A Conserved Developmental Patterning Network Produces Quantitatively Different Output in Multiple Species of Drosophila
Differences in the level, timing, or location of gene expression can contribute to alternative phenotypes at the molecular and organismal level. Understanding the origins of expression differences is complicated by the fact that organismal morphology and gene regulatory networks could potentially vary even between closely related species. To assess the scope of such changes, we used high-resolution imaging methods to measure mRNA expression in blastoderm embryos of Drosophila yakuba and Drosophila pseudoobscura and assembled these data into cellular resolution atlases, where expression levels for 13 genes in the segmentation network are averaged into species-specific, cellular resolution morphological frameworks. We demonstrate that the blastoderm embryos of these species differ in their morphology in terms of size, shape, and number of nuclei. We present an approach to compare cellular gene expression patterns between species, while accounting for varying embryo morphology, and apply it to our data and an equivalent dataset for Drosophila melanogaster. Our analysis reveals that all individual genes differ quantitatively in their spatio-temporal expression patterns between these species, primarily in terms of their relative position and dynamics. Despite many small quantitative differences, cellular gene expression profiles for the whole set of genes examined are largely similar. This suggests that cell types at this stage of development are conserved, though they can differ in their relative position by up to 3–4 cell widths and in their relative proportion between species by as much as 5-fold. Quantitative differences in the dynamics and relative level of a subset of genes between corresponding cell types may reflect altered regulatory functions between species. Our results emphasize that transcriptional networks can diverge over short evolutionary timescales and that even small changes can lead to distinct output in terms of the placement and number of equivalent cells.
Vyšlo v časopise:
A Conserved Developmental Patterning Network Produces Quantitatively Different Output in Multiple Species of Drosophila. PLoS Genet 7(10): e32767. doi:10.1371/journal.pgen.1002346
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002346
Souhrn
Differences in the level, timing, or location of gene expression can contribute to alternative phenotypes at the molecular and organismal level. Understanding the origins of expression differences is complicated by the fact that organismal morphology and gene regulatory networks could potentially vary even between closely related species. To assess the scope of such changes, we used high-resolution imaging methods to measure mRNA expression in blastoderm embryos of Drosophila yakuba and Drosophila pseudoobscura and assembled these data into cellular resolution atlases, where expression levels for 13 genes in the segmentation network are averaged into species-specific, cellular resolution morphological frameworks. We demonstrate that the blastoderm embryos of these species differ in their morphology in terms of size, shape, and number of nuclei. We present an approach to compare cellular gene expression patterns between species, while accounting for varying embryo morphology, and apply it to our data and an equivalent dataset for Drosophila melanogaster. Our analysis reveals that all individual genes differ quantitatively in their spatio-temporal expression patterns between these species, primarily in terms of their relative position and dynamics. Despite many small quantitative differences, cellular gene expression profiles for the whole set of genes examined are largely similar. This suggests that cell types at this stage of development are conserved, though they can differ in their relative position by up to 3–4 cell widths and in their relative proportion between species by as much as 5-fold. Quantitative differences in the dynamics and relative level of a subset of genes between corresponding cell types may reflect altered regulatory functions between species. Our results emphasize that transcriptional networks can diverge over short evolutionary timescales and that even small changes can lead to distinct output in terms of the placement and number of equivalent cells.
Zdroje
1. CarrollSB 2008 Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134 25 36
2. WrayGA 2007 The evolutionary significance of cis-regulatory mutations. Nat Rev Genet 8 206 216
3. Meireles-FilhoACStarkA 2009 Comparative genomics of gene regulation-conservation and divergence of cis-regulatory information. Curr Opin Genet Dev 19 565 570
4. MayoAESettyYShavitSZaslaverAAlonU 2006 Plasticity of the cis-regulatory input function of a gene. PLoS Biol 4 e45 doi:10.1371/journal.pbio.0040045
5. RosenfeldNYoungJWAlonUSwainPSElowitzMB 2005 Gene regulation at the single-cell level. Science (New York, NY) 307 1962 1965
6. Luengo HendriksCLKeranenSVFowlkesCCSimirenkoLWeberGH 2006 Three-dimensional morphology and gene expression in the Drosophila blastoderm at cellular resolution I: data acquisition pipeline. Genome Biol 7 R123
7. FowlkesCCHendriksCLKeränenSVWeberGHRübelO 2008 A quantitative spatiotemporal atlas of gene expression in the Drosophila blastoderm. Cell 133 364 374
8. GrazeRMMcIntyreLMMainBJWayneMLNuzhdinSV 2009 Regulatory Divergence in Drosophila melanogaster and D. simulans, a Genomewide Analysis of Allele-Specific Expression. Genetics 183 547
9. KalinkaATVargaKMGerrardDTPreibischSCorcoranDL 2010 Gene expression divergence recapitulates the developmental hourglass model. Nature 468 811
10. TautzDNigroL 1998 Microevolutionary divergence pattern of the segmentation gene hunchback in Drosophila. Molecular Biology and Evolution 15 1403 1411
11. KimJKerrJQMinGS 2000 Molecular heterochrony in the early development of Drosophila. Proceedings of the National Academy of Sciences of the United States of America 97 212 216
12. LudwigMZPalssonAAlekseevaEBergmanCMNathanJ 2005 Functional evolution of a cis-regulatory module. PLoS Biol 3 e93 doi:10.1371/journal.pbio.0030093
13. HareEEPetersonBKIyerVNMeierREisenMB 2008 Sepsid even-skipped enhancers are functionally conserved in Drosophila despite lack of sequence conservation. PLoS Genet 4 e1000106 doi:10.1371/journal.pgen.1000106
14. LottSLudwigMKreitmanM 2011 Evolution and Inheritance of Early Embryonic Patterning in Drosophila Simulans and D. Sechellia. Evolution 65 1388 99
15. St JohnstonDNüsslein-VolhardC 1992 The origin of pattern and polarity in the Drosophila embryo. Cell 68 201 219
16. LemkeSBuschSEAntonopoulosDAMeyerFDomanusMH 2010 Maternal activation of gap genes in the hover fly Episyrphus. Development 137 1709 1719
17. LemkeSStauberMShawPJRafiqiAMPrellA 2008 Bicoid occurrence and Bicoid-dependent hunchback regulation in lower cyclorrhaphan flies. Evol Dev 10 413 420
18. WilsonMJHavlerMDeardenPK 2010 Giant, Krüppel, and caudal act as gap genes with extensive roles in patterning the honeybee embryo. Developmental biology 339 200 211
19. TautzD 2004 Segmentation. Dev Cell 7 301 312
20. ShawPJSalamehAMcGregorAPBalaSDoverGA 2001 Divergent structure and function of the bicoid gene in Muscoidea fly species. Evol Dev 3 251 262
21. RosenbergMILynchJADesplanC 2009 Heads and tails: evolution of antero-posterior patterning in insects. Biochim Biophys Acta 1789 333 342
22. GoltsevYHsiongWLanzaroGLevineM 2004 Different combinations of gap repressors for common stripes in Anopheles and Drosophila embryos. Developmental Biology 275 435 446
23. McGregorAP 2006 Wasps, beetles and the beginning of the ends. Bioessays 28 683 686
24. SchroederMDGreerCGaulU 2011 How to make stripes: deciphering the transition from non-periodic to periodic patterns in Drosophila segmentation. Development (Cambridge, England) 138 3067 3078
25. BlankenshipJTWieschausE 2001 Two new roles for the Drosophila AP patterning system in early morphogenesis. Development (Cambridge, England) 128 5129 5138
26. KeränenSFowlkesCHendriksCLSudarDKnowlesD 2006 Three-dimensional morphology and gene expression in the Drosophila blastoderm at cellular resolution II: dynamics. Genome Biol 7 R124
27. FowlkesCCMalikJCris KeranenSVBigginMD 2005 Registering Drosophila Embryos at Cellular Resolution to Build a Quantitative 3D Atlas of Gene Expression Patterns and Morphology. 2005 IEEE Computational Systems Bioinformatics Conference - Workshops (CSBW'05) 354 357
28. MacarthurSLiXLiJBrownJBChuH 2009 Developmental roles of 21 Drosophila transcription factors are determined by quantitative differences in binding to an overlapping set of thousands of genomic regions. Genome Biol 10 R80
29. ConsortiumDGClarkAGEisenMBSmithDRBergmanCM 2007 Evolution of genes and genomes on the Drosophila phylogeny. Nature 450 203 218
30. BradleyRKLiXTrapnellCDavidsonSPachterL 2010 Binding site turnover produces pervasive quantitative changes in transcription factor binding between closely related Drosophila species. PLoS Biol 8 e1000343 doi:10.1371/journal.pbio.1000343
31. PennisiE 2011 Disease Risk Links to Gene Regulation. Science (New York, NY) 332 1031 1031
32. HuiskenJStainierDYR 2009 Selective plane illumination microscopy techniques in developmental biology. Development (Cambridge, England) 136 1963 1975
33. ReynaudEGTomancakP 2010 Meeting report: first light sheet based fluorescence microscopy workshop. Biotechnology journal 5 798 804
34. KaliskyTQuakeSR 2011 Single-cell genomics. Nat Methods 8 311 314
35. WohlbachDJThompsonDAGaschAPRegevA 2009 From elements to modules: regulatory evolution in Ascomycota fungi. Current opinion in genetics & development 19 571 578
36. PeterISDavidsonEH 2011 Evolution of gene regulatory networks controlling body plan development. Cell 144 970 985
37. KimJHeXSinhaS 2009 Evolution of regulatory sequences in 12 Drosophila species. PLoS Genet 5 e1000330 doi:10.1371/journal.pgen.1000330
38. CrockerJTamoriYErivesA 2008 Evolution Acts on Enhancer Organization to Fine-Tune Gradient Threshold Readouts. PLoS Biol 6 e263 doi:10.1371/journal.pbio.0060263
39. X-YLSean ThomasSaboPeterJSandstromRichardBThurmanRobertECanfieldTheresaDGisteErikaFisherWilliamHammondsAnnCelnikerSusanEBigginMarkDStamatoyannopoulosJohnA 2011 Dynamic reprogramming of chromatin accessibility during Drosophila embryo development. Genome Biology 12 R43
40. HoskinsRALandolinJMBrownJBSandlerJETakahashiH 2011 Genome-wide analysis of promoter architecture in Drosophila melanogaster. Genome research 21 182 192
41. BerezikovERobineNSamsonovaAWestholmJONaqviA 2011 Deep annotation of Drosophila melanogaster microRNAs yields insights into their processing, modification, and emergence. Genome research 21 203 215
42. JanssensHHouSJaegerJKimARMyasnikovaE 2006 Quantitative and predictive model of transcriptional control of the Drosophila melanogaster even skipped gene. Nat Genet 38 1159 1165
43. SegalERaveh-SadkaTSchroederMUnnerstallUGaulU 2008 Predicting expression patterns from regulatory sequence in Drosophila segmentation. Nature 451 535 540
44. HeXSameeMABlattiCSinhaS 2010 Thermodynamics-based models of transcriptional regulation by enhancers: the roles of synergistic activation, cooperative binding and short-range repression. PLoS Comput Biol 6 e1000935 doi:10.1371/journal.pcbi.1000935
45. FakhouriWDAyASayalRDreschJDayringerE 2010 Deciphering a transcriptional regulatory code: modeling short-range repression in the Drosophila embryo. Molecular Systems Biology 6 341
46. NambaRPazderaTMCerroneRLMindenJS 1997 Drosophila embryonic pattern repair: how embryos respond to bicoid dosage alteration. Development 124 1393 1403
47. BullaugheyK 2011 Changes in selective effects over time facilitate turnover of enhancer sequences. Genetics 187 567 582
48. HeBZHollowayAKMaerklSJKreitmanM 2011 Does positive selection drive transcription factor binding site turnover? A test with Drosophila cis-regulatory modules. PLoS Genet 7 e1002053 doi:10.1371/journal.pgen.1002053
49. WittkoppPJStewartEEArnoldLLNeidertAHHaerumBK 2009 Intraspecific polymorphism to interspecific divergence: genetics of pigmentation in Drosophila. Science 326 540 544
50. ManceauMDominguesVSMallarinoRHoekstraHE 2011 The developmental role of Agouti in color pattern evolution. Science 331 1062 1065
51. McGregorAPOrgogozoVDelonIZanetJSrinivasanDG 2007 Morphological evolution through multiple cis-regulatory mutations at a single gene. Nature
52. ChanYFMarksMEJonesFCVillarrealGJShapiroMD 2010 Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327 302 305
53. SchwarzkopfLBlowsMWCaleyMJ 1999 Life-History Consequences of Divergent Selection on Egg Size in Drosophila melanogaster. Am Nat 154 333 340
54. AzevedoRBFrenchVPartridgeL 1996 Thermal evolution of egg size in Drosophila Melanogaster. Evolution; international journal of organic evolution 50 2338 2345
55. MilesCMLottSHendriksCLLudwigMManu 2011 Artificial selection on egg size perturbs early pattern formation in Drosophila melanogaster. Evolution 65 33 42
56. HendriksCLLKeränenSVBigginMDKnowlesDW 2007 Automatic channel unmixing for high-throughput quantitative analysis of fluorescence images. Optics Express 15 12306 12317
57. MeyerMMunznerTDePaceAPfisterH 2010 MulteeSum: a tool for comparative spatial and temporal gene expression data. IEEE Trans Vis Comput Graph 16 908 917
58. JaegerJ 2011 The gap gene network. Cell Mol Life Sci 68 243 274
59. CarrollSB 1990 Zebra patterns in fly embryos: activation of stripes or repression of interstripes? Cell 60 9 16
60. MeyerMWongBStyczynskiMMunznerTPfisterH 2010 Pathline: A tool for comparative functional genomics. Computer Graphics Forum 29 3 1043 1052
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2011 Číslo 10
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- The Glycobiome Reveals Mechanisms of Pentose and Hexose Co-Utilization in Bacteria
- Global Mapping of Cell Type–Specific Open Chromatin by FAIRE-seq Reveals the Regulatory Role of the NFI Family in Adipocyte Differentiation
- Genetic Determinants of Serum Testosterone Concentrations in Men
- MicroRNA Expression and Regulation in Human, Chimpanzee, and Macaque Brains