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Expansion of Imaginal Disc Growth Factor Gene Family in Diptera Reflects the Evolution of Novel Functions

. 2019 Oct 20 ; 10 (10) : . [epub] 20191020

Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic

Document type Journal Article

Grant support
19-13784Y Grantová Agentura České Republiky
INTER-COST no. LTC17073 Czech Republic Ministry of Education, Youth and Sports

Imaginal disc growth factors (IDGFs) are a small protein family found in insects. They are related to chitinases and implicated in multiple functions, including cell growth stimulation, antimicrobial activity, insect hemolymph clotting, and maintenance of the extracellular matrix. A number of new IDGFs have been found in several insect species and their detailed phylogenetic analysis provides a good basis for further functional studies. To achieve this goal, we sequenced Idgf cDNAs from several lepidopteran and trichopteran species and supplemented our data with sequences retrieved from public databases. A comparison of Idgf genes in different species showed that Diptera typically contain several Idgf paralogs with a simple exon-intron structure (2-3 exons), whereas lepidopteran Idgfs appear as a single copy per genome and contain a higher number of exons (around 9). Our results show that, while lepidopteran Idgfs, having single orthologs, are characterized by low divergence and stronger purifying selection over most of the molecule, the duplicated Idgf genes in Diptera, Idgf1 and Idgf4, exhibit signs of positive selection. This characterization of IDGF evolution provides, to our knowledge, the first information on the changes that formed these important molecules.

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Kawamura K., Shibata T., Saget O., Peel D., Bryant P.J. A new family of growth factors produced by the fat body and active on Drosophila imaginal disc cells. Development. 1999;126:211–219. PubMed

Kirkpatrick R.B., Matico R.E., McNulty D.E., Strickler J.E., Rosenb M. An abundantly secreted glycorotein from Drosophila melanogaster is related to mammalian secretory proteins produced in rheumatoid tissues and by activated macrophages. Gene. 1995;153:147–154. doi: 10.1016/0378-1119(94)00756-I. PubMed DOI

Broz V., Kucerova L., Rouhova L., Fleischmannova J., Strnad H., Bryant P.J., Zurovec M. Drosophila imaginal disc growth factor 2 is a trophic factor involved in energy balance, detoxification, and innate immunity. Sci. Rep. 2017;7:43273. doi: 10.1038/srep43273. PubMed DOI PMC

Kucerova L., Broz V., Arefin B., Maaroufi H.O., Hurychova J., Strnad H., Zurovec M., Theopold U. The Drosophila Chitinase-like protein IDGF3 is involved in protection against nematodes and in wound healing. J. Innate Immun. 2016;8:199–210. doi: 10.1159/000442351. PubMed DOI PMC

Pesch Y.Y., Riedel D., Patil K.R., Loch G., Behr M. Chitinases and imaginal disc growth factors organize the extracellular matrix formation at barrier tissues in insects. Sci. Rep. 2016;6:18340. doi: 10.1038/srep18340. PubMed DOI PMC

Shi L., Paskewitz S.M. Identification and molecular characterization of two immune-responsive chitinase-like proteins from Anopheles gambiae. Insect Mol. Biol. 2004;13:387–398. doi: 10.1111/j.0962-1075.2004.00496.x. PubMed DOI

Uraki R., Hastings A.K., Brackney D.E., Armstrong P.M., Fikrig E. AgBR1 antibodies delay lethal Aedes aegypti-borne West Nile virus infection in mice. NPJ Vaccines. 2019;4:23. doi: 10.1038/s41541-019-0120-x. PubMed DOI PMC

Varela P.F., Llera A.S., Mariuzza R.A., Tormo J. Crystal structure of imaginal disc growth factor-2. A member of a new family of growth-promoting glycoproteins from Drosophila melanogaster. J. Biol. Chem. 2002;277:13229–13236. doi: 10.1074/jbc.M110502200. PubMed DOI

Kanost M.R., Zepp M.K., Ladendorff N.E., Andersson L.A. Isolation and characterization of a hemocyte aggregation inhibitor from hemolymph of Manduca sexta larvae. Arch. Insect Biochem. 1994;27:123–136. doi: 10.1002/arch.940270205. PubMed DOI

Pan Y., Lu P., Wang Y., Yin L.J., Ma H.X., Ma G.H., Chen K.P., He Y.Q. In silico identification of novel chitinase-like proteins in the silkworm, Bombyx mori, genome. J. Insect Sci. 2012;12:1–14. doi: 10.1673/031.012.15001. PubMed DOI PMC

Kludkiewicz B., Kucerova L., Konikova T., Strnad H., Hradilova M., Zaloudikova A., Sehadova H., Konik P., Sehnal F., Zurovec M. The expansion of genes encoding soluble silk components in the greater wax moth, Galleria mellonella. Insect Biochem. Mol. Biol. 2019;106:28–38. doi: 10.1016/j.ibmb.2018.11.003. PubMed DOI

Zurovcova M., Tatarenkov A., Berec L. Differences in the pattern of evolution in six physically linked genes of Drosophila melanogaster. Gene. 2006;381:24–33. doi: 10.1016/j.gene.2006.06.011. PubMed DOI

Kucerova L., Zurovec M., Kludkiewicz B., Hradilova M., Strnad H., Sehnal F. Modular structure, sequence diversification and appropriate nomenclature of seroins produced in the silk glands of Lepidoptera. Sci. Rep. 2019;9:3797. doi: 10.1038/s41598-019-40401-3. PubMed DOI PMC

Zurovec M., Yonemura N., Kludkiewicz B., Sehnal F., Kodrik D., Vieira L.C., Kucerova L., Strnad H., Konik P., Sehadova H. Sericin composition in the silk of Antheraea yamamai. Biomacromolecules. 2016;17:1776–1787. doi: 10.1021/acs.biomac.6b00189. PubMed DOI

Grabherr M.G., Haas B.J., Yassour M., Levin J.Z., Thompson D.A., Amit I., Adiconis X., Fan L., Raychowdhury R., Zeng Q.D., et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 2011;29:644–652. doi: 10.1038/nbt.1883. PubMed DOI PMC

Afgan E., Baker D., Batut B., van den Beek M., Bouvier D., Cech M., Chilton J., Clements D., Coraor N., Gruning B.A., et al. The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update. Nucleic Acids Res. 2018;46:W537–W544. doi: 10.1093/nar/gky379. PubMed DOI PMC

Edgar R.C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–1797. doi: 10.1093/nar/gkh340. PubMed DOI PMC

Lefort V., Longueville J.E., Gascuel O. SMS: Smart Model Selection in PhyML. Mol. Biol. Evol. 2017;34:2422–2424. doi: 10.1093/molbev/msx149. PubMed DOI PMC

Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 2013;30:2725–2729. doi: 10.1093/molbev/mst197. PubMed DOI PMC

Guindon S., Dufayard J.F., Lefort V., Anisimova M., Hordijk W., Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst. Biol. 2010;59:307–321. doi: 10.1093/sysbio/syq010. PubMed DOI

Ronquist F., Teslenko M., van der Mark P., Ayres D.L., Darling A., Hohna S., Larget B., Liu L., Suchard M.A., Huelsenbeck J.P. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 2012;61:539–542. doi: 10.1093/sysbio/sys029. PubMed DOI PMC

FigTree, Version 1.4.3. [(accessed on 4 October 2016)]; Available online: http://tree.bio.ed.ac.uk/software/figtree.

Stern A., Doron-Faigenboim A., Erez E., Martz E., Bacharach E., Pupko T. Selecton 2007: Advanced models for detecting positive and purifying selection using a Bayesian inference approach. Nucleic Acids Res. 2007;35:W506–W511. doi: 10.1093/nar/gkm382. PubMed DOI PMC

Doron-Faigenboim A., Stern A., Bacharach E., Pupko T. Selecton: A server for detecting evolutionary forces at a single amino-acid site. Bioinformatics. 2005;21:2101–2103. doi: 10.1093/bioinformatics/bti259. PubMed DOI

Swanson W.J., Nielsen R., Yang Q. Pervasive adaptive evolution in mammalian fertilization proteins. Mol. Biol. Evol. 2003;20:18–20. doi: 10.1093/oxfordjournals.molbev.a004233. PubMed DOI

Pond S.L.K., Frost S.D.W., Muse S.V. HyPhy: Hypothesis testing using phylogenies. Bioinformatics. 2005;21:676–679. doi: 10.1093/bioinformatics/bti079. PubMed DOI

Murrell B., Moola S., Mabona A., Weighill T., Sheward D., Pond S.L.K., Scheffler K. FUBAR: A Fast, Unconstrained Bayesian AppRoximation for Inferring Selection. Mol. Biol. Evol. 2013;30:1196–1205. doi: 10.1093/molbev/mst030. PubMed DOI PMC

Murrell B., Wertheim J.O., Moola S., Weighill T., Scheffler K., Pond S.L.K. Detecting individual sites subject to episodic diversifying selection. PLoS Genet. 2012;8:e1002764. doi: 10.1371/journal.pgen.1002764. PubMed DOI PMC

Pond S.L.K., Murrell B., Fourment M., Frost S.D.W., Delport W., Scheffler K. A Random Effects Branch-Site Model for detecting episodic diversifying seection. Mol. Biol. Evol. 2011;28:3033–3043. doi: 10.1093/molbev/msr125. PubMed DOI PMC

Smith M.D., Wertheim J.O., Weaver S., Murrell B., Scheffler K., Pond S.L.K. Less is more: An Adaptive Branch-Site Random Effects Model for detection of episodic diversifying selection. Mol. Biol. Evol. 2015;32:1342–1353. doi: 10.1093/molbev/msv022. PubMed DOI PMC

Wertheim J.O., Murrell B., Smith M.D., Kosakovsky Pond S.L., Scheffler K. RELAX: Detecting relaxed selection in a phylogenetic framework. Mol. Biol. Evol. 2015;32:820–832. doi: 10.1093/molbev/msu400. PubMed DOI PMC

McClellan D.A., McCracken K.G. Estimating the influence of selection on the variable amino acid sites of the cytochrome B protein functional domains. Mol. Biol. Evol. 2001;18:917–925. doi: 10.1093/oxfordjournals.molbev.a003892. PubMed DOI

Woolley S., Johnson J., Smith M.J., Crandall K.A., McClellan D.A. TreeSAAP: Selection on amino acid properties using phylogenetic trees. Bioinformatics. 2003;19:671–672. doi: 10.1093/bioinformatics/btg043. PubMed DOI

Hoang D.T., Chernmor O., von Haeseler A., Minh B.Q., Vinh L.S. UFBoot2: Improving the Ultrafast Bootstrap Approximation. Mol. Biol. Evol. 2018;35:518–522. doi: 10.1093/molbev/msx281. PubMed DOI PMC

Kalyaanamoorthy S., Minh B.Q., Wong T.K.F., von Haeseler A., Jermiin L.S. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nat. Methods. 2017;14:587–589. doi: 10.1038/nmeth.4285. PubMed DOI PMC

Nguyen L.T., Schmidt H.A., von Haeseler A., Minh B.Q. IQ-TREE: A fast and effective stochastic algorithm for estimating Maximum-Likelihood phylogenies. Mol. Biol. Evol. 2015;32:268–274. doi: 10.1093/molbev/msu300. PubMed DOI PMC

Trifinopoulos J., Nguyen L.T., von Haeseler A., Minh B.Q. W-IQ-TREE: A fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res. 2016;44:W232–W235. doi: 10.1093/nar/gkw256. PubMed DOI PMC

i5K Consortium The i5K Initiative: Advancing arthropod genomics for knowledge, human health, agriculture, and the environment. J. Hered. 2013;104:595–600. doi: 10.1093/jhered/est050. PubMed DOI PMC

Wiegmann B.M., Trautwein M.D., Winkler I.S., Barr N.B., Kim J.W., Lambkin C., Bertone M.A., Cassel B.K., Bayless K.M., Heimberg A.M., et al. Episodic radiations in the fly tree of life. Proc. Natl. Acad. Sci. USA. 2011;108:5690–5695. doi: 10.1073/pnas.1012675108. PubMed DOI PMC

Wahlberg N., Wheat C.W., Pena C. Timing and patterns in the taxonomic diversification of Lepidoptera (butterflies and moths) PLoS ONE. 2013;8:e80875. doi: 10.1371/journal.pone.0080875. PubMed DOI PMC

Nielsen R. Statistical tests of selective neutrality in the age of genomics. Heredity. 2001;86:641–647. doi: 10.1046/j.1365-2540.2001.00895.x. PubMed DOI

Yang Z.H. Inference of selection from multiple species alignments. Curr. Opin. Genet. Dev. 2002;12:688–694. doi: 10.1016/S0959-437X(02)00348-9. PubMed DOI

Misof B., Liu S., Meusemann K., Peters R.S., Donath A., Mayer C., Frandsen P.B., Ware J., Flouri T., Beutel R.G., et al. Phylogenomics resolves the timing and pattern of insect evolution. Science. 2014;346:763–767. doi: 10.1126/science.1257570. PubMed DOI

Jmol: An Open-Source Java Viewer for Chemical Structures in 3D. [(accessed on 23 March 2018)]; Available online: https://www.webcitation.org/getfile?fileid=90d165802e6a28166f4628fb5502a4783e6cf685.

Dolezal T., Gazi M., Zurovec M., Bryant P.J. Genetic analysis of the ADGF multigene family by homologous recombination and gene conversion in Drosophila. Genetics. 2003;165:653–666. PubMed PMC

Gubb D. Intron-Delay and the precision of expression of homeotic gene-products in Drosophila. Dev. Genet. 1986;7:119–131. doi: 10.1002/dvg.1020070302. DOI

Troczka B.J., Richardson E., Homem R.A., Davies T.G.E. An analysis of variability in genome organisation of intracellular calcium release channels across insect orders. Gene. 2018;670:70–86. doi: 10.1016/j.gene.2018.05.075. PubMed DOI PMC

Xi Y., Pan P.L., Ye Y.X., Yu B., Xu H.J., Zhang C.X. Chitinase-like gene family in the brown planthopper, Nilaparvata lugens. Insect Mol. Biol. 2015;24:29–40. doi: 10.1111/imb.12133. PubMed DOI

Omar M.A.A., Ao Y., Li M., He K., Xu L., Tong H., Jiang M., Li F. The functional difference of eight chitinase genes between male and female of the cotton mealybug, Phenacoccus solenopsis. Insect Mol. Biol. 2019;28:550–567. doi: 10.1111/imb.12572. PubMed DOI

Wang H.B., Sakudoh T., Kawasaki H., Iwanaga M., Araki K., Fujimoto H., Takada N., Iwano H., Tsuchida K. Purification and expression analysis of imaginal disc growth factor in the silkworm, Bombyx mori. J. Insect Physiol. 2009;55:1065–1071. doi: 10.1016/j.jinsphys.2009.08.001. PubMed DOI

Tsuzuki S., Iwami M., Sakurai S. Ecdysteroid-inducible genes in the programmed cell death during insect metamorphosis. Insect Biochem. Mol. Biol. 2001;31:321–331. doi: 10.1016/S0965-1748(00)00124-7. PubMed DOI

Asgari S., Schmidt O. Isolation of an imaginal disc growth factor homologue from Pieris rapae and its expression following parasitization by Cotesia rubecula. J. Insect Physiol. 2004;50:687–694. doi: 10.1016/j.jinsphys.2004.05.003. PubMed DOI

Zhang J., Iwai S., Tsugehara T., Takeda M. MbIDGF, a novel member of the imaginal disc growth factor family in Mamestra brassicae, stimulates cell proliferation in two lepidopteran cell lines without insulin. Insect Biochem. Mol. 2006;36:536–546. doi: 10.1016/j.ibmb.2006.04.002. PubMed DOI

Zhu Q.S., Arakane Y., Banerjee D., Beeman R.W., Kramer K.J., Muthukrishnan S. Domain organization and phylogenetic analysis of the chitinase-like family of proteins in three species of insects. Insect Biochem. Mol. 2008;38:452–466. doi: 10.1016/j.ibmb.2007.06.010. PubMed DOI

Gu X., Li Z., Su Y., Zhao Y., Liu L. Imaginal disc growth factor 4 regulates development and temperature adaptation in Bactrocera dorsalis. Sci. Rep. 2019;9:931. doi: 10.1038/s41598-018-37414-9. PubMed DOI PMC

De Gregorio E., Spellman P.T., Rubin G.M., Lemaitre B. Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays. Proc. Natl. Acad. Sci. USA. 2001;98:12590–12595. doi: 10.1073/pnas.221458698. PubMed DOI PMC

Collin M.A., Mita K., Sehnal F., Hayashi C.Y. Molecular evolution of lepidopteran silk proteins: Insights from the ghost moth, Hepialus californicus. J. Mol. Evol. 2010;70:519–529. doi: 10.1007/s00239-010-9349-8. PubMed DOI PMC

Zurovcova M., Ayala F.J. Polymorphism patterns in two tightly linked developmental genes, Idgf1 and Idgf3, of Drosophila melanogaster. Genetics. 2002;162:177–188. PubMed PMC

Li H., Greene L.H. Sequence and structural analysis of the chitinase insertion domain reveals two conserved motifs involved in chitin-binding. PLoS ONE. 2010;5:e8654. doi: 10.1371/journal.pone.0008654. PubMed DOI PMC

Zees A.C., Pyrpassopoulos S., Vorgias C.E. Insights into the role of the (alpha plus beta) insertion in the TIM-barrel catalytic domain, regarding the stability and the enzymatic activity of Chitinase A from Serratia marcescens. BBA Proteins Proteom. 2009;1794:23–31. doi: 10.1016/j.bbapap.2008.09.018. PubMed DOI

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