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Conservation of gene architecture and domains amidst sequence divergence in the hsrω lncRNA gene across the Drosophila genus: an in silico analysis

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Abstract

The developmentally active and cell-stress responsive hsrω locus in Drosophila melanogaster carries two exons, one omega intron, one short translatable open reading frame (ORFω), long stretch of unique tandem repeats and an overlapping mir-4951 near its 3′ end. It produces multiple long noncoding RNAs (lncRNAs) using two transcription start and four termination sites. Earlier cytogenetic studies revealed functional conservation of hsrω in several Drosophila species. However, sequence analysis in three species showed poor conservation for ORFω, tandem repeat and other regions while the 16 nt at 5′ and 60 nt at 3′ splice junctions of the omega intron, respectively, were found to be ultra-conserved. The present bioinformatic study using the splice-junction landmarks in D. melanogaster hsrω identified orthologues in publicly available 34 Drosophila species genomes. Each orthologue carries a short ORFω, ultra-conserved splice junctions of omega intron, repeat region, conserved 3′-end located at mir-4951, and syntenic neighbours. Multiple copies of conserved nonamer motifs are seen in the tandem repeat region, despite a high variability in the repeat sequences. Intriguingly, only the omega intron sequences in different species show evolutionary relationships matching the general phylogenetic history in the genus. Search in other known insect genomes did not reveal sequence homology although a locus with similar functional properties is suggested in Chironomus and Ceratitis genera. Amidst the high sequence divergence, the conserved organization of exons, ORFω and omega intron in this gene’s proximal part and tandem repeats in distal part across the Drosophila genus is remarkable and possibly reflects functional importance of higher order structure of hsrω lncRNAs and the small omega peptide.

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References

  • Anastasiadou E., Jacob L. S. and Slack F. J. 2018 Non-coding RNA networks in cancer. Nat. Rev. Cancer 18, 5.

    CAS  PubMed  Google Scholar 

  • Anderson A. R., Collinge J. E., Hoffmann A. A., Kellett M. and McKechnie S. W. 2003 Thermal tolerance trade-offs associated with the right arm of chromosome 3 and marked by the hsr-omega gene in Drosophila melanogaster. Heredity 90, 195–202.

    CAS  PubMed  Google Scholar 

  • Ashburner M. and Bonner J. J. 1979 The induction of gene activity in Drosophilia by heat shock. Cell 17, 241–254.

    CAS  PubMed  Google Scholar 

  • Aurora R. and Rosee G. D. 1998 Helix capping. Protein Sci. 7, 21–38.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Aurora R., Srinivasan R. and Rose G. D. 1994 Rules for alpha-helix termination by glycine. Science 264, 1126–1130.

    CAS  PubMed  Google Scholar 

  • Baeriswyl S., Gan B. H., Siriwardena T. N., Visini R., Robadey M., Javor S. et al. 2019 X-ray crystal structures of short antimicrobial peptides as Pseudomonas aeruginosa lectin B complexes. ACS Chem. Biol. 14, 758–766.

    CAS  PubMed  Google Scholar 

  • Bai Y., Casola C., Feschotte C. and Betran E. 2007 Comparative genomics reveals a constant rate of origination and convergent acquisition of functional retrogenes in Drosophila. Genome Biol. 8, R11.

    PubMed  PubMed Central  Google Scholar 

  • Bendena W. G., Garbe J. C., Traverse K. L., Lakhotia S. C. and Pardue M. L. 1989 Multiple inducers of the Drosophila heat shock locus 93D (hsr omega): inducer-specific patterns of the three transcripts. J. Cell Biol. 108, 2017–2028.

    CAS  PubMed  Google Scholar 

  • Bendena W. G., Ayme-Southgate A., Garbe J. C. and Pardue M. L. 1991 Expression of heat-shock locus hsr-omega in nonstressed cells during development in Drosophila melanogaster. Dev. Biol. 144, 65–77.

    CAS  PubMed  Google Scholar 

  • Benson G. 1999 Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27, 573–580.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Botella L. M., Morcillo G., Barettino D. and Diez J. L. 1991 Heat-shock induction and cytoplasmic localization of transcripts from telomeric-associated sequences in Chironomus thummi. Exp. Cell Res. 196, 206–209.

    CAS  PubMed  Google Scholar 

  • Bronski M. J., Martinez C. C., Weld H. A. and Eisen M. B. 2020 Whole genome sequences of 23 species from the Drosophila montium species group (Diptera: Drosophilidae): a resource for testing evolutionary hypotheses. G3 (Bethesda) 10, 1443–1455.

  • Burma P. K. and Lakhotia S. C. 1984 Cytological identity of 93D-like heat-shock loci in Drosophila melanogaster. Indian J. Exp. Biol. 22, 577–580.

    CAS  Google Scholar 

  • Bystroff C. and Garde S. 2003 Helix propensities of short peptides: molecular dynamics versus bioinformatics. Proteins 50, 552–562.

    CAS  PubMed  Google Scholar 

  • Chakraborty M., Chang C., Khost D. E., Vedanayagam J., Adrion J. R., Liao Y. et al. 2020 Evolution of genome structure in the Drosophila simulans species complex. bioRxiv, 968743.

  • Chen J., Shishkin A. A., Zhu X., Kadri S., Maza I., Guttman M. et al. 2016 Evolutionary analysis across mammals reveals distinct classes of long non-coding RNAs. Genome Biol. 17, 19.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chodroff R. A., Goodstadt L., Sirey T. M., Oliver P. L., Davies K. E., Green E. D. et al. 2010 Long noncoding RNA genes: conservation of sequence and brain expression among diverse amniotes. Genome Biol. 11, R72.

    PubMed  PubMed Central  Google Scholar 

  • Chowdhuri D. K. and Lakhotia S. C. 1986 Different effects different effects of 93d on 87c heat-shock puff activity in Drosophila melanogaster and Drosophila simulans. Chromosoma 94, 279–284.

    Google Scholar 

  • Chung C., Berson A., Kennerdell J. R., Sartoris A., Unger T., Porta S. et al. 2018 Aberrant activation of non-coding RNA targets of transcriptional elongation complexes contributes to TDP-43 toxicity. Nat. Commun. 9, 4406.

    PubMed  PubMed Central  Google Scholar 

  • Collinge J. E., Anderson A. R., Weeks A. R., Johnson T. K. and McKechnie S. W. 2008 Latitudinal and cold-tolerance variation associate with DNA repeat-number variation in the hsr-omega RNA gene of Drosophila melanogaster. Heredity (Edinb) 101, 260–270.

    CAS  Google Scholar 

  • Corona-Gomez J. A., Garcia-Lopez I. J., Stadler P. F. and Fernandez-Valverde S. L. 2019 Splicing conservation signals in plant long non-coding RNAs. bioRxiv, 588954.

  • Dangli A., Grond C., Kloetzel P. and Bautz E. K. 1983 Heat-shock puff 93 D from Drosophila melanogaster: accumulation of a RNP-specific antigen associated with giant particles of possible storage function. Embo J. 2, 1747–1751.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Derksen J. 1975 Induced RNP production in different cell types of Drosophila. Cell Differ. 4, 1–10.

    CAS  PubMed  Google Scholar 

  • Drosopoulou E., Konstantopoulou I. and Scouras Z. G. 1996 The heat shock genes in the Drosophila montium subgroup: Chromosomal localization and evolutionary implications. Chromosoma 105, 104–110.

    CAS  PubMed  Google Scholar 

  • Durmaz E., Benson C., Kapun M., Schmidt P. and Flatt T. 2018 An inversion supergene in Drosophila underpins latitudinal clines in survival traits. J. Evol. Biol. 31, 1354–1364.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fatima R., Akhade V. S., Pal D. and Rao M. R. S. 2015 Long noncoding RNAs in development and cancer: potential biomarkers and therapeutic targets. Mol. Cell. Ther. 3, 1–19.

    CAS  Google Scholar 

  • Ferreira H. J. and Esteller M. 2018 Non-coding RNAs, epigenetics, and cancer: tying it all together. Cancer Metastasis Rev. 37, 55–73.

    CAS  PubMed  Google Scholar 

  • Fini M. E., Bendena W. G. and Pardue M. L. 1989 Unusual behavior of the cytoplasmic transcript of hsr omega: an abundant, stress-inducible RNA that is translated but yields no detectable protein product. J. Cell Biol. 108, 2045–2057.

    CAS  PubMed  Google Scholar 

  • Forood B., Feliciano E. J. and Nambiar K. P. 1993 Stabilization of alpha-helical structures in short peptides via end capping. Proc. Natl. Acad. Sci. USA 90, 838–842.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Garbe J. C. and Pardue M. L. 1986 Heat shock locus 93D of Drosophila melanogaster: a spliced RNA most strongly conserved in the intron sequence. Proc. Natl. Acad. Sci. USA 83, 1812–1816.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Garbe J. C., Bendena W. G., Alfano M. and Pardue M. L. 1986 A Drosophila heat shock locus with a rapidly diverging sequence but a conserved structure. J. Biol. Chem. 261, 16889–16894.

    CAS  PubMed  Google Scholar 

  • Garbe J. C., Bendena W. G. and Pardue M. L. 1989 Sequence evolution of the Drosophila heat shock locus hsr omega. I. The nonrepeated portion of the gene. Genetics 122, 403–415.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gubenko I. S., Subbota R. P. and Semeshin V. F. 1992 Unusual Drosophila virilis stress‐puff at 20CD: cytological localization of a heat sensitive locus and some peculiarities of the heat shock response. Hereditas 115, 283–290.

    Google Scholar 

  • Haerty W. and Ponting C. P. 2013 Mutations within lncRNAs are effectively selected against in fruitfly but not in human. Genome Biol. 14, R49.

    PubMed  PubMed Central  Google Scholar 

  • Harper E. T. and Rose G. D. 1993 Helix stop signals in proteins and peptides: the capping box. Biochemistry 32, 7605–7609.

    CAS  PubMed  Google Scholar 

  • Hirose T. and Nakagawa S. 2016 Clues to long noncoding RNA taxonomy. Biochim. Biophys. Acta 1, 1–2.

    Google Scholar 

  • Hoffmann A. A., Sgro C. M. and Weeks A. R. 2004 Chromosomal inversion polymorphisms and adaptation. Trends Ecol. Evol. 19, 482–488.

    PubMed  Google Scholar 

  • Jolly C. and Lakhotia S. C. 2006 Human sat III and Drosophila hsrω transcripts: a common paradigm for regulation of nuclear RNA processing in stressed cells. Nucliec Acids Res. 34, 5508–5514.

    CAS  Google Scholar 

  • Jones D. T. 1999 Protein secondary structure prediction based on position-specific scoring matrices. J. Mol. Biol. 292, 195–202.

    CAS  PubMed  Google Scholar 

  • Kapusta A. and Feschotte C. 2014 Volatile evolution of long noncoding RNA repertoires: mechanisms and biological implications. Trends Genet. 30, 439–452.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kelso M. J., Beyer R. L., Hoang H. N., Lakdawala A. S., Snyder J. P., Oliver W. V. et al. 2004 α-turn mimetics: short peptide α-helices composed of cyclic metallopentapeptide modules. J. Amer. Chem. Soc. 126, 4828–4842.

    CAS  Google Scholar 

  • Kennington W. J., Partridge L. and Hoffmann A. A. 2006 Patterns of diversity and linkage disequilibrium within the cosmopolitan inversion In(3R)Payne in Drosophila melanogaster are indicative of coadaptation. Genetics 172, 1655–1663.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Khanna R. and Mohanty S. 2017 Whole genome sequence resource of Indian Zaprionus indianus. Mol. Ecol. Resour. 17, 557–564.

    CAS  PubMed  Google Scholar 

  • Kopp F. and Mendell J. T. 2018 Functional classification and experimental dissection of long noncoding RNAs. Cell 172, 393–407.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Krstenansky J. L., Owen T. J., Hagaman K. A. and McLean L. R. 1989 Short model peptides having a high α-helical tendency: design and solution properties. FEBS Lett. 242, 409–413.

    CAS  PubMed  Google Scholar 

  • Kumar S., Stecher G., Li M., Knyaz C. and Tamura K. 2018 MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lakhotia S. C. 1987 The 93D heat shock locus in Drosophila: a review. J. Genet. 66, 139–157.

    CAS  Google Scholar 

  • Lakhotia S. C. 1989 The 93D heat-shock locus of Drosophila melanogaster - modulation by genetic and developmental factors. Genome 31, 677–683.

    CAS  PubMed  Google Scholar 

  • Lakhotia S. C. 1996 RNA polymerase II dependent genes that do not code for protein. Ind. J. Biochem. Biophys. 33, 93–102.

    CAS  Google Scholar 

  • Lakhotia S. C. 2011 Forty years of the 93D puff of Drosophila melanogaster. J. Biosci. 36, 399–423.

    CAS  PubMed  Google Scholar 

  • Lakhotia S. C. 2012 Long non-coding RNAs coordinate cellular responses to stress. Wiley Interdiscip. Rev. RNA 3, 779–796.

    CAS  PubMed  Google Scholar 

  • Lakhotia S. C. 2015 Divergent actions of long noncoding RNAs on X-chromosome remodelling in mammals and Drosophila achieve the same end result: dosage compensation. J. Genet. 94, 575–584.

    CAS  PubMed  Google Scholar 

  • Lakhotia S. C. 2016 Non-coding RNAs have key roles in cell regulation. Proc. Indian Natl. Sci. Acad. 82, 1171-1182.

    Google Scholar 

  • Lakhotia S. C. 2017a From heterochromatin to long noncoding RNAs in Drosophila: Expanding the arena of gene function and regulation. Adv. Exp. Med. Biol. 1008, 75–118.

    CAS  PubMed  Google Scholar 

  • Lakhotia S. C. 2017b Non-coding RNAs demystify constitutive heterochromatin as essential modulator of epigenotype. Nucleus 60, 299–314.

    Google Scholar 

  • Lakhotia S. C. 2018 Central dogma, selfish DNA and noncoding RNAs: a historical perspective Proc. Indian Natl. Sci. Acad. 84, 315–427.

    Google Scholar 

  • Lakhotia S. C. and Mukherjee A. S. 1970 Activation of a specific puff by benzamide in D. melanogaster. Drosophila Inf. Ser. 45, 108.

  • Lakhotia S. C. and Mukherjee T. 1980 Specific activation of puff 93D of Drosophila melanogaster by benzamide and the effect of benzamide treatment on the heat shock induced puffing activity. Chromosoma 81, 125–136.

    CAS  PubMed  Google Scholar 

  • Lakhotia S. C. and Mukherjee T. 1982 Absence of novel translation products in relation to induced activity of the 93D puff in Drosophila melanogaster. Chromosoma 85, 369–374.

    CAS  PubMed  Google Scholar 

  • Lakhotia S. C. and Singh A. K. 1982 Conservation of the 93D puff of Drosophila melanogaster in different species of Drosophila. Chromosoma 86, 265–278.

    Google Scholar 

  • Lakhotia S. C., Ray P., Rajendra T. K. and Prasanth K. V. 1999 The non-coding transcripts of hsr-omega gene in Drosophila: Do they regulate trafficking and availability of nuclear RNA-processing factors? Curr. Sci. 77, 553–563.

    CAS  Google Scholar 

  • Lakhotia S. C., Rajendra T. K. and Prasanth K. V. 2001 Developmental regulation and complex organization of the promoter of the non-coding hsr(omega) gene of Drosophila melanogaster. J Biosci. 26, 25–38.

    CAS  PubMed  Google Scholar 

  • Lakhotia S. C., Mallik M., Singh A. K. and Ray M. 2012 The large noncoding hsrω-n transcripts are essential for thermotolerance and remobilization of hnRNPs, HP1 and RNA polymerase II during recovery from heat shock in Drosophila. Chromosoma 121, 49–70.

    CAS  PubMed  Google Scholar 

  • Lakhotia S. C., Mallick B. and Roy J. 2020 Non-coding RNAs: ever-expanding diversity of types and functions. In RNA-based regulation in human health and disease (ed. R. Pandey), 1st edition, vol. 16, pp. 432. Elsevier, San Diego (in press).

  • Leenders H. J., Derksen J., Mass P. M. J. M. and Berendes H. D. 1973 Selective induction of a giant puff in Drosophila hydei by vitamin B6 and derivatives. Chromosoma 41, 447–460.

    CAS  Google Scholar 

  • Lengyel J. A., Ransom L. J., Graham M. L. and Pardue M. L. 1980 Transcription and metabolism of RNA from the Drosophila melanogaster heat shock puff site 93D. Chromosoma 80, 237–252.

    CAS  PubMed  Google Scholar 

  • Lin Y., Schmidt B. F., Bruchez M. P. and McManus C. J. 2018 Structural analyses of NEAT1 lncRNAs suggest long-range RNA interactions that may contribute to paraspeckle architecture. Nucleic Acids Res. 46, 3742–3752.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lo Piccolo L. 2018 Drosophila as a model to gain insight into the role of lncRNAs in neurological disorders. Adv. Exp. Med. Biol. 1076, 119–146.

    Google Scholar 

  • Mallik M. and Lakhotia S. C. 2009 The developmentally active and stress-inducible noncoding hsromega gene is a novel regulator of apoptosis in Drosophila. Genetics 183, 831–852.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mallik M. and Lakhotia S. C. 2011 Pleiotropic consequences of misexpression of the developmentally active and stress-inducible non-coding hsrω gene in Drosophila. J. Biosci. 36, 265–280.

    CAS  PubMed  Google Scholar 

  • Marqusee S. and Baldwin R. L. 1987 Helix stabilization by Glu-… Lys+ salt bridges in short peptides of de novo design. Proc. Natl. Acad. Sci. USA 84, 8898–8902.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Martinez-Guitarte J. L., Diez J. L. and Morcillo G. 2008 Transcription and activation under environmental stress of the complex telomeric repeats of Chironomus thummi. Chromosome Res. 16, 1085–1096.

    CAS  PubMed  Google Scholar 

  • Martínez‐Guitarte J. L. and Morcillo G. 2014 Telomeric transcriptome from Chironomus riparius (Diptera), a species with noncanonical telomeres. Insect Mol. Biol. 23, 367–380.

    PubMed  Google Scholar 

  • Matsumoto A. and Nakayama K. I. 2018 Hidden peptides encoded by putative noncoding RNAs. Cell Struct. Funct. 43, 75–83.

    PubMed  Google Scholar 

  • McColl G., Hoffmann A. A. and McKechnie S. W. 1996 Response of two heat shock genes to selection for knockdown heat resistance in Drosophila melanogaster. Genetics 143, 1615–1627.

    CAS  PubMed  PubMed Central  Google Scholar 

  • McKechnie S. W., Halford M. M., McColl G. and Hoffmann A. A. 1998 Both allelic variation and expression of nuclear and cytoplasmic transcripts of Hsr-omega are closely associated with thermal phenotype in Drosophila. Proc. Natl. Acad. Sci. USA 95, 2423–2428.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mohler J. and Pardue M. L. 1984 Mutational analysis of the region surrounding the 93d heat shock locus of Drosophila melanogaster. Genetics 106, 249–265.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moltó M. D., Martínez‐Sebastián M. J. and De Frutos R. 1993 Gene arrangement phylogeny of the E element in Drosophila species of the Obscura group. J. Evol. Biol. 6, 753–758.

    Google Scholar 

  • Morcillo G., Diez J. L., Carbajal M. E. and Tanguay R. M. 1993 HSP90 associates with specific heat shock puffs (hsrω) in polytene chromosomes of Drosophila and Chironomus. Chromosoma 102, 648–659.

    CAS  PubMed  Google Scholar 

  • Mukherjee T. and Lakhotia S. C. 1979 3H-uridine incorporation in the puff 93D and in chromocentric heterochromatin of heat shocked salivary glands of Drosophila melanogaster. Chromosoma 74, 75–82.

    CAS  PubMed  Google Scholar 

  • Muller H. J. 1940 Bearing of the Drosophila work on systematics. In The new systematics (ed. J. Huxley), pp. 185–268. Clarendon Press, Oxford.

    Google Scholar 

  • Mutsuddi M. and Lakhotia S. C. 1995 Spatial expression of the hsr-omega (93D) gene in different tissues of Drosophila melanogaster and identification of promoter elements controlling its developmental expression. Dev. Genet.17, 303–311.

    CAS  PubMed  Google Scholar 

  • Nath B. B. and Lakhotia S. C. 1991 Search for a Drosophila-93D-like locus in Chironomus and Anopheles. Cytobios 65, 7–13.

    CAS  PubMed  Google Scholar 

  • Noh J. H., Kim K. M., McClusky W. G., Abdelmohsen K. and Gorospe M. 2018 Cytoplasmic functions of long noncoding RNAs. Wiley Interdiscip. Rev. RNA 9, e1471.

    PubMed  PubMed Central  Google Scholar 

  • O’Grady P. M. and DeSalle R. 2018 Phylogeny of the genus Drosophila. Genetics 209, 1–25.

    PubMed  PubMed Central  Google Scholar 

  • Onorati M. C., Lazzaro S., Mallik M., Ingrassia A. M. R., Carreca A. P., Singh A. K. et al. 2011 The ISWI chromatin remodeler organizes the hsrω ncrna–containing omega speckle nuclear compartments. PLoS Genet. 7, e1002096.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peters F., Lubsen N. and Sondermeijer P. 1980 Rapid sequence divergence in a heat shock locus of Drosophila. Chromosoma 81, 271–280.

    CAS  PubMed  Google Scholar 

  • Peters F., Grond C. J., Sondermeijer P. J. A. and Lubsen N. H. 1982 Chromosomal arrangement of heat shock locus 2-48B in Drosophila hydei. Chromosoma 85.

  • Peters F., Lubsen N. H., Walldorf U., Moormann R. J. and Hovemann B. 1984 The unusual structure of heat shock locus 2-48B in Drosophila hydei. Mol. Gen. Genet. 197, 392–398.

    CAS  PubMed  Google Scholar 

  • Ponting C. P. 2017 Biological function in the twilight zone of sequence conservation. BMC Biol. 15, 71.

    PubMed  PubMed Central  Google Scholar 

  • Prasanth K. V., Rajendra T. K., Lal A. K. and Lakhotia S. C. 2000 Omega speckles - a novel class of nuclear speckles containing hnRNPs associated with noncoding hsr-omega RNA in Drosophila. J. Cell Sci. 113 Pt 19, 3485–3497.

    CAS  PubMed  Google Scholar 

  • Quinn J. J., Zhang Q. C., Georgiev P., Ilik I. A., Akhtar A. and Chang H. Y. 2016 Rapid evolutionary turnover underlies conserved lncRNA-genome interactions. Genes Dev. 30, 191–207.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rako L., Blacket M., McKechnie S. and Hoffmann A. 2007 Candidate genes and thermal phenotypes: identifying ecologically important genetic variation for thermotolerance in the Australian Drosophila melanogaster cline. Mol. Ecol. 16, 2948–2957.

    CAS  PubMed  Google Scholar 

  • Ransohoff J. D., Wei Y. F. and Khavari P. A. 2018 The functions and unique features of long intergenic non-coding RNA. Nat. Rev. Mol. Cell Biol. 19, 143.

    CAS  PubMed  Google Scholar 

  • Ryseck R. P., Walldorf U. and Hovemann B. 1985 Two major RNA products are transcribed from heat-shock locus 93D of Drosophila melanogaster. Chromosoma 93, 17–20.

    CAS  PubMed  Google Scholar 

  • Ryseck R. P., Walldorf U., Hoffmann T. and Hovemann B. 1987 Heat shock loci 93D of Drosophila melanogaster and 48B of Drosophila hydei exhibit a common structural and transcriptional pattern. Nucleic Acids Res. 15, 3317–3333.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Salamov A. A. and Solovyev V. V. 1997 Recognition of 3′-processing sites of human mRNA precursors. Comput. Appl. Biosci. 13, 23–28.

    CAS  PubMed  Google Scholar 

  • Saumweber H., Symmons P., Kabisch R., Will H. and Bonhoeffer F. 1980 Monoclonal antibodies against chromosomal proteins of Drosophila melanogaster: establishment of antibody producing cell lines and partial characterization of corresponding antigens. Chromosoma 80, 253–275.

    CAS  PubMed  Google Scholar 

  • Seetharam A. S. and Stuart G. W. 2012 Whole genome phylogenies for multiple Drosophila species. BMC Res. Notes 5, 670.

    PubMed  PubMed Central  Google Scholar 

  • Seetharam A. S. and Stuart G. W. 2013 Whole genome phylogeny for 21 Drosophila species using predicted 2b-RAD fragments. Peer J. 1, e226.

    PubMed  PubMed Central  Google Scholar 

  • Semeshin V. F., Zhimulev I. F., Kritikou D. and Zacharopoulou A. 1995 Electron microscope investigation of polytene chromosomes in the mediterranean fruit fly Ceratitis capitata. Genome 38, 652–660.

    CAS  PubMed  Google Scholar 

  • Shin S. Y. and Hahm K. 2004 A short α-helical antimicrobial peptide with antibacterial selectivity. Biotechnol. Lett. 26, 735–739.

    CAS  PubMed  Google Scholar 

  • Singh A. K. and Lakhotia S. C. 2015 Dynamics of hnRNPs and omega speckles in normal and heat shocked live cell nuclei of Drosophila melanogaster. Chromosoma 124, 367–383.

    CAS  PubMed  Google Scholar 

  • Stoiber M., Celniker S., Cherbas L., Brown B. and Cherbas P. 2016 Diverse hormone response networks in 41 independent Drosophila cell lines. G3 (Bethesda) 6, 683–694.

  • Tamura K. and Nei M. 1993 Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10, 512–526.

    CAS  PubMed  Google Scholar 

  • Tavares R. C. A., Pyle A. M. and Somarowthu S. 2019 Phylogenetic analysis with improved parameters reveals conservation in lncRNA structures. J. Mol. Biol. 431, 1592–1603.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Van Der Linde K., Houle D., Spicer G. S. and Steppan S. J. 2010 A supermatrix-based molecular phylogeny of the family Drosophilidae. Genet. Res. 92, 25–38.

    Google Scholar 

  • Zhang B., Mao Y. S., Diermeier S. D., Novikova I. V., Nawrocki E. P., Jones T. A. et al. 2017 Identification and characterization of a class of MALAT1-like genomic loci. Cell Rep. 19, 1723–1738.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zu K., Sikes M. L. and Beyer A. L. 1998 Separable roles in vivo for the two RNA binding domains of Drosophila A1-hnRNP homolog. RNA 4, 1585–1598.

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank the Department of Biotechnology, Ministry of Science and Technology, Govt. of India, New Delhi for supporting this work (BT/PR6150/COE/34/20/2013). SCL is currently supported by the Science and Engineering Research Board (SERB), Govt. of India, as SERB Distinguished Fellow. RKS is supported by the Council of Scientific and Industrial Research, New Delhi through research fellowship. EM was supported by Summer Project fellowship of the Science Academies.

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Correspondence to Subhash Chandra Lakhotia.

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Corresponding editor: H. A. Ranganath

RKS, EM and SCL undertook the bioinformatic analyses and wrote the manuscript.

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Sahu, R.K., Mutt, E. & Lakhotia, S.C. Conservation of gene architecture and domains amidst sequence divergence in the hsrω lncRNA gene across the Drosophila genus: an in silico analysis. J Genet 99, 64 (2020). https://doi.org/10.1007/s12041-020-01218-6

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