#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Maternal Co-ordinate Gene Regulation and Axis Polarity in the Scuttle Fly


The basic head-to-tail polarity of an animal is established very early in development. In dipteran insects (flies, midges, and mosquitoes), polarity is established with the help of so-called morphogen gradients. Morphogens are regulatory proteins that are distributed as a concentration gradient, often involving diffusion from a localised source. This graded distribution then leads to the concentration-dependent activation of different target genes along the embryo’s axis. We examine this process, which differs to a surprising extent between dipteran species, in the scuttle fly Megaselia abdita, and compare our results to the model organism Drosophila melanogaster. In this way, we not only gain insights into how the mechanisms that establish polarity function differently in different species, but also how the system has evolved since these two flies shared a common ancestor. Specifically, we pin down the main difference between Drosophila and Megaselia in the altered function of the maternal Hunchback morphogen gradient, which activates target genes in the former, but not the latter species, where it has been completely replaced by the Bicoid morphogen during evolution.


Vyšlo v časopise: Maternal Co-ordinate Gene Regulation and Axis Polarity in the Scuttle Fly. PLoS Genet 11(3): e32767. doi:10.1371/journal.pgen.1005042
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005042

Souhrn

The basic head-to-tail polarity of an animal is established very early in development. In dipteran insects (flies, midges, and mosquitoes), polarity is established with the help of so-called morphogen gradients. Morphogens are regulatory proteins that are distributed as a concentration gradient, often involving diffusion from a localised source. This graded distribution then leads to the concentration-dependent activation of different target genes along the embryo’s axis. We examine this process, which differs to a surprising extent between dipteran species, in the scuttle fly Megaselia abdita, and compare our results to the model organism Drosophila melanogaster. In this way, we not only gain insights into how the mechanisms that establish polarity function differently in different species, but also how the system has evolved since these two flies shared a common ancestor. Specifically, we pin down the main difference between Drosophila and Megaselia in the altered function of the maternal Hunchback morphogen gradient, which activates target genes in the former, but not the latter species, where it has been completely replaced by the Bicoid morphogen during evolution.


Zdroje

1. Nüsslein-Volhard C, Wieschaus E (1980) Mutations affecting segment number and polarity in Drosophila. Nature 287: 795–801. 6776413

2. Akam M (1987) The molecular basis for metameric pattern in the Drosophila embryo. Development 101: 1–22. 2896587

3. Ingham PW (1988) The molecular genetics of embryonic pattern formation in Drosophila. Nature 335: 25–34. 2901040

4. St Johnston D, Nüsslein-Volhard C (1992) The origin of pattern and polarity in the Drosophila embryo. Cell 68: 201–219. 1733499

5. Jaeger J (2011) The gap gene network. Cell Mol Life Sci 68: 243–274. doi: 10.1007/s00018-010-0536-y 20927566

6. Driever W, Nüsslein-Volhard C (1988) The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner. Cell 54: 95–104. 3383245

7. Little SC, Tkačik G, Kneeland TB, Wieschaus EF, Gregor T (2011) The formation of the Bicoid morphogen gradient requires protein movement from anteriorly localized mRNA. PLoS Biol 9: e1000596. doi: 10.1371/journal.pbio.1000596 21390295

8. Gregor T, Wieschaus EF, McGregor AP, Bialek W, Tank DW (2007) Stability and Nuclear Dynamics of the Bicoid Morphogen Gradient. Cell 130: 141–152. 17632061

9. Mlodzik M, Gehring WJ (1987) Expression of the caudal gene in the germ line of Drosophila: formation of an RNA and protein gradient during early embryogenesis. Cell 48: 465–478. 2433048

10. Mlodzik M, Fjose A, Gehring WJ (1985) Isolation of caudal, a Drosophila homeo box-containing gene with maternal expression, whose transcripts form a concentration gradient at the pre-blastoderm stage. EMBO J 4: 2961–2969. 16453641

11. Macdonald PM, Struhl G (1986) A molecular gradient in early Drosophila embryos and its role in specifying the body pattern. Nature 324: 537–545. 2878369

12. Surkova S, Kosman D, Kozlov K, Manu, Myasnikova E, et al. (2008) Characterization of the Drosophila segment determination morphome. Dev Biol 313: 844–862. 18067886

13. Rivera-Pomar R, Lu X, Perrimon N, Taubert H, Jäckle H (1995) Activation of posterior gap gene expression in the Drosophila blastoderm. Nature 376: 253–256. 7617036

14. Mlodzik M, Gehring W (1987) Hierachy of the genetic interactions that specify the anterior-posterior segmentation pattern of the Drosophila embryo monitored by caudal protein expression. Development 101: 421–435.

15. Driever W, Thoma G, Nüsslein-Volhard C (1989) Determination of spatial domains of zygotic gene expression in the Drosophila embryo by the affinity of binding sites for the bicoid morphogen. Nature 340: 363–367. 2502714

16. Driever W, Nüsslein-Volhard C (1989) The bicoid protein is a positive regulator of hunchback transcription in the early Drosophila embryo. Nature 337: 138–143. 2911348

17. Struhl G, Struhl K, Macdonald PM (1989) The gradient morphogen bicoid is a concentration-dependent transcriptional activator. Cell 57: 1259–1273. 2567637

18. Gregor T, Tank DW, Wieschaus EF, Bialek W (2007) Probing the Limits to Positional Information. Cell 130: 153–164. 17632062

19. Ochoa-Espinosa A, Yucel G, Kaplan L, Pare A, Pura N, et al. (2005) The role of binding site cluster strength in Bicoid-dependent patterning in Drosophila. Proc Natl Acad Sci U S A 102: 4960–4965. 15793007

20. Gao Q, Wang Y, Finkelstein R (1996) Orthodenticle regulation during embryonic head development in drosophila. Mech Dev 56: 3–15. 8798143

21. Wang C, Lehmann R (1991) Nanos is the localized posterior determinant in Drosophila. Cell 66: 637–647. 1908748

22. Forrest KM, Gavis ER (2003) Live imaging of endogenous RNA reveals a diffusion and entrapment mechanism for nanos mRNA localization in Drosophila. Curr Biol 13: 1159–1168. 12867026

23. Lehmann R, Nüsslein-Volhard C (1991) The maternal gene nanos has a central role in posterior pattern formation of the Drosophila embryo. Development 112: 679–691. 1935684

24. Hülskamp M, Pfeifle C, Tautz D (1990) A morphogenetic gradient of hunchback protein organizes the expression of the gap genes Krüppel and knirps in the early Drosophila embryo. Nature 346: 577–580. 2377231

25. Struhl G (1989) Differing strategies for organizing anterior and posterior body pattern in Drosophila embryos. Nature 338: 741–744. 2716822

26. Irish V, Lehmann R, Akam M (1989) The Drosophila posterior-group gene nanos functions by repressing hunchback activity. Nature 338: 646–648. 2704419

27. Yajima H (1964) Studies on embryonic determination of the harlequin-fly, Chironomus dorsalis. II. Effects of partial irradiation of the egg by UV light. J Embryol exp Morph 12: 89–100. 14155410

28. Kalthoff K, Sander K (1968) Der Entwicklungsgang der Missbildung Doppelabdomen im partiell UV-bestrahlten Ei von Smittia parthenogenetica (Dipt., Chironomidae). Wilhelm Roux Arch EntwMech Org 161: 129/278.

29. Kalthoff K (1978) Pattern formation in early insect embryogenesis—data calling for modification of a recent model. J Cell Sci 29: 1–15. 627599

30. Stauber M, Jäckle H, Schmidt-Ott U (1999) The anterior determinant bicoid of Drosophila is a derived Hox class 3 gene. Proc Natl Acad Sci U S A 96: 3786–3789. 10097115

31. Stauber M, Taubert H, Schmidt-Ott U (2000) Function of bicoid and hunchback homologs in the basal cyclorrhaphan fly Megaselia (Phoridae). Proc Natl Acad Sci U S A 97: 10844–10849. 10995461

32. Stauber M, Prell A, Schmidt-Ott U (2002) A single Hox3 gene with composite bicoid and zerknüllt expression characteristics in non-Cyclorrhaphan flies. Proc Natl Acad Sci U S A 99: 274–279. 11773616

33. Schmidt-Ott U, Rafiqi AM, Lemke S (2010) Hox Genes. Deutsch JS, editor New York, NY: Springer New York. doi: 10.1007/978-1-4419-6673-5

34. Bonneton F, Shaw PJ, Fazakerley C, Shi M, Dover GA (1997) Comparison of bicoid-dependent regulation of hunchback between Musca domestica and Drosophila melanogaster. Mech Dev 66: 143–156. 9376318

35. McGregor AP, Shaw PJ, Hancock JM, Bopp D, Hediger M, et al. (2001) Rapid restructuring of bicoid-dependent hunchback promoters within and between Dipteran species: implications for molecular coevolution. Evol Dev 3: 397–407. 11806635

36. Shaw PJ, Wratten NS, McGregor AP, Dover GA (2002) Coevolution in bicoid-dependent promoters and the inception of regulatory incompatibilities among species of higher Diptera. Evol Dev 4: 265–277. 12168619

37. Lemke S, Stauber M, Shaw PJ, Rafiqi AM, Prell A, et al. (2008) Bicoid occurrence and Bicoid-dependent hunchback regulation in lower cyclorrhaphan flies. Evol Dev 10: 413–420. doi: 10.1111/j.1525-142X.2008.00252.x 18638318

38. Lemke S, Busch SE, Antonopoulos D a., Meyer F, Domanus MH, et al. (2010) Maternal activation of gap genes in the hover fly Episyrphus. Development 137: 1709–1719. doi: 10.1242/dev.046649 20430746

39. Shaw PJ, Salameh A, McGregor AP, Bala S, Dover GA (2001) Divergent structure and function of the bicoid gene in Muscoidea fly species. Evol Dev 3: 251–262. 11478522

40. Bownes M, Kalthoff K (1974) Embryonic defects in Drosophila eggs after partial u.v. irradiation at different wavelengths. J Embryol Exp Morphol 31: 329–345. 4211978

41. Frohnhöfer HG, Lehmann R, Nüsslein-Volhard C (1986) Manipulating the anteroposterior pattern of the Drosophila embryo. J Embryol Exp Morphol 97 Suppl: 169–179. 3625112

42. Schulz C, Tautz D (1995) Zygotic caudal regulation by hunchback and its role in abdominal segment formation of the Drosophila embryo. Development 121: 1023–1028. 7743918

43. Simpson-Brose M, Treisman J, Desplan C (1994) Synergy between the hunchback and bicoid morphogens is required for anterior patterning in Drosophila. Cell 78: 855–865. 8087852

44. Lemke S, Schmidt-Ott U (2009) Evidence for a composite anterior determinant in the hover fly Episyrphus balteatus (Syrphidae), a cyclorrhaphan fly with an anterodorsal serosa anlage. Development 136: 117–127. doi: 10.1242/dev.030270 19060334

45. Wiegmann BM, Trautwein MD, Winkler IS, Barr NB, Kim J-W, et al. (2011) Episodic radiations in the fly tree of life. Proc Natl Acad Sci U S A 108: 5690–5695. doi: 10.1073/pnas.1012675108 21402926

46. Jiménez-Guri E, Huerta-Cepas J, Cozzuto L, Wotton KR, Kang H, et al. (2013) Comparative transcriptomics of early dipteran development. BMC Genomics 14: 123. doi: 10.1186/1471-2164-14-123 23432914

47. Stauber M, Lemke S, Schmidt-Ott U (2008) Expression and regulation of caudal in the lower cyclorrhaphan fly Megaselia. Dev Genes Evol 218: 81–87. doi: 10.1007/s00427-008-0204-5 18214532

48. Wotton KR, Jimenez-Guri E, Crombach A, Janssens H, Alcaine Colet A, et al. (2014) Quantitative System Drift Compensates for Altered Maternal Inputs to the Gap Gene Network of the Scuttle Fly Megaselia abdita. eLIFE 4: e04785.

49. Moreno E, Morata G (1999) Caudal is the Hox gene that specifies the most posterior Drosophila segment. Nature 400: 873–877. 10476966

50. Olesnicky EC, Brent AE, Tonnes L, Walker M, Pultz MA, et al. (2006) A caudal mRNA gradient controls posterior development in the wasp Nasonia. Development 133: 3973–3982. 16971471

51. Tautz D (1988) Regulation of the Drosophila segmentation gene hunchback by two maternal morphogenetic centres. Nature 332: 281–284. 2450283

52. Eldon ED, Pirrotta V (1991) Interactions of the Drosophila gap gene giant with maternal and zygotic pattern-forming genes. Development 111: 367–378. 1716553

53. Kraut R, Levine M (1991) Spatial regulation of the gap gene giant during Drosophila development. Development 111: 601–609. 1893877

54. Schulz C, Tautz D (1994) Autonomous concentration-dependent activation and repression of Krüppel by hunchback in the Drosophila embryo. Development 120: 3043–3049. 7607091

55. Bullock SL, Stauber M, Prell A, Hughes JR, Ish-Horowicz D, et al. (2004) Differential cytoplasmic mRNA localisation adjusts pair-rule transcription factor activity to cytoarchitecture in dipteran evolution. Development 131: 4251–4261. 15280214

56. Wotton KR, Jiménez-Guri E, García Matheu B, Jaeger J (2014) A staging scheme for the development of the scuttle fly Megaselia abdita. PLoS ONE 9: e84421. doi: 10.1371/journal.pone.0084421 24409295

57. Surkova S, Golubkova E, Manu, Panok L, Mamon L, et al. (2013) Quantitative dynamics and increased variability of segmentation gene expression in the Drosophila Krüppel and knirps mutants. Dev Biol 376: 99–112. doi: 10.1016/j.ydbio.2013.01.008 23333947

58. Jäckle H, Tautz D, Schuh R, Seifert E, Lehmann R (1986) Cross-regulatory interactions among the gap genes of Drosophila. Nature 324: 668–670.

59. Harding K, Levine M (1988) Gap genes define the limits of antennapedia and bithorax gene expression during early development in Drosophila. EMBO J 7: 205–214. 2896123

60. Gaul U, Jäckle H (1987) Pole region-dependent repression of the Drosophila gap gene Krüppel by maternal gene products. Cell 51: 549–555. 3119224

61. Dearolf CR, Topol J, Parker CS (1989) The caudal gene product is a direct activator of fushi tarazu transcription during Drosophila embryogenesis. Nature 341: 340–343. 2571934

62. Mlodzik M, Gibson G, Gehring WJ (1990) Effects of ectopic expression of caudal during Drosophila development. Development 109: 271–277. 1976085

63. La Rosée A, Häder T, Taubert H, Rivera-Pomar R, Jäckle H (1997) Mechanism and Bicoid-dependent control of hairy stripe 7 expression in the posterior region of the Drosophila embryo. EMBO J 16: 4403–4411. 9250684

64. Häder T, La Rosée A, Ziebold U, Busch M, Taubert H, et al. (1998) Activation of posterior pair-rule stripe expression in response to maternal caudal and zygotic knirps activities. Mech Dev 71: 177–186. 9507113

65. Kraut R, Levine M (1991) Mutually repressive interactions between the gap genes giant and Krüppel define middle body regions of the Drosophila embryo. Development 111: 611–621. 1893878

66. Rohr KB, Tautz D, Sander K (1999) Segmentation gene expression in the mothmidge Clogmia albipunctata (Diptera, psychodidae) and other primitive dipterans. Dev Genes Evol 209: 145–154. 10079357

67. Liu PZ, Kaufman TC (2004) hunchback is required for suppression of abdominal identity, and for proper germband growth and segmentation in the intermediate germband insect Oncopeltus fasciatus. Development 131: 1515–1527. 14998925

68. Pultz MA, Westendorf L, Gale SD, Hawkins K, Lynch J, et al. (2005) A major role for zygotic hunchback in patterning the Nasonia embryo. Development 132: 3705–3715. 16077090

69. Mito T, Sarashina I, Zhang H, Iwahashi A, Okamoto H, et al. (2005) Non-canonical functions of hunchback in segment patterning of the intermediate germ cricket Gryllus bimaculatus. Development 132: 2069–2079. 15788457

70. He Z, Cao Y, Yin Y, Wang Z, Chen B, et al. (2006) Role of hunchback in segment patterning of Locusta migratoria manilensis revealed by parental RNAi: 439–445.

71. Schwager EE, Pechmann M, Feitosa NM, McGregor AP, Damen WGM (2009) hunchback functions as a segmentation gene in the spider Achaearanea tepidariorum. Curr Biol 19: 1333–1340. doi: 10.1016/j.cub.2009.06.061 19631543

72. Wilson MJ, Dearden PK (2011) Diversity in insect axis formation: two orthodenticle genes and hunchback act in anterior patterning and influence dorsoventral organization in the honeybee (Apis mellifera). Development 138: 3497–3507. doi: 10.1242/dev.067926 21771808

73. Wolff C, Sommer R, Schröder R, Glaser G, Tautz D (1995) Conserved and divergent expression aspects of the Drosophila segmentation gene hunchback in the short germ band embryo of the flour beetle Tribolium. Development 121: 4227–4236. 8575322

74. Patel NH, Hayward DC, Lall S, Pirkl NR, DiPietro D, et al. (2001) Grasshopper hunchback expression reveals conserved and novel aspects of axis formation and segmentation. Development 128: 3459–3472. 11566852

75. Marques-Souza H, Aranda M, Tautz D (2008) Delimiting the conserved features of hunchback function for the trunk organization of insects. Development 135: 881–888. doi: 10.1242/dev.018317 18216167

76. Ben-David J, Chipman AD (2010) Mutual regulatory interactions of the trunk gap genes during blastoderm patterning in the hemipteran Oncopeltus fasciatus. Dev Biol 346: 140–149. doi: 10.1016/j.ydbio.2010.07.010 20643118

77. Weiss K, Fullerton S (2000) Phenogenetic Drift and the Evolution of Genotype Phenotype Relationships. Theor Popul Biol 195: 187–95.

78. True JR, Haag ES (2001) Developmental system drift and flexibility in evolutionary trajectories. Evol Dev 3: 109–19. 11341673

79. Weiss KM (2005) The phenogenetic logic of life. Nat Rev Genet 6: 36–45. 15630420

80. Haag ES (2007) Compensatory vs. pseudocompensatory evolution in molecular and developmental interactions. Genetica 129: 45–55. 17109184

81. Pavlicev M, Wagner GP (2012) A model of developmental evolution: selection, pleiotropy and compensation. Trends Ecol Evol 27: 316–22. doi: 10.1016/j.tree.2012.01.016 22385978

82. Rafiqi AM, Lemke S, Schmidt-Ott U (2011) Megaselia abdita: fixing and devitellinizing embryos. Cold Spring Harb Protoc 2011: pdb.prot5602. doi: 10.1101/pdb.prot5602 21460051

83. Rafiqi AM, Lemke S, Schmidt-Ott U (2011) Megaselia abdita: culturing and egg collection. Cold Spring Harb Protoc 2011: pdb.prot5600. doi: 10.1101/pdb.prot5600 21460049

84. Crombach A, Wotton KR, Cicin-Sain D, Jaeger J (2012) Medium-throughput processing of whole mount in situ hybridisation experiments into gene expression domains. PLoS ONE 7: e46658. doi: 10.1371/journal.pone.0046658 23029561

85. Crombach A, Wotton KR, Cicin-Sain D, Ashyraliyev M, Jaeger J (2012) Efficient reverse-engineering of a developmental gene regulatory network. PLoS Comput Biol 8: e1002589. doi: 10.1371/journal.pcbi.1002589 22807664

86. Surkova S, Myasnikova E, Janssens H, Kozlov KN, Samsonova AA, et al. (2008) Pipeline for acquisition of quantitative data on segmentation gene expression from confocal images. Fly 2: 1–9. 18849648

87. Rafiqi A, Lemke S, Schmidt-Ott U (2011) The scuttle fly Megaselia abdita (Phoridae): a link between Drosophila and mosquito development. Cold Spring Harb Protoc 4: 349–353.

88. Wotton KR, Jimenez-Guri E, Crombach A, Cicin-Sain D, Jaeger J (2014) High-resolution gene expression data from blastoderm embryos of the scuttle fly Megaselia abdita. Sci Data doi: 10.1038/sdata.2015.5.

89. Cicin-Sain D, Hermoso Pulido A, Crombach A, Wotton KR, Jiménez-Guri E, et al. (2015) SuperFly: a comparative database for quantified spatio-temporal gene expression patterns in early dipteran embryos. Nucleic Acids Res 43 (database issue): D752–756.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2015 Číslo 3
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#