Evidence for active maintenance of phylotranscriptomic hourglass patterns in animal and plant embryogenesis

Molecular Biology and Evolution

Volumn 32, Issue 5, 2015, Pages 1221-1231

  Drost, Hajk Georg ^a   Gabel, Alexander ^a   Grosse, Ivo ^a,b   Quint, Marcel ^c  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b GERMAN CENTRE FOR INTEGRATIVE BIODIVERSITY RESEARCH IDIV HALLE JENA LEIPZIG   (Germany)

^c LEIBNIZ INSTITUTE OF PLANT BIOCHEMISTRY   (Germany)

Author keywords

developmental hourglass; embryogenesis; evo devo; phylotranscriptomics

Indexed keywords

TRANSCRIPTOME;

ARABIDOPSIS THALIANA; ARTICLE; DEVELOPMENTAL STAGE; DROSOPHILA MELANOGASTER; EMBRYO; EMBRYO DEVELOPMENT; ESSENTIAL GENE; EUKARYOTE EVOLUTION; EXTANT SPECIES; MORPHOGENESIS; NONHUMAN; ONTOGENY; PHENOTYPE; PHYLOGENY; PHYLOTRANSCRIPTOMICS; PLANT DEVELOPMENT; SPECIES; STEM CELL NICHE; TARGET ORGANISM; TRANSCRIPTOME DIVERGENCE INDEX; TRANSCRIPTOMICS; ZEBRA FISH; ANIMAL; ARABIDOPSIS; BIOLOGICAL MODEL; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MOLECULAR EVOLUTION;

ANIMALIA; ARABIDOPSIS THALIANA; DANIO RERIO; DROSOPHILA MELANOGASTER;

ANIMALS; ARABIDOPSIS; DROSOPHILA MELANOGASTER; EMBRYONIC DEVELOPMENT; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MODELS, GENETIC; PHYLOGENY; PLANT DEVELOPMENT; TRANSCRIPTOME; ZEBRAFISH;

EID: 84929630779     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msv012     Document Type: Article

References (52)

1. Arbeitman MN, Furlong EE, Imam F, Johnson E, Null BH, Baker BS, Krasnow MA, Scott MP, Davis RW, White KP. (2002). Gene expression during the life cycle of Drosophila melanogaster. Science 297: 2270-2275
2. Benjamini Y, Hochberg Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol. 57: 289-300
3. Bininda-Emonds OR, Jeffery JE, Richardson MK. (2003). Inverting the hourglass: quantitative evidence against the phylotypic stage in vertebrate development. Proc Biol Sci. 270: 341-346
4. Comeron JM. (1995). A method for estimating the numbers of synonymous and nonsynonymous substitutions per site. J Mol Evol. 41: 1152-1159
5. Comte A, Roux J, Robinson-Rechavi M. (2010). Molecular signaling in zebrafish development and the vertebrate phylotypic period. Evol Dev. 12: 144-156
6. Cruickshank T, Wade MJ. (2008). Microevolutionary support for a developmental hourglass: gene expression patterns shape sequence variation and divergence in Drosophila. Evol Dev. 10: 583-590
7. Darwin C. (1859). On the origin of species. London: Murray
8. Davidson EH, Erwin DH. (2009). An integrated view of precambrian eumetazoan evolution. Cold Spring Harb Symp Quant Biol. 74: 65-80
9. Davis JC, Brandman O, Petrov DA. (2005). Protein evolution in the context of Drosophila development. J Mol Evol. 60: 774-785
10. De Mendoza A, Sebé-Pedrós A, Sestak MS, Matejcic M, Torruella G, Domazet-Lošo T, Ruiz-Trillo I. (2013). Transcription factor evolution in eukaryotes and the assembly of the regulatory toolkit in multicellular lineages. Proc Natl Acad Sci USA. 110: E4858-E4866
11. Demuth JP, De Bie T, Stajich JE, Cristianini N, Hahn MW. (2006). The evolution of mammalian gene families. PLoS One 1: e85
12. Domazet-Lošo T, Brajković J, Tautz D. (2007). A phylostratigraphy approach to uncover the genomic history of major adaptations in metazoan lineages. Trends Genet. 23: 533-539
13. Domazet-Lošo T, Tautz D. (2010). A phylogenetically based transcriptome age index mirrors ontogenetic divergence patterns. Nature 468: 815-818
14. Drost HG. (2014). A framework to perform phylotranscriptomics analyses for evolutionary developmental biology research. R package version 0.0.1. Available from: http: //CRAN.R-project.org/package=myTAI
15. Duboule D. (1994). Temporal colinearity and the phylotypic progression: a basis for the stability of a vertebrate Bauplan and the evolution of morphologies through heterochrony. Dev Suppl. 135-142
16. Dunn OJ. (1964). Multiple comparisons using rank sums. Technometrics 6: 241-252
17. Flicek P, Amode MR, Barrell D, Beal K, Billis K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fitzgerald S, et al. (2014). Ensembl 2014. Nucleic Acids Res. 42(Database Issue): D749-D755
18. Galis F, Metz JA. (2001). Testing the vulnerability of the phylotypic stage: on modularity and evolutionary conservation. J Exp Zool. 291: 195-204
19. Gerstein MB, Rozowsky J, Yan KK, Wang D, Cheng C, Brown JB, Davis CA, Hillier L, Sisu C, Li JJ, et al. (2014). Comparative analysis of the transcriptome across distant species. Nature 512: 445-448
20. Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, et al. (2012). Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 40: D1178-D1186
21. Graveley BR, Brooks AN, Carlson JW, Duff MO, Landolin JM, Yang L, Artieri CG, van Baren MJ, Boley N, Booth BW, et al. (2011). The developmental transcriptome of Drosophila melanogaster. Nature 470: 473-479
22. Hall BK. (1997). Phylotypic stage or phantom: is there a highly conserved embryonic stage in vertebrates?. Trends Ecol Evol. 12: 461-463
23. Hazkani-Covo E, Wool D, Graur D. (2005). In search of the vertebrate phylotypic stage: a molecular examination of the developmental hourglass model and von Baer's third law. J Exp Zool B Mol Dev Evol. 304: 150-158
24. He J, Deem MW. (2010). Hierarchical evolution of animal body plans. Dev Biol. 337: 157-161
25. Hedges SB, Dudley J, Kumar S. (2006). TimeTree: a public knowledgebase of divergence times among organisms. Bioinformatics 22: 2971-2972
26. Hu TT, Pattyn P, Bakker EG, Cao J, Cheng JF, Clark RM, Fahlgren N, Fawcett JA, Grimwood J, Gundlach H, et al. (2011). The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat Genet. 43: 476-481
27. Irie N, Kuratani S. (2011). Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis. Nat Commun. 2: 248
28. Irie N, Sehara-Fujisawa A. (2007). The vertebrate phylotypic stage and an early bilaterian-related stage in mouse embryogenesis defined by genomic information. BMC Biol. 5: 1
29. Kalinka AT, Tomancak P. (2012). The evolution of early animal embryos: conservation or divergence?. Trends Ecol Evol. 27: 385-393
30. Kalinka AT, Varga KM, Gerrard DT, Preibisch S, Corcoran DL, Jarrells J, Ohler U, Bergman CM, Tomancak P. (2010). Gene expression divergence recapitulates the developmental hourglass model. Nature 468: 811-814
31. Kaplan DR, Cooke TJ. (1997). Fundamental concepts in the embryogenesis of dicotyledons: a morphological interpretation of embryo mutants. Plant Cell 9: 1903-1919
32. Koch MA, Kiefer M. (2005). Genome evolution among cruciferous plants: a lecture from the comparison of the genetic maps of three diploid species-Capsella rubella, Arabidopsis lyrata subsppetraea, and A. thaliana. Am J Bot. 92: 761-767
33. Levin M, Hashimshony T, Wagner F, Yanai I. (2012). Developmental milestones punctuate gene expression in the Caenorhabditis embryo. Dev Cell 22: 1101-1108
34. Meinke D, Muralla R, Sweeney C, Dickerman A. (2008). Identifying essential genes in Arabidopsis thaliana. Trends Plant Sci. 13: 483-491
35. Meyerowitz EM. (2002). Plants compared to animals: the broadest comparative study of development. Science 295: 1482-1485
36. Ninova M, Ronshaugen M, Griffiths-Jones S. (2014). Conserved temporal patterns of microRNA expression in Drosophila support a developmental hourglass model. Genome Biol Evol. 6: 2459-2467
37. Peter IS, Davidson EH. (2011). Evolution of gene regulatory networks controlling body plan development. Cell 144: 970-984
38. Piasecka B, Lichocki P, Moretti S, Bergmann S, Robinson-Rechavi M. (2013). The hourglass and the early conservation models-co-existing patterns of developmental constraints in vertebrates. PLoS Genet. 9: e1003476
39. Quint M, Drost HG, Gabel A, Ullrich KK, Boenn M, Grosse I. (2012). A transcriptomic hourglass in plant embryogenesis. Nature 490: 98-101
40. Raff RA. (1996). The shape of life: genes, development and the evolution of animal form. Chicago: University Chicago Press
41. Richardson MK. (1995). Heterochrony and the phylotypic period. Dev Biol. 172: 412-421
42. Richardson MK. (1999). Vertebrate evolution: the developmental origins of adult variation. Bioessays 21: 604-613
43. Richardson MK, Hanken J, Gooneratne ML, Pieau C, Raynaud A, Selwood L, Wright GM. (1997). There is no highly conserved embryonic stage in the vertebrates: implications for current theories of evolution and development. Anat Embryol. 196: 91-106
44. Roux J, Robinson-Rechavi M. (2008). Developmental constraints on vertebrate genome evolution. PLoS Genet. 4: e1000311
45. Sander K. (1983). The evolution of patterning mechanisms: gleanings from insect embryogenesis and spermatogenesis. In: Goodwin BC, Holder N, Wylie C, editors. Development and evolution, The Sixth Symposium of the British Society for Developmental Biology. Cambridge: Cambridge University Press. p. 137-160
46. Schep AN, Adryan B. (2013). a comparative analysis of transcription factor expression during metazoan embryonic development. PLoS One 8: e66826
47. St. Pierre SE, Ponting L, Stefancsik R, McQuilton P, FlyBase Consortium. (2014). FlyBase 102-advanced approaches to interrogating FlyBase. Nucleic Acids Res. 42: D780-D788
48. Suyama M, Torrents D, Bork P. (2006). PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 34: W609-W612
49. Thornton K. (2003). Libsequence: a C11 class library for evolutionary genetic analysis. Bioinformatics 19: 2325-2327
50. von Baer KE 1828. ü ber Entwicklungsgeschichte der Thiere: Beobachtung und Reflexion. Konigsberg: Gebrüder Bornträger
51. Wang Z, Pascual-Anaya J, Zadissa A, Li W, Niimura Y, Huang Z, Li C, White S, Xiong Z, Fang D, et al. (2013). The draft genomes of soft-shell turtle and green sea turtle yield insights into the development and evolution of the turtle-specific body plan. Nat Genet. 45: 701-706
52. Xiang D, Venglat P, Tibiche C, Yang H, Risseeuw E, Cao Y, Babic V, Cloutier M, Keller W, Wang E, et al. (2011). Genome-wide analysis reveals gene expression and metabolic network dynamics during embryo development in Arabidopsis. Plant Physiol. 156: 346-356