annotation of Drosophila seminal fluid proteins using transcriptional genetic networks
      Available formats
      ×

Copyright

Corresponding author

*Corresponding author: North Carolina State University, Raleigh, NC, USA.

References

Hide All
Alonso, J. M., Stepanova, A. N., Leisse, T. J., Kim, C. J., Chen, H., Shinn, P., Stevenson, D. K., Zimmerman, J., Barajas, P., Cheuk, R., Gadrinab, C., Heller, C., Jeske, A., Koesema, E., Meyers, C. C., Parker, H., Prednis, L., Ansari, Y., Choy, N., Deen, H., Geralt, M., Hazari, N., Hom, E., Karnes, M., Mulholland, C., Ndubaku, R., Schmidt, I., Guzman, P., Aguilar-Henonin, L., Schmid, M., Weigel, D., Carter, D. E., Marchand, T., Risseeuw, E., Brogden, D., Zeko, A., Crosby, W. L., Berry, C. C. & Ecker, J. R. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653657.
Aravind, L. (2000). Guilt by association: contextual information in genome analysis. Genome Research 10, 10741077.
Ayroles, J. F., Carbone, M. A., Stone, E. A., Jordan, K. W., Lyman, R. F., Magwire, M. M., Rollmann, S. M., Duncan, L. H., Lawrence, F., Anholt, R. R. H. & Mackay, T. F. C. (2009). Systems genetics of complex traits in Drosophila melanogaster. Nature Genetics 41, 299307.
Bellen, H. J., Levis, R. W., Liao, G., He, Y., Carlson, J. W., Tsang, G., Evans-Holm, M., Hiesinger, P. R., Schulze, K. L., Rubin, G. M., Hoskins, R. A. & Spradling, A. C. (2004). The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes. Genetics 67, 761781.
Bertuccioli, C., Fasano, L., Jun, S., Wang, S., Sheng, G. & Desplan, C. (1996). In vivo requirement for the paired domain and homeodomain of the paired segmentation gene product. Development 122, 26732685.
Bréhélin, L., Florent, I., Gascuel, O. & Maréchal, E. (2010). Assessing functional annotation transfers with inter-species conserved coexpression: application to Plasmodium falciparum. BMC Genomics 11, 35.
Carvalho, G. B., Kapahi, P., Anderson, D. J. & Benzer, S. (2006). Allocrine modulation of feeding behavior by the sex peptide of Drosophila. Current Biology 16, 692696.
Chapman, T., Bangham, J., Vinti, G., Seifried, B., Lung, O., Wolfner, M. F., Smith, H. K. & Partridge, L. (2003). The sex peptide of Drosophila melanogaster: female post-mating responses analyzed by using RNA interference. Proceedings of the National Academy of Sciences USA 100, 99239928.
Chintapalli, V. R., Wang, J. & Dow, J. A. (2007). Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nature Genetics 39, 715720.
Costello, J. C., Dalkilic, M. M., Beason, S. M., Gehlhausen, J. R., Patwardhan, R., Middha, S., Eads, B. D. & Andrews, J. R. (2009). Gene networks in Drosophila melanogaster: integrating experimental data to predict gene function. Genome Biology 10, R97.
Dietzl, G., Chen, D., Schnorrer, F., Su, K. C., Barinova, Y., Fellner, M., Gasser, B., Kinsey, K., Oppel, S., Scheiblauer, S., Couto, A., Marra, V., Keleman, K. & Dickson, B. J. (2007). A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448, 151156.
Dowell, R. D., Ryan, O., Jansen, A., Cheung, D., Agarwala, S., Danford, T., Bernstein, D. A., Rolfe, P. A., Heisler, L. E., Chin, B., Nislow, C., Giaever, G., Phillips, P. C., Fink, G. R., Gifford, D. K. & Boone, C. (2010). Genotype to phenotype: a complex problem. Science 328, 469.
Emanuelsson, O., Brunak, S., von Heijne, G. & Nielsen, H. (2007). Locating proteins in the cell using TargetP, SignalP and related tools. Nature Protocols 2, 953971.
Findlay, G. D., MacCoss, M. J. & Swanson, W. J. (2009). Proteomic discovery of previously unannotated, rapidly evolving seminal fluid genes in Drosophila. Genome Research 19, 886896.
Findlay, G. D., Yi, X., Maccoss, M. J. & Swanson, W. J. (2008). Proteomics reveals novel Drosophila seminal fluid proteins transferred at mating. Public Library of Science Biology 6, e178.
Flint, J. & Mackay, T. F. C. (2009). Genetic architecture of quantitative traits in mice, flies, and humans. Genome Research 19, 723733.
Guan, C., Ye, C., Yang, X. & Gao, J. (2010). A review of current large-scale mouse knockout efforts. Genesis 48, 7385.
Heifetz, Y., Lung, O., Frongillo, E. A. Jr. & Wolfner, M. F. (2000). The Drosophila seminal fluid protein Acp26Aa stimulates release of oocytes by the ovary. Current Biology 10, 99–102.
Hrmova, M. & Fincher, G. B. (2009). Functional genomics and structural biology in the definition of gene function. Methods in Molecular Biology 513, 199227.
Huang, D. W., Sherman, B. T. & Lempicki, R. A. (2009). Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nature Protocols 4, 4457.
Isaac, R. E., Li, C., Leedale, A. E. & Shirras, A. D. (2010). Drosophila male sex peptide inhibits siesta sleep and promotes locomotor activity in the post-mated female. Proceedings of the Biological Sciences 277, 6570.
Kamath, R. S. & Ahringer, J. (2003). Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30, 313321.
Kilchherr, E., Schumaker, V. N., Phillips, M. L. & Curtiss, L. K. (1986). Activation of the first component of human complement, C1, by monoclonal antibodies directed against different domains of subcomponent C1q. Journal of Immunology 137, 255262.
Klie, S., Nikoloski, Z. & Selbig, J. (2010). Biological cluster evaluation for gene function prediction. Journal of Computational Biology (Epublication ahead of print).
Langfelder, P. & Horvath, S. (2007). Eigengene networks for studying the relationships between co-expression modules. BMC Systems Biology 1, 54.
Liu, H. & Kubli, E. (2003). Sex-peptide is the molecular basis of the sperm effect in Drosophila melanogaster. Proceedings of the National Academy of Sciences USA 100, 99299933.
Luo, F., Yang, Y., Zhong, J., Gao, H., Khan, L., Thompson, D. K. & Zhou, J. (2007). Constructing gene co-expression networks and predicting functions of unknown genes by random matrix theory. BMC Bioinformatics 8, 299.
Mackay, T. F. C., Stone, E. A. & Ayroles, J. F. (2009). The genetics of quantitative traits: challenges and prospects. Nature Reviews Genetics 10, 565677.
Miozzi, L., Piro, R. M., Rosa, F., Ala, U., Silengo, L., Di Cunto, F. & Provero, P. (2008). Functional annotation and identification of candidate disease genes by computational analysis of normal tissue gene expression data. Public Library of Science One 6, e2439.
Neubaum, D. M. & Wolfner, M. F. (1999). Wise, winsome, or weird? Mechanisms of sperm storage in female animals. Current Topics in Developmental Biology 41, 6797.
Ni, J. Q., Liu, L. P., Binari, R., Hardy, R., Shim, H. S., Cavallaro, A., Booker, M., Pfeiffer, B. D., Markstein, M., Wang, H., Villalta, C., Laverty, T. R., Perkins, L. A. & Perrimon, N. (2009). A Drosophila resource of transgenic RNAi lines for neurogenetics. Genetics 182, 10891100.
Nüsslein-Volhard, C. & Wieschaus, E. (1980). Mutations affecting segment number and polarity in Drosophila. Nature 287, 795801.
Peña-Castillo, L. & Hughes, T. R. (2007). Why are there still over 1000 uncharacterized yeast genes? Genetics 176, 7–14.
Ravi Ram, K. & Wolfner, M. F. (2007). Seminal influences: Drosophila ACPs and the molecular interplay between males and females during reproduction. Integrative and Comparative Biology 47, 427445.
Ravi Ram, K. & Wolfner, M. F. (2009). A network of interactions among seminal proteins underlies the long-term postmating response in Drosophila. Proceedings of the National Academy of Sciences USA 106, 1538415389.
Reverter, A., Ingham, A. & Dalrymple, B. P. (2008). Mining tissue specificity, gene connectivity and disease association to reveal a set of genes that modify the action of disease causing genes. BioData Mining 1, 8.
Saudan, P., Hauck, K., Soller, M., Choffat, Y., Ottiger, M., Spörri, M., Ding, Z., Hess, D., Gehrig, P. M., Klauser, S., Hunziker, P. & Kubli, E. (2002). Ductus ejaculatorius peptide 99B (DUP99B), a novel Drosophila melanogaster sex-peptide pheromone. European Journal of Biochemistry 269, 989997.
Spirek, M., Benko, Z., Carnecka, M., Rumpf, C., Cipak, L., Batova, M., Marova, I., Nam, M., Kim, D. U., Park, H. O., Hayles, J., Hoe, K. L., Nurse, P. & Gregan, J. (2010). S. pombe genome deletion project: an update. Cell Cycle 9, 23992402.
Stone, E. A. & Ayroles, J. F. (2009). Modulated modularity clustering as an exploratory tool for functional genomic inference. Public Library of Science Genetics 5, e1000479.
Swanson, W. J., Clark, A. G., Waldrip-Dail, H. M., Wolfner, M. F. & Aquadro, C. F. (2001). Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila. Proceedings of the National Academy of Sciences USA 98, 73757379.
Tram, U. & Wolfner, M. F. (1999). Male seminal fluid proteins are essential for sperm storage in Drosophila melanogaster. Genetics 153, 837844.
Vandepoele, K., Quimbaya, M., Casneuf, T., De Veylder, L. & Van de Peer, Y. (2009). Unraveling transcriptional control in Arabidopsis using cis-regulatory elements and coexpression networks. Plant Physiology 150, 535546.
Walker, M. G., Volkmuth, W., Sprinzak, E., Hodgson, D. & Klingler, T. (1999). Prediction of gene function by genome-scale expression analysis: prostate cancer-associated genes. Genome Research 9, 11981203.
Winzeler, E. A., Shoemaker, D. D., Astromoff, A., Liang, H., Anderson, K., Andre, B., Bangham, R., Benito, R., Boeke, J. D., Bussey, H., Chu, A. M., Connelly, C., Davis, K., Dietrich, F., Dow, S. W., El Bakkoury, M., Foury, F., Friend, S. H., Gentalen, E., Giaever, G., Hegemann, J. H., Jones, T., Laub, M., Liao, H., Liebundguth, N., Lockhart, D. J., Lucau-Danila, A., Lussier, M., M'Rabet, N., Menard, P., Mittmann, M., Pai, C., Rebischung, C., Revuelta, J. L., Riles, L., Roberts, C. J., Ross-MacDonald, P., Scherens, B., Snyder, M., Sookhai-Mahadeo, S., Storms, R. K., Véronneau, S., Voet, M., Volckaert, G., Ward, T. R., Wysocki, R., Yen, G. S., Yu, K., Zimmermann, K., Philippsen, P., Johnston, M. & Davis, R. W. (1999). Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285, 901906.
Wolfner, M. F. (2009). Battle and ballet: molecular interactions between the sexes in Drosophila. Journal of Heredity 100, 399410.
Xue, L. & Noll, M. (1996). The functional conservation of proteins in evolutionary alleles and the dominant role of enhancers in evolution. European Molecular Biology Organization Journal 15, 37223731.
Xue, L. & Noll, M. (2000). Drosophila female sexual behavior induced by sterile males showing copulation complementation. Proceedings of the National Academy of Sciences USA 97, 32723275.
Xue, L. & Noll, M. (2002). Dual role of the Pax gene paired in accessory gland development of Drosophila. Development 129, 339346.
Type Description Title
EXCEL
Supplementary materials

Ayroles Supplementary Material
Table.xls

 Excel (814 KB)
814 KB
EXCEL
Supplementary materials

Ayroles Supplementary Material
Table.xls

 Excel (127 KB)
127 KB

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed