Transcriptomic data from panarthropods shed new light on the evolution of insulator binding proteins in insects : Insect insulator proteins.
Body plan development in multi-cellular organisms is largely determined by homeotic genes. Expression of homeotic genes, in turn, is partially regulated by insulator binding proteins (IBPs). While only a few enhancer blocking IBPs have been identified in vertebrates, the common fruit fly Drosophila melanogaster harbors at least twelve different enhancer blocking IBPs. We screened recently compiled insect transcriptomes from the 1KITE project and genomic and transcriptomic data from public databases, aiming to trace the origin of IBPs in insects and other arthropods.



Our study shows that the last common ancestor of insects (Hexapoda) already possessed a substantial number of IBPs. Specifically, of the known twelve insect IBPs, at least three (i.e., CP190, Su(Hw), and CTCF) already existed prior to the evolution of insects. Furthermore we found GAF orthologs in early branching insect orders, including Zygentoma (silverfish and firebrats) and Diplura (two-pronged bristletails). Mod(mdg4) is most likely a derived feature of Neoptera, while Pita is likely an evolutionary novelty of holometabolous insects. Zw5 appears to be restricted to schizophoran flies, whereas BEAF-32, ZIPIC and the Elba complex, are probably unique to the genus Drosophila. Selection models indicate that insect IBPs evolved under neutral or purifying selection.



Our results suggest that a substantial number of IBPs either pre-date the evolution of insects or evolved early during insect evolution. This suggests an evolutionary history of insulator binding proteins in insects different to that previously thought. Moreover, our study demonstrates the versatility of the 1KITE transcriptomic data for comparative analyses in insects and other arthropods.
Center of Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, Adenauerallee 160, 51113, Bonn, Germany. s6thpaul@uni-bonn.de.
Thomas
0000-0002-5673-974X
T
Pauli
University of Tübingen, Geschwister-Scholl-Platz, 72074, Tübingen, Germany.
Lucia
L
Vedder
Johannes Gutenberg University Mainz, Institute of Molecular Biology (IMB), Ackermannweg 4, 55128, Mainz, Germany.
Daniel
D
Dowling
Center of Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, Adenauerallee 160, 51113, Bonn, Germany.
Malte
M
Petersen
Center of Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, Adenauerallee 160, 51113, Bonn, Germany.|Department for Evolutionary Biology and Ecology (Institut for Biology I, Zoology), University of Freiburg, Hauptstr. 1, 79104, Freiburg, Germany.|Australian National Insect Collection, CSIRO National Research Collections Australia, Clunies Ross Street, Acton, ACT, 2601, Australia.
Karen
K
Meusemann
Center of Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, Adenauerallee 160, 51113, Bonn, Germany.
Alexander
A
Donath
Zoological Research Museum Alexander Koenig, Arthropod Department, Adenauerallee 160, 53113, Bonn, Germany.
Ralph S
RS
Peters
University of Bonn, Institute of Evolutionary Biology and Ecology, An der Immenburg 1, 53121, Bonn, Germany.
Lars
L
Podsiadlowski
Center of Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, Adenauerallee 160, 51113, Bonn, Germany.
Christoph
C
Mayer
China National GeneBank-Shenzhen, BGI-Shenzhen, Shenzhen, Guangdong Province, 518083, China.|Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Voldgade 5-7, 1350, Copenhagen, Denmark.
Shanlin
S
Liu
Beijing Advanced Innovation Center for Food Nutrition and Human Health, China Agricultural University, Beijing, 100193, China.|College of Food Science and Nutritional Engineering, China Agricultural University, Beijing, 100083, China.
Xin
X
Zhou
University of Cologne, Cologne Biocenter, Institute for Genetics, Zülpicher Straße 47a, 50674, Köln, Germany.
Peter
P
Heger
University of Cologne, Cologne Biocenter, Institute for Genetics, Zülpicher Straße 47a, 50674, Köln, Germany.
Thomas
T
Wiehe
Department of Zoology, University of Kassel, Heinrich-Plett-Str. 40, 34132, Kassel, Germany.
Lars
L
Hering
Department of Zoology, University of Kassel, Heinrich-Plett-Str. 40, 34132, Kassel, Germany.
Georg
G
Mayer
Center of Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, Adenauerallee 160, 51113, Bonn, Germany.
Bernhard
B
Misof
Center of Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, Adenauerallee 160, 51113, Bonn, Germany. oliver.niehuis@gmail.com.
Oliver
O
Niehuis
D000818:Animals; D001181:Arthropods / Q000235:genetics*; D004268:DNA-Binding Proteins / Q000235:genetics*; D004331:Drosophila melanogaster / Q000235:genetics; D004742:Enhancer Elements, Genetic; D019143:Evolution, Molecular; D020869:Gene Expression Profiling; D038101:Insulator Elements; D010802:Phylogeny; D059467:Transcriptome
D004268:DNA-Binding Proteins
Arthropod evolution; Comparative transcriptomic analyses; Gene evolution; Insulator binding proteins