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Title: Big Genomes Facilitate the Comparative Identification of Regulatory Elements

Journal Article · · PLoS ONE
 [1];  [1];  [2];  [2];  [3];  [3];  [4];  [4];  [5]
  1. Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Genomics Division
  2. Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology
  3. Univ. of Arizona, Tucson, AZ (United States). Dept. of Ecology and Evolutionary Biology
  4. US Dept. of Agriculture (USDA), Hilo, HI (United States). Pacific Basin Agricultrual Research Center
  5. Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Genomics Division; Univ. of California, Berkeley, CA (United States). Howard Hugehes Medical Inst.; Univ. of California, Berkeley, CA (United States). California Inst. of Quantitative Biosciences; Univ. of California, Berkeley, CA (United States). Center for Integrative Genomics

The identification of regulatory sequences in animal genomes remains a significant challenge. Comparative genomic methods that use patterns of evolutionary conservation to identify non-coding sequences with regulatory function have yielded many new vertebrate enhancers. However, these methods have not contributed significantly to the identification of regulatory sequences in sequenced invertebrate taxa. We demonstrate here that this differential success, which is often attributed to fundamental differences in the nature of vertebrate and invertebrate regulatory sequences, is instead primarily a product of the relatively small size of sequenced invertebrate genomes. We sequenced and compared loci involved in early embryonic patterning from four species of true fruit flies (family Tephritidae) that have genomes four to six times larger than those of Drosophila melanogaster. Unlike in Drosophila, where virtually all non-coding DNA is highly conserved, blocks of conserved non-coding sequence in tephritids are flanked by large stretches of poorly conserved sequence, similar to what is observed in vertebrate genomes. We tested the activities of nine conserved non-coding sequences flanking the even-skipped gene of the teprhitid Ceratis capitata in transgenic D. melanogaster embryos, six of which drove patterns that recapitulate those of known D. melanogaster enhancers. In contrast, none of the three non-conserved tephritid non-coding sequences that we tested drove expression in D. melanogaster embryos. Based on the landscape of non-coding conservation in tephritids, and our initial success in using conservation in tephritids to identify D. melanogaster regulatory sequences, we suggest that comparison of tephritid genomes may provide a systematic means to annotate the non-coding portion of the D. melanogaster genome. We also propose that large genomes be given more consideration in the selection of species for comparative genomics projects, to provide increased power to detect functional non-coding DNAs and to provide a less biased view of the evolution and function of animal genomes.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1627369
Journal Information:
PLoS ONE, Vol. 4, Issue 3; ISSN 1932-6203
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English

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Long-Range Regulatory Synergy Is Required to Allow Control of the TAC1 Locus by MEK/ERK Signalling in Sensory Neurones journal January 2010
Evidence for Deep Regulatory Similarities in Early Developmental Programs across Highly Diverged Insects journal August 2014
Quantitative system drift compensates for altered maternal inputs to the gap gene network of the scuttle fly Megaselia abdita journal January 2015
Molecular Techniques for the Detection and Differentiation of Host and Parasitoid Species and the Implications for Fruit Fly Management journal August 2012
Assessing Computational Methods of Cis-Regulatory Module Prediction journal December 2010
Hox gene Ultrabithorax regulates distinct sets of target genes at successive stages of Drosophila haltere morphogenesis journal January 2011
Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence journal December 2011
The gap gene network journal October 2010
The draft genome of the pest tephritid fruit fly Bactrocera tryoni: resources for the genomic analysis of hybridising species journal January 2014
Conserved noncoding elements and the evolution of animal body plans journal July 2009
Sex and the single embryo: early deveopment in the Mediterranean fruit fly, Ceratitis capitata journal January 2010
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