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Hybrid larval lethality of Drosophila is caused by parent-of-origin expression: an insight from imaginal discs morphogenesis of Lhr pausing rescue hybrids of D. melanogaster and D. simulans

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Abstract

Hybrid males that inherit haploid set of chromosomes along with Hybrid male rescue, (Hmr+) gene from D. melanogaster mother and an autosomal set with Lethal hybrid rescue, (Lhr+) gene from D. simulans father, die at the larval/pupal transition phase due to insufficient growth of imaginal disc tissues. Comparable pattern reminiscent of hybrid F1female lethality was noted when D. melanogaster compound females were crossed with D. simulans males. The lethality is suppressed when the hybrids inherit one mutant allele of hybrid incompatibility gene (either Lhr−, or Hmr−) from either of the parent. In order to better understand the cause of lethality of F1 hybrids at larval stage, the imaginal discs development of lethal hybrids were examined and compared with those of ‘rescued’ hybrids with Lhr− and parental species. The study revealed the following major findings: (a) when hybrid male and female larvae carry only D. melanogaster X chromosome(s) in presence of both Lhr+ and Hmr+ genes, broad-ranging cell death reaction was induced in the disc tissues and eventually death of the hybrid larvae, (b) when hybrid females carry the X chromosome of both species in the background of maternal cytoplasm of D. melanogaster, the frequency of cell death in the discs was reduced significantly and discs were able to metamorphose, (c) when hybrid males and females inherit one set of autosome from Lhr null strain of D. simulans, the frequency of non-apoptotic cell death in the discs was suppressed significantly and discs development were restored, although the discs displayed fluctuating asymmetric of development. To understand the defects in the chromosomal organization associated with abnormal development of the ‘rescued’ hybrids, the functional organization of the polytene chromosomes of the ‘rescued’ hybrids were examined. It was noted that incomplete pairing of the autosomes of two species along with abnormal X chromosomal telomeric structure may have some bearing on developmental defects of the ‘rescued’ hybrids. From the results it is suggested that (1) cell death reaction in the imaginal discs of the larval lethal hybrids may be the result of divergent lineage of maternal and paternal sets of chromosomes in zygote in presences of two species specific mediator genes, Lhr+, and Hmr+, (2) suppression of larval lethality, in absence of Lhr function, indicated that the non-apoptotic type of cell death factor in the disc cells was controlled genetically by the two mediator genes in the disc cells, (3) re-specification of compartmental organization of paternal segment polarity genes in ‘rescued’ hybrid discs might cause non-random tissue damages and eventually the apoptotic type of cell death resulting into asymmetric development of the appendages in hybrids. In sum, our data revealed that cell death reaction in imaginal discs, associated with larval lethality in hybrids was a developmentally controlled program, through incompatible interactions between species specific mediator genes, Lhr+, Hmr+ and D. melanogaster X chromosome and the pattern of cell death reaction in the discs was different from apoptosis.

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References

  1. Acharyya M, Chatterjee RN. Expression patterns of developmental genes in male and female reproductive system in Drosophila melanogaster. Entom. 2001;26:164–72.

    Google Scholar 

  2. Agnes F, Suzanne M, Noselli S. The Drosophila JNK pathway controls the morphogenesis of imaginal discs during metamorphosis. Development. 1999;126:5453–82.

    CAS  PubMed  Google Scholar 

  3. Arias C, Fussero G, Zaeharonok M, Macias A. Dpp expressing and non-expressing cells: Two different populations of growing cells in Drosophila. PLoS ONE. 2015. https://doi.org/10.1371/Journal.Pone.0121457.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Bachtrog D. Positive selection at the binding sites of the Male-Specific Lethal Complex involved in dosage compensation in Drosophila. Genetics. 2008;180:1123–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Barbash DA. Ninety years of Drosophila melanogaster hybrids. Genetics. 2010;186:1–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Barbash DA, Awadalla P, Tarone AM. Functional divergence caused by ancient positive selection of Drosophila hybrid incompatibility locus. PLoS Biol. 2004;2(6):e142.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Benitez S, Sosa C, Tomasini N, Macias A. Both JNK and apoptosis pathways regulates growth and terminalia rotation during Drosophila genital discs development. Int. J. Dev. Biol. 2010;54:643–53.

    Article  CAS  PubMed  Google Scholar 

  8. Blythe SA, Wieschaus EF. Establishment and maintenance of heritable chromatin structure during early Drosophila embryogenesis. Elife. 2016;5:e20148. https://doi.org/10.7554/eLife.20148.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Bolkan BJ, Booker R, Goldberg ML, Barbash DA. Developmental and cell cycle progression defects in Drosophila hybrid males. Genetics. 2007;177:2233–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Bosco G, Campbell P, Leiva-Neto JT, Markow TA. Analysis of Drosophila species genome size and satellite DNA content reveals significant differences among strains as well as between species. Genetics. 2007;177:1277–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Brideau NJ, Barbash DA. Functional conservation of Drosophila hybrid incompatibility gene Lhr. BMC Evol. Biol. 2011;11:57.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Brideau NJ, Flores HA, Wang J, Maheshwari S, Wang X, Barbash DA. Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila. Science. 2006;314:1292–5.

    Article  CAS  PubMed  Google Scholar 

  13. Bryant PJ. Pattern formation in imaginal discs. In: Ashburner M, Wright TRF, editors. The genetics and biology of Drosophila. London: Academic Press; 1978. p. 229–335.

    Google Scholar 

  14. Chatterjee P, Banerjee S, Chatterjee RN (2008) Expression patterns of developmental genes in wing and leg imaginal discs of Drosophila melanogaster. In: Ramkrishna, Chatterjee RN (eds) Zoological Research in Human Welfare. Zoological Survey of India Publication, pp 245–257

  15. Chatterjee RN. Dosage compensation and its roles in evolution of sex chromosomes and phenotypic dimorphism: lessons from Drosophila, C. elegans and mammals. Nucleus. 2017;60:315–33.

    Article  Google Scholar 

  16. Chatterjee RN, Chatterjee P. Evolutionary origins of chromatin remodeling of dosage compensation: lessons from epigenetic modifications of X chromosomes in germ cells in Drosophila, C elegans and mammals. Nucleus. 2012;55:3–16.

    Article  Google Scholar 

  17. Chatterjee RN, Chatterjee P, Pal A, Pal-Bhadra M. Drosophila simulanslethal hybrid rescue mutation ( Lhr) rescues inviable hybrids by restoring X chromosomal dosage compensation and causes fluctuating asymmetry of development. J Genet. 2007;86:203–15.

    Article  CAS  PubMed  Google Scholar 

  18. Chatterjee RN, Chatterjee R, Ghosh S. Heterochromatin-binding proteins regulate male X polytene chromosome morphology anddosage compensation: an evidence from a variegated rearranged strain [In (1)BM 2,(rv)] and its interactions with hyperploids and mle mutation in Drosophila melanogaster. Nucleus. 2016;59:141–54.

    Article  Google Scholar 

  19. Chatterjee RN, Chatterjee C, Kuthe S, Acharyya-Ari M, Chatterjee R. Intersex (ix) mutations of Drosophila melanogaster cause nonrandom cell death in genital discs can induce tumerous in genitals in response to decapentaplegic (dppdisk) mutations. J Genet. 2015;94:207–20.

    Article  CAS  PubMed  Google Scholar 

  20. Chen EH, Baker BS. Compartmental organization of the Drosophila genital discs. Development. 1997;124:205–18.

    CAS  PubMed  Google Scholar 

  21. Cohen SN. Imaginal disc development. In: Bate M, editor. Cold spring. New Delhi: Harbor Press; 1993. p. 747–841.

    Google Scholar 

  22. Deshpande N, Meller VH. Chromatin that guides dosage compensation is modulated by the siRNA pathway in Drosophila melanogaster. Genetics. 2018;209:1085–97.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. DiBartolomeis SM, Tartof KD, Jackson FR. A superfamily of Drosophila satellite related (SR) DNA repeats restricted to the X chromosome euchromatin. Nucleic Acids Res. 1992;20:1113–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Epper F, Sanchez L. Effect of engrailed in the genital disc of Drosophila melanogaster. Dev Biol. 1983;100:387–98.

    Article  CAS  PubMed  Google Scholar 

  25. Erickson JW, Cline TW. A bZIP protein, sisterless-a collaborates with bHLH transcription factors early in Drosophila development to determine sex. Genes Dev. 1993;7:1688–702.

    Article  CAS  PubMed  Google Scholar 

  26. Freeland DM, Kuhn DT. Expression patterns of developmental genes reveal segment and parasegment organization of Drosophila melanogaster genital discs. Mech Dev. 1996;56:61–72.

    Article  CAS  PubMed  Google Scholar 

  27. Ferree PM, Barbash DA. Species-specific heterochromatin prevents mitotic chromosome segregationto cause hybrid lethality in Drosophila. PLoS Biol. 2009;7:e1000234.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Fly Base Consortium. The Fly Base data base of the Drosophila genome projects and community literature. Nucleic Acids Res. 2003;31:172–5.

    Article  CAS  Google Scholar 

  29. Gerland TA, Sun B, Smialowski P, Lukacs A, Thomae AW, et al. The Drosophila speciation factor HMR localizes to genomic insulator sites. PLoS ONE. 2017;12:e0171798.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Hutter P, Ashburner M. Genetic rescue of inviable hybrids between Drosophila melanogaster and its sibling species. Nature. 1987;327:331–3.

    Article  CAS  PubMed  Google Scholar 

  31. Hamm DC, Harrison MM. Regulatory principles governing the maternal-to-zygotic transition: insights from Drosophila melanogaster. Open Biol. 2018;8:180183. https://doi.org/10.1098/rsob.180183.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Jagannathan M, Warsinger-Pepe N, Watase GJ, Yamashita YM. Comparative analysis of satellite DNA in the Drosophila melanogaster species complex. G3 (Bethesda). 2017;7:693–704. https://doi.org/10.1534/g3.116.035352.

    Article  Google Scholar 

  33. Jan YN, Ghysen A, Christoph I, Barbel S, Jan LY. Formation of neuronal pathways in the imaginal discs of Drosophila melanogaster. The J Neurosci. 1985;5:2453–64.

    Article  CAS  PubMed  Google Scholar 

  34. Johnstone O, Lasko P. Translational regulation and RNA localization in Drosophila oocytes and embryos. Annu Rev Genet. 2001;35:365–406.

    Article  CAS  PubMed  Google Scholar 

  35. Klebes A, Biehs B, Cifuentes F, Kornberg TB. Expression profiling Drosophila imaginal discs. Genome Biol. 2002;3(0038–0038):16.

    Google Scholar 

  36. Kuhn GCS, Kuttler H, Moreira-Filho O, Heslop-Harrison JS. The 1688 Repetitive DNA of drosophila: concerted evolution at different genomic scales and association with genes. Mol Biol Evol. 2012;29:7–11.

    Article  CAS  PubMed  Google Scholar 

  37. Lindsley DL, Zimm G. The genome of Drosophila melanogaster. San Diego: Academic Press; 1992.

    Google Scholar 

  38. Lohe AR, Brutlag DL. Identical satellite DNA sequences insibling species of Drosophila. J Mol Biol. 1987;194:161–70.

    Article  CAS  PubMed  Google Scholar 

  39. Lohe A, Roberts P. Evolution of satellite DNA sequences in Drosophila. In: Verma RS, editor. Heterochromatin, molecular and structural aspects. Cambridge: Cambridge University Press; 1988. p. 148–186.

    Google Scholar 

  40. Lohe AR, Hilliker AJ, Roberts PA. Mapping simple repeated DNA sequences in heterochromatin of Drosophila melanogaster. Genetics. 1993;134:1149–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Lu X, Shapiro JA, Ting CT, Li Y, Li C, et al. Genome-wide misexpression of X-linked versus autosomal genes associated with hybrid male sterility. Genome Res. 2010;20:1097–102.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Maheswari S, Barbash DA. The genetics of hybrid incompatibilities. Annu Rev Genet. 2011;45:331–55.

    Article  CAS  Google Scholar 

  43. Mattila J, Omelyanchuk L, Kyttala S, Turunen H, Nokkala S. Role of Jun N-terminal Kinase (JNK) signaling in the wound healing and regeneration of a Drosophila melanogaster wing imaginal disc. Int J Dev Biol. 2005;49:391–9.

    Article  CAS  PubMed  Google Scholar 

  44. Milan M, Campuzano S, García-Bellido A. Developmental parameters of cell death in the wing disc of Drosophila. Dev Biol Proc Natl Acad Sci. 1997;94:5691–6.

    Article  CAS  Google Scholar 

  45. Mino M, Maekawa K, Ogawa K, Yamagish H, Inoue M. Cell death processes during expression of hybrid lethality in interspecific F1 hybrid between Nicotinagossei Domain and Nicotianatabaum. Plant physiol. 2002;130:1776–877.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Orr HA. Does postzygotic isolation result from improper dosage compensation? Genetics. 1989;122:891–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Orr HA, Madden LD, Coyne JA, Goodwin R, Hawley RS. The developmental genetics of hybrid inviability: a mitotic defect in Drosophila hybrids. Genetics. 1997;145:1031–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Pal K, Forcato M, Jost D, Sexton T, Vaillant C, Salviato E, Mazza EMC, Lugli E, Cavalli G, Ferrari F. Global chromatin conformation differences in the Drosophila dosage compensated chromosome X. Nature Commun. 2019. https://doi.org/10.1038/s41467-019-13350-8.

    Article  Google Scholar 

  49. Pal Bhadra M, Bhadra U, Birchler JA. Misregulation of Sex-lethal and disruption of male-specific lethal complex localization in Drosophila species hybrids. Genetics. 2006;174:1151–9.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Palmer AR. Fluctuating asymmetry analyses: a primer. In: Markow TA, editor. Developmental instability: its origins and evolutionary implications. Dordrechet: Kluwer Academic Publishers; 1994.

    Google Scholar 

  51. Palmer AR, Strobeck C. Fluctuating asymmetry: measurement, analysis, patterns. Annu Rev Ecol Syst. 1986;17:391–421.

    Article  Google Scholar 

  52. Pegueroles G, Papaceit M, Quintana A, Guillén A, Prevosti A, Serra L. An experimental study of evolution in progress: clines for quantitative traits in colonizing and Palearctic populations of Drosophila. Evol Ecol. 1995;9:453–65.

    Article  Google Scholar 

  53. Pierre WW, Morra R, Lucchesi J, Yedvobnick BA. Male-specific effect of dominant-negative Fos. Develop Dyn. 2008;237:3361–72.

    Article  CAS  Google Scholar 

  54. Ranz JM, Namgyal K, Gibson G, Hartl DL. Anomalies in the expression profile of interspecifichybrids of Drosophila melanogaster and Drosophila simulans. Genome Res. 2004;14:373–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Ray M, Acharyya M, Chatterjee RN. Expression of engrailed and wingless genes in the imaginal discs of Drosophila melanogaster- D. simulans hybrids. Entom. 2001;26:159–63.

    Google Scholar 

  56. Reiland J, Noor MAF. Little qualitative RNA misexpression in sterile male F1 hybrids of Drosophila pseudoobscura and D. persimilis. BMC Evolut Biol. 2002;2:16.

    Article  Google Scholar 

  57. Robertson FW, Reeve E. Studies of quantitative inheritance. I. The effects of selection of wing and thorax length in Drosophila melanogaster. J Genet. 1952;50:414–48.

    Article  Google Scholar 

  58. Rodriguez MA, Vermaak D, Bayes JJ, Malik HS. Species-specific positive selection of the male-specific lethal complex that participates in dosage compensation in Drosophila. Proc Natl Acad Sci. 2007;104:15412–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Sainz A, Wilder JA, Wolf M, Hollocher H. Drosophila melanogaster and D simulans rescue strains produce fit offspring, despite divergent centromere-specific histone alleles. Heredity. 2003;91:28–35.

    Article  CAS  PubMed  Google Scholar 

  60. Sanchez L, Dübendorfer A. Development of imaginal discs from lethal hybrids between Drosophila melanogaster and Drosophila mauritiana. Rouxs Arch Dev Biol. 1983;192:48–50.

    Article  Google Scholar 

  61. Sanchez L, Santamaria P. Reproductive isolation and morphogenetic evolution in Drosophila analyzed by breakage of ethological barriers. Genetics. 1997;147:231–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Sanchez L, Casares F, Gorfinkiel N, Guerrero I. The genital disc of Drosophila melanogaster. II. Role of the genes hedgehog, decapentaplegic and wingless. Dev Genes Evol. 1997;207:229–41.

    Article  CAS  PubMed  Google Scholar 

  63. Satyaki PRV, Cuykendall TN, Wie KHC, Brideau NJ, Kwak H, Aruna S, Ferree PM, Ji S, Barbash DA. The Hmr and Lhr hybrid incompatibility genes suppress a broad range of heterochromatic repeats. PLoS Genet. 2014;10:e1004240.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Sawamura K. The origin of reproductive isolation: biological mechanisms of genetic incompatibility. In: Kato M, editor. The biology of biodiversity. Tokyo: Springer; 1999. p. 3–19.

    Google Scholar 

  65. Sawamura K, Yamamoto M. Cytogenetical localization of Zygotic hybrid rescue (Zhr), a Drosophila melanogaster gene that rescues interspecific hybrids from embryonic lethality. Mol Gen Genet. 1993;239:441–9.

    Article  CAS  PubMed  Google Scholar 

  66. Sawamura K, Taira T, Watanabe TK. Hybrid lethal systems in the Drosophila melanogaster species complex. I. The maternal hybrid rescue (mhr) gene of Drosophila simulans. Genetics. 1993;133:299–305.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Sawamura K, Watanabe TK, Yamamoto M-T. Hybrid lethal systems in the Drosophila melanogaster species complex. Genetica. 1993;88:175–85.

    Article  CAS  PubMed  Google Scholar 

  68. Sawamura K, Yamamoto MT, Watanabe TK. Hybrid lethal systems in the Drosophila melanogasterspecies complex. II. The zygotic hybrid rescue (Zhr) gene of D. melanogaster. Genetics. 1993;133:307–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Shrestha S, Oh D-H, McKowen JK, Dassanayake M, Hart CM. 4C-seq characterization of Drosophila BEAF binding regions provides evidence for highly variable long- distance interactions between active chromatin. PLoS ONE. 2018;13(9):e0203843.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Sokoloff A. Morphological variation in natural and experimental populations of Drosophila pseudoobscura and Drosophila persimilis. Evolution. 1966;20:49–71.

    Article  PubMed  Google Scholar 

  71. Tadros W, Lipshitz HD. The maternal-to-zygotic transition: a play in two acts. Development. 2009;136:3033–42.

    Article  CAS  PubMed  Google Scholar 

  72. Thomae AW, Schade GO, Padeken J, Borath M, Vetter I, Kremmer E, Imhof A. A pair of centromeric proteins mediates reproductive isolation in Drosophila species. Develop Cell. 2013;27(4):412–24.

    Article  CAS  Google Scholar 

  73. Usakin L, Abad J, Vagin VV, de Pablos B, Villasante A, et al. Transcription of the 1.688 satellite DNA family is under the control of RNA interference machinery in Drosophila melanogaster ovaries. Genetics. 2007;176:1343–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Watanabe TK. A gene that rescues the lethal hybrids between Drosophila melanogaster and D. simulans. Jpn Genet. 1979;54:325–31.

    Article  Google Scholar 

  75. Wieschaus E, Sweeton D. Requirements for X linked zygotic gene activity during cellularization of early Drosophila embryos. Development. 1988;104:483–93.

    CAS  PubMed  Google Scholar 

  76. Wu J, Xu J, Liu B, Yao G, et al. Chromatin analysis in human early development reveals epigenetic transition during ZGA. Nature. 2018. https://doi.org/10.1038/s41586-018-0080-8.

    Article  PubMed  PubMed Central  Google Scholar 

  77. Xia W, Xu J, Yu G, Yao G, et al. Resetting histone modifications during human parental –to-zygotic transition. Science. 2019;365:353–60. https://doi.org/10.1126/Scie.aaw5118.

    Article  CAS  PubMed  Google Scholar 

  78. Zecca M, Basler K, Sturuhl G. Sequential organizing activities of engrailed, hedgehog and decapentaplegic in Drosophila wing. Development. 1995;121:2265–78.

    CAS  PubMed  Google Scholar 

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Acknowledgements

The work was supported by UGC Emeritus Fellowship [Sanction No. F. 6-6/2015-17/EMERITUS-2015-17-GEN-5478(SA-II) dt.21.09.2015] to RNC. Authors are thankful to Dr. D. Barbash, Cornell University, USA for facilitating Lhr and In(1)AB, w stocks and Dr. Isabel Guerrero, Spain for X gal stocks,

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  1. S. Kuthe

    Present address: Dr. Kanailal Bhattachayya College, 15, Kona Road, Ramrajatala, P.O. Santragachi, Howrah, WB, 711104, India

  2. Piyali Chatterje

    Present address: Gabberia Girls’ High School, Gabberia, WB, 743336, India

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  1. Genetics Research Unit, Department of Zoology, University of Calcutta, 35, B. C. Road, Kolkata, 700 019, India

    R. N. Chatterjee, S. Kuthe & Piyali Chatterje

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Chatterjee, R.N., Kuthe, S. & Chatterje, P. Hybrid larval lethality of Drosophila is caused by parent-of-origin expression: an insight from imaginal discs morphogenesis of Lhr pausing rescue hybrids of D. melanogaster and D. simulans. Nucleus 64, 61–78 (2021). https://doi.org/10.1007/s13237-020-00327-y

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