EvoDevo | |
A quantitative atlas of Even-skipped and Hunchback expression in Clogmia albipunctata (Diptera: Psychodidae) blastoderm embryos | |
Johannes Jaeger1  Michael Akam2  Marco Musy1  Eva Jiménez-Guri1  Damjan Cicin-Sain1  Ken Siggens2  Hilde Janssens1  | |
[1] EMBL/CRG Research Unit in Systems Biology, Centre de Regulació Genòmica (CRG), and Universitat Pompeu Fabra (UPF), Dr. Aiguader 88, 08003 Barcelona, Spain;Department of Zoology, Downing Street, Cambridge CB2 3EJ UK | |
关键词: Quantitative expression data; Image bioinformatics; Even-skipped; Hunchback; Segmentation gene network; Comparative network analysis; Pattern formation; Non-model organism; Non-drosophilid diptera; Clogmia albipunctata; | |
Others : 804119 DOI : 10.1186/2041-9139-5-1 |
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received in 2013-09-17, accepted in 2013-11-22, 发布年份 2014 | |
【 摘 要 】
Background
Comparative studies of developmental processes are one of the main approaches to evolutionary developmental biology (evo-devo). Over recent years, there has been a shift of focus from the comparative study of particular regulatory genes to the level of whole gene networks. Reverse-engineering methods can be used to computationally reconstitute and analyze the function and dynamics of such networks. These methods require quantitative spatio-temporal expression data for model fitting. Obtaining such data in non-model organisms remains a major technical challenge, impeding the wider application of data-driven mathematical modeling to evo-devo.
Results
We have raised antibodies against four segmentation gene products in the moth midge Clogmia albipunctata, a non-drosophilid dipteran species. We have used these antibodies to create a quantitative atlas of protein expression patterns for the gap gene hunchback (hb), and the pair-rule gene even-skipped (eve). Our data reveal differences in the dynamics of Hb boundary positioning and Eve stripe formation between C. albipunctata and Drosophila melanogaster. Despite these differences, the overall relative spatial arrangement of Hb and Eve domains is remarkably conserved between these two distantly related dipteran species.
Conclusions
We provide a proof of principle that it is possible to acquire quantitative gene expression data at high accuracy and spatio-temporal resolution in non-model organisms. Our quantitative data extend earlier qualitative studies of segmentation gene expression in C. albipunctata, and provide a starting point for comparative reverse-engineering studies of the evolutionary and developmental dynamics of the segmentation gene system.
【 授权许可】
2013 Janssens et al.; licensee BioMed Central Ltd.
【 预 览 】
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20140708053551736.pdf | 1630KB | download | |
Figure 7. | 87KB | Image | download |
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Figure 5. | 122KB | Image | download |
Figure 4. | 129KB | Image | download |
Figure 3. | 86KB | Image | download |
Figure 2. | 113KB | Image | download |
Figure 1. | 85KB | Image | download |
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【 参考文献 】
- [1]Müller GB: Evo-devo: extending the evolutionary synthesis. Nat Rev Genet 2007, 8:943-949.
- [2]Wilkins AS: The Evolution of Developmental Pathways. Sunderland, MA: Sinauer Associates; 2002.
- [3]Davidson EH: The Regulatory Genome: Gene Regulatory Networks in Development and Evolution. Burlington, MA: Academic; 2006.
- [4]Stern DL, Orgogozo V: The loci of evolution: how predictable is genetic evolution? Evolution 2008, 62:2155-2177.
- [5]Stern DL, Orgogozo V: Is genetic evolution predictable? Science 2009, 323:746-751.
- [6]Maynard Smith J, Burian R, Kauffman S, Alberch P, Campbell J, Goodwin B, Lande R, Raup D, Wolpert L: Developmental constraints and evolution. Q Rev Biol 1985, 60:265-287.
- [7]Salazar-Ciudad I, Marín-Riera M: Adaptive dynamics under development-based genotype-phenotype maps. Nature 2013, 497:361-364.
- [8]Hinman VF, Nguyen AT, Cameron A, Davidson EH: Developmental gene regulatory network architecture across 500 million years of echinoderm evolution. Proc Natl Acad Sci USA 2003, 100:13356-13361.
- [9]Davidson EH, Erwin DH: Gene regulatory networks and the evolution of animal body plans. Science 2006, 311:796-800.
- [10]Hinman V, Davidson EH: Evolutionary plasticity of developmental gene regulatory network architecture. Proc Natl Acad Sci USA 2007, 104:19404-19409.
- [11]Wilkins AS: Between “design” and “bricolage”: genetic networks, levels of selection, and adaptive evolution. Proc Natl Acad Sci USA 2007, 104:8590-8596.
- [12]Gao F, Davidson EH: Transfer of a large gene regulatory apparatus to a new developmental address in echinoid evolution. Proc Natl Acad Sci USA 2008, 105:6091-6096.
- [13]Erwin DH, Davidson EH: The evolution of hierarchical gene regulatory networks. Nat Rev Genet 2009, 10:141-148.
- [14]Davidson EH: Emerging properties of animal gene regulatory networks. Nature 2010, 468:911-920.
- [15]Davidson EH: Evolutionary bioscience as regulatory systems biology. Dev Biol 2011, 357:35-40.
- [16]Monteiro A: Gene regulatory networks reused to build novel traits. Bioessays 2011, 34:181-186.
- [17]Peter IS, Davidson EH: Evolution of gene regulatory networks controlling body plan development. Cell 2011, 144:970-985.
- [18]Jaeger J, Irons D, Monk N: The inheritance of process: a dynamical systems approach. J Exp Zool B Mol Dev Evol 2012, 318:591-612.
- [19]Jaeger J, Crombach A: Life’s attractors: understanding developmental systems through reverse engineering and in silico evolution. In Evolutionary Systems Biology. Edited by Soyer O. Berlin: Springer; 2012:93-120.
- [20]Waddington CH: The Strategy of the Genes. London, UK: George Allen & Unwin Ltd; 1957.
- [21]Maynard Smith J: Natural selection and the concept of a protein space. Nature 1970, 225:563-564.
- [22]Dawkins R: The evolution of evolvability. In Artificial Life, the Proceedings of an Interdisciplinary Workshop on the Synthesis and Simulation of Living Systems. Edited by Langton C. Redwood City, CA: Addison-Wesley; 1989:201-220.
- [23]Wagner GP, Altenberg L: Complex adaptations and the evolution of evolvability. Evolution 1996, 50:967-976.
- [24]Kirschner M, Gerhart J: Evolvability. Proc Natl Acad Sci USA 1998, 95:8420-8427.
- [25]Flatt T: The evolutionary genetics of canalization. Q Rev Biol 2005, 80:287-316.
- [26]Wagner A: Robustness and Evolvability in Living Systems. Princeton, NJ: Princeton University Press; 2005.
- [27]Aldana M, Balleza E, Kauffman S, Resendiz O: Robustness and evolvability in genetic regulatory networks. J Theor Biol 2007, 245:433-448.
- [28]Gerhart J, Kirschner M: The theory of facilitated variation. Proc Natl Acad Sci USA 2007, 104:8582-8589.
- [29]Hendrikse JL, Parsons TE, Hallgrímsson B: Evolvability as the proper focus of evolutionary developmental biology. Evol Dev 2007, 9:393-401.
- [30]Pigliucci M: Is evolvability evolvable? Nat Rev Genet 2008, 9:75-82.
- [31]Wagner A: Robustness and evolvability: a paradox resolved. Proc R Soc B 2008, 275:91-100.
- [32]Masel J, Siegal ML: Robustness: mechanisms and consequences. Trends Genet 2009, 25:395-403.
- [33]Masel J, Trotter MV: Robustness and evolvability. Trends Genet 2010, 26:406-414.
- [34]Pigliucci M: Genotype-phenotype mapping and the end of the ‘genes as blueprint’ metaphor. Philos Trans R Soc Lond B Biol Sci 2010, 365:557-566.
- [35]Wagner GP, Zhang J: The pleiotropic structure of the genotype-phenotype map: the evolvability of complex organisms. Nat Rev Genet 2011, 12:204-213.
- [36]Wagner A: The Origins of Evolutionary Innovations: A Theory of Transformative Change in Living Systems. Oxford: Oxford University Press; 2011.
- [37]Wagner A: The role of robustness in phenotypic adaptation and innovation. Proc R Soc B 2012, 279:1249-1258.
- [38]Banga JR: Optimization in computational systems biology. BMC Syst Biol 2008, 2:47. BioMed Central Full Text
- [39]Ashyraliyev M, Fomekong-Nanfack Y, Kaandorp JA, Blom J: Systems biology: parameter estimation for biochemical models. FEBS J 2009, 276:886-902.
- [40]Hecker M, Lambeck S, Toepfer S, Van Someren E, Guthke R: Gene regulatory network inference: data integration in dynamic models - a review. BioSystems 2009, 96:86-103.
- [41]Jaeger J, Monk NAM: Reverse engineering of gene regulatory networks. In Learning and Inference in Computational Systems Biology. Edited by Lawrence ND, Girolami M, Rattray M, Sanguinetti G. Cambridge, MA: MIT Press; 2010:9-34.
- [42]Reinitz J, Mjolsness E, Sharp DH: Cooperative control of positional information in Drosophila by bicoid and maternal hunchback. J Exp Zool 1995, 271:47-56.
- [43]Jaeger J, Surkova S, Blagov M, Janssens H, Kosman D, Kozlov KN, Manu , Myasnikova E, Vanario-Alonso CE, Samsonova M, Sharp DH, Reinitz J: Dynamic control of positional information in the early Drosophila embryo. Nature 2004, 430:368-371.
- [44]Perkins TJ, Jaeger J, Reinitz J, Glass L: Reverse engineering the gap gene network. PLoS Comput Biol 2006, 2:e51.
- [45]Manu , Surkova S, Spirov AV, Gursky V, Janssens H, Kim A-R, Radulescu O, Vanario-Alonso CE, Sharp DH, Samsonova M, Reinitz J: Canalization of gene expression in the Drosophila blastoderm by gap gene cross regulation. PLoS Biol 2009, 7:e1000049.
- [46]Manu , Surkova S, Spirov AV, Gursky V, Janssens H, Kim A-R, Radulescu O, Vanario-Alonso CE, Sharp DH, Samsonova M, Reinitz J: Canalization of gene expression and domain shifts in the Drosophila blastoderm by dynamical attractors. PLoS Comput Biol 2009, 5:e1000303.
- [47]Ashyraliyev M, Siggens K, Janssens H, Blom J, Akam M, Jaeger J: Gene circuit analysis of the terminal gap gene huckebein. PLoS Comput Biol 2009, 5:e1000548.
- [48]Crombach A, Wotton KR, Cicin-Sain D, Ashyraliyev M, Jaeger J: Efficient reverse-engineering of a developmental gene regulatory network. PLoS Comput Biol 2012, 8:e1002589.
- [49]Becker K, Balsa-Canto E, Cicin-Sain D, Hoermann A, Janssens H, Banga JR, Jaeger J: Reverse-engineering post-transcriptional regulation of gap genes in Drosophila melanogaster. PLoS Comput Biol 2013, 9:e1003281.
- [50]Surkova S, Myasnikova E, Janssens H, Kozlov KN, Samsonova AA, Reinitz J, Samsonova M: Pipeline for acquisition of quantitative data on segmentation gene expression from confocal images. Fly 2008, 2:1-9.
- [51]Crombach A, Cicin-Sain D, Wotton KR, Jaeger J: Medium-throughput processing of whole mount in situ hybridisation experiments into gene expression domains. PLoS ONE 2012, 7:e46658.
- [52]Rohr KB, Tautz D, Sander K: Segmentation gene expression in the mothmidge Clogmia albipunctata (Diptera, psychodidae) and other primitive dipterans. Dev Genes Evol 1999, 209:145-154.
- [53]Bullock SL, Stauber M, Prell A, Hughes JR, Ish-Horowicz D, Schmidt-Ott U: Differential cytoplasmic mRNA localisation adjusts pair-rule transcription factor activity to cytoarchitecture in dipteran evolution. Development 2004, 131:4251-4261.
- [54]García Solache MA, Jaeger J, Akam M: A systematic analysis of the gap gene system in the moth midge Clogmia albipunctata. Dev Biol 2010, 344:306-318.
- [55]Jiménez-Guri E, Wotton KR, Gavilán B, Jaeger J: A staging scheme for the development of the moth midge Clogmia albipunctata. PLoS ONE 2014, 9(1):e84422.
- [56]Janssens H, Kosman D, Vanario-Alonso CE, Jaeger J, Samsonova M, Reinitz J: A high-throughput method for quantifying gene expression data from early Drosophila embryos. Dev Genes Evol 2005, 215:374-381.
- [57]Surkova S, Myasnikova E, Kozlov KN, Pisarev A, Reinitz J, Samsonova M: Quantitative imaging of gene expression in Drosophila embryos. In Imaging in Developmental Biology. Edited by Sharpe J, Wong RA. Cold Spring Harbor, NY: Cold Spring Harbor Press; 2011:683-698.
- [58]Myasnikova E, Samsonova M, Kosman D, Reinitz J: Removal of background signal from in situ data on the expression of segmentation genes in Drosophila. Dev Genes Evol 2005, 215:320-326.
- [59]Myasnikova E, Samsonova A, Kozlov KN, Samsonova M, Reinitz J: Registration of the expression patterns of Drosophila segmentation genes by two independent methods. Bioinformatics 2001, 17:3-12.
- [60]Kozlov KN, Myasnikova E, Samsonova AA, Surkova S, Reinitz J, Samsonova M: GCPReg package for registration of the segmentation gene expression data in Drosophila. Fly 2009, 3:151-156.
- [61]Janssens H, Crombach A, Wotton KR, Cicin-Sain D, Surkova S, Lim CL, Samsonova M, Akam M, Jaeger J: Lack of tailless leads to an increase in expression variability in Drosophila embryos. Dev Biol 2013, 377:305-317.
- [62]Foe VE, Alberts BM: Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J Cell Sci 1983, 61:31-70.
- [63]Surkova S, Kosman D, Kozlov K, Manu , Myasnikova E, Samsonova AA, Spirov A, Vanario-Alonso CE, Samsonova M, Reinitz J: Characterization of the Drosophila segment determination morphome. Dev Biol 2008, 313:844-862.
- [64]Tautz D: Regulation of the Drosophila segmentation gene hunchback by two maternal morphogenetic centres. Nature 1988, 332:281-284.
- [65]Keränen SV, Fowlkes CC, Luengo Hendriks CL, Sudar D, Knowles DW, Malik J, Biggin MD: Three-dimensional morphology and gene expression in the Drosophila blastoderm at cellular resolution II: dynamics. Genome Biol 2006, 7:R124. BioMed Central Full Text
- [66]Alberch P: From genes to phenotype: dynamical systems and evolvability. Genetica 1991, 84:5-11.