What can vertebrates tell us about segmentation?

EvoDevo

Clemens Kiecker¹  Andrew Lumsden¹  Thomas Butts¹  Anthony Graham¹ 

[1] MRC Centre for Developmental Neurobiology, King’s College London, London SE1 1UL, UK

关键词: Evolution;    Vertebrates;    Pharyngeal arches;    Rhombomeres;    Somites;    Metamerism;    Segmentation;   

Others  :  814290
DOI  :  10.1186/2041-9139-5-24

 received in 2014-04-29, accepted in 2014-06-11,  发布年份 2014

【 摘 要 】

Segmentation is a feature of the body plans of a number of diverse animal groupings, including the annelids, arthropods and chordates. However, it has been unclear whether or not these different manifestations of segmentation are independently derived or have a common origin. Central to this issue is whether or not there are common developmental mechanisms that establish segmentation and the evolutionary origins of these processes. A fruitful way to address this issue is to consider how segmentation in vertebrates is directed. During vertebrate development three different segmental systems are established: the somites, the rhombomeres and the pharyngeal arches. In each an iteration of parts along the long axis is established. However, it is clear that the formation of the somites, rhombomeres or pharyngeal arches have little in common, and as such there is no single segmentation process. These different segmental systems also have distinct evolutionary histories, thus highlighting the fact that segmentation can and does evolve independently at multiple points. We conclude that the term segmentation indicates nothing more than a morphological description and that it implies no mechanistic similarity. Thus it is probable that segmentation has arisen repeatedly during animal evolution.

【 授权许可】

   
2014 Graham et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Tautz D: Segmentation. Dev Cell 2004, 7:301-312.
• [2]Hannibal RL, Patel NH: What is a segment? EvoDevo 2013, 4:35. BioMed Central Full Text
• [3]Pourquie O: Vertebrate segmentation: from cyclic gene networks to scoliosis. Cell 2011, 145:650-663.
• [4]Maroto M, Bone RA, Dale JK: Somitogenesis. Development 2012, 139:2453-2456.
• [5]Dubrulle J, McGrew MJ, Pourquie O: FGF signaling controls somite boundary position and regulates segmentation clock control of spatiotemporal Hox gene activation. Cell 2001, 106:219-232.
• [6]Dubrulle J, Pourquie O: fgf8 mRNA decay establishes a gradient that couples axial elongation to patterning in the vertebrate embryo. Nature 2004, 427:419-422.
• [7]Aulehla A, Wiegraebe W, Baubet V, Wahl MB, Deng C, Taketo M, Lewandoski M, Pourquie O: A beta-catenin gradient links the clock and wavefront systems in mouse embryo segmentation. Nat Cell Biol 2008, 10:186-193.
• [8]del Corral DR, Olivera-Martinez I, Goriely A, Gale E, Maden M, Storey K: Opposing FGF and retinoid pathways control ventral neural pattern, neuronal differentiation, and segmentation during body axis extension. Neuron 2003, 40:65-79.
• [9]Goldbeter A, Gonze D, Pourquie O: Sharp developmental thresholds defined through bistability by antagonistic gradients of retinoic acid and FGF signaling. Dev Dynam 2007, 236:1495-1508.
• [10]Takahashi Y, Koizumi K, Takagi A, Kitajima S, Inoue T, Koseki H, Saga Y: Mesp2 initiates somite segmentation through the Notch signalling pathway. Nat Genet 2000, 25:390-396.
• [11]Dias AS, de Almeida I, Belmonte JM, Glazier JA, Stern CD: Somites without a clock. Science 2014, 343:791-795.
• [12]Ozbudak EM, Lewis J: Notch signalling synchronizes the zebrafish segmentation clock but is not needed to create somite boundaries. PLoS Genet 2008, 4:e15.
• [13]Soza-Ried C, Ozturk E, Ish-Horowicz D, Lewis J: Pulses of Notch activation synchronise oscillating somite cells and entrain the zebrafish segmentation clock. Development 2014, 141:1780-1788.
• [14]Verbout AJ: A critical review of the ‘neugliederung’ concept in relation to the development of the vertebral column. Acta Biotheor 1976, 25:219-258.
• [15]Bagnall KM, Sanders EJ, Higgins SJ, Leam H: The effects of somite removal on vertebral formation in the chick. Anat Embryol (Berl) 1988, 178:183-190.
• [16]Aoyama H, Asamoto K: The developmental fate of the rostral/caudal half of a somite for vertebra and rib formation: experimental confirmation of the resegmentation theory using chick-quail chimeras. Mech Dev 2000, 99:71-82.
• [17]Morin-Kensicki EM, Melancon E, Eisen JS: Segmental relationship between somites and vertebral column in zebrafish. Development 2002, 129:3851-3860.
• [18]Keynes RJ, Stern CD: Segmentation in the vertebrate nervous system. Nature 1984, 310:786-789.
• [19]Krull CE, Lansford R, Gale NW, Collazo A, Marcelle C, Yancopoulos GD, Fraser SE, Bronner-Fraser M: Interactions of Eph-related receptors and ligands confer rostrocaudal pattern to trunk neural crest migration. Curr Biol 1997, 7:571-580.
• [20]Wang HU, Anderson DJ: Eph family transmembrane ligands can mediate repulsive guidance of trunk neural crest migration and motor axon outgrowth. Neuron 1997, 18:383-396.
• [21]Bernhardt RR, Goerlinger S, Roos M, Schachner M: Anterior-posterior subdivision of the somite in embryonic zebrafish: implications for motor axon guidance. Dev Dyn 1998, 213:334-347.
• [22]Eickholt BJ, Mackenzie SL, Graham A, Walsh FS, Doherty P: Evidence for collapsin-1 functioning in the control of neural crest migration in both trunk and hindbrain regions. Development 1999, 126:2181-2189.
• [23]Gammill LS, Gonzalez C, Gu C, Bronner-Fraser M: Guidance of trunk neural crest migration requires neuropilin 2/semaphorin 3 F signaling. Development 2006, 133:99-106.
• [24]Iimura T, Denans N, Pourquie O: Establishment of Hox vertebral identities in the embryonic spine precursors. Curr Top Dev Biol 2009, 88:201-234.
• [25]Lumsden A, Keynes R: Segmental patterns of neuronal development in the chick hindbrain. Nature 1989, 337:424-428.
• [26]Kuratani S, Horigome N, Ueki T, Aizawa S, Hirano S: Stereotyped axonal bundle formation and neuromeric patterns in embryos of a cyclostome, Lampetra japonica. J Comp Neurol 1998, 391:99-114.
• [27]Kuratani S, Horigome N: Developmental morphology of branchiomeric nerves in a cat shark, Scyliorhinus torazame, with special reference to rhombomeres, cephalic mesoderm, and distribution patterns of cephalic crest cells. Zool Sci 2000, 17:893-909.
• [28]Clarke JDW, Lumsden A: Segmental repetition of neuronal phenotype sets in the chick-embryo hindbrain. Development 1993, 118:151-162.
• [29]Eickholt BJ, Graham A, Lumsden A, Wizenmann A: Rhombomere interactions control the segmental differentiation of hindbrain neurons. Mol Cell Neurosci 2001, 18:141-148.
• [30]Wizenmann A, Lumsden A: Segregation of rhombomeres by differential chemoaffinity. Mol Cell Neurosci 1997, 9:448-459.
• [31]Xu Q, Wilkinson DG: Boundary formation in the development of the vertebrate hindbrain. Wiley Interdiscip Rev Dev Biol 2013, 2:735-745.
• [32]Fraser S, Keynes R, Lumsden A: Segmentation in the chick embryo hindbrain is defined by cell lineage restrictions. Nature 1990, 344:431-435.
• [33]Xu Q, Alldus G, Holder N, Wilkinson DG: Expression of truncated Sek-1 receptor tyrosine kinase disrupts the segmental restriction of gene expression in the Xenopus and zebrafish hindbrain. Development 1995, 121:4005-4016.
• [34]Lumsden A: The cellular basis of segmentation in the developing hindbrain. Trends Neurosci 1990, 13:329-335.
• [35]Maden M: Retinoic acid in the development, regeneration and maintenance of the nervous system. Nat Rev Neurosci 2007, 8:755-765.
• [36]Lumsden A, Sprawson N, Graham A: Segmental origin and migration of neural crest cells in the hindbrain region of the chick embryo. Development 1991, 113:1281-1291.
• [37]Schilling TF, Kimmel CB: Segment and cell type lineage restrictions during pharyngeal arch development in the zebrafish embryo. Development 1994, 120:483-494.
• [38]Begbie J, Graham A: Integration between the epibranchial placodes and the hindbrain. Science 2001, 294:595-598.
• [39]Graham A, Richardson J: Developmental and evolutionary origins of the pharyngeal apparatus. EvoDevo 2012, 3:24. BioMed Central Full Text
• [40]Veitch E, Begbie J, Schilling TF, Smith MM, Graham A: Pharyngeal arch patterning in the absence of neural crest. Curr Biol 1999, 9:1481-1484.
• [41]Crump JG, Swartz ME, Kimmel CB: An integrin-dependent role of pouch endoderm in hyoid cartilage development. PLoS Biol 2004, 2:E244.
• [42]Piotrowski T, Nusslein-Volhard C: The endoderm plays an important role in patterning the segmented pharyngeal region in zebrafish (Danio rerio). Dev Biol 2000, 225:339-356.
• [43]Crump JG, Maves L, Lawson ND, Weinstein BM, Kimmel CB: An essential role for Fgfs in endodermal pouch formation influences later craniofacial skeletal patterning. Development 2004, 131:5703-5716.
• [44]Niederreither K, Subbarayan V, Dolle P, Chambon P: Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat Genet 1999, 21:444-448.
• [45]Quinlan R, Gale E, Maden M, Graham A: Deficits in the posterior pharyngeal endoderm in the absence of retinoids. Dev Dyn 2002, 225:54-60.
• [46]Begemann G, Schilling TF, Rauch GJ, Geisler R, Ingham PW: The zebrafish neckless mutation reveals a requirement for raldh2 in mesodermal signals that pattern the hindbrain. Development 2001, 128:3081-3094.
• [47]Choe CP, Collazo A, le Trinh A, Pan L, Moens CB, Crump JG: Wnt-dependent epithelial transitions drive pharyngeal pouch formation. Dev Cell 2013, 24:296-309.
• [48]Xu H, Cerrato F, Baldini A: Timed mutation and cell-fate mapping reveal reiterated roles of Tbx1 during embryogenesis, and a crucial function during segmentation of the pharyngeal system via regulation of endoderm expansion. Development 2005, 132:4387-4395.
• [49]Irving C, Mason I: Signalling by FGF8 from the isthmus patterns anterior hindbrain and establishes the anterior limit of Hox gene expression. Development 2000, 127:177-186.
• [50]Maves L, Jackman W, Kimmel CB: FGF3 and FGF8 mediate a rhombomere 4 signaling activity in the zebrafish hindbrain. Development 2002, 129:3825-3837.
• [51]Bertrand S, Camasses A, Somorjai I, Belgacem MR, Chabrol O, Escande ML, Pontarotti P, Escriva H: Amphioxus FGF signaling predicts the acquisition of vertebrate morphological traits. Proc Natl Acad Sci U S A 2011, 108:9160-9165.
• [52]Wada H, Garcia-Fernandez J, Holland PW: Colinear and segmental expression of amphioxus Hox genes. Dev Biol 1999, 213:131-141.
• [53]Knight RD, Panopoulou GD, Holland PW, Shimeld SM: An amphioxus Krox gene: insights into vertebrate hindbrain evolution. Dev Genes Evol 2000, 210:518-521.
• [54]Holland LZ, Holland ND: Expression of AmphiHox-1 and AmphiPax-1 in amphioxus embryos treated with retinoic acid: insights into evolution and patterning of the chordate nerve cord and pharynx. Development 1996, 122:1829-1838.
• [55]Kozmik Z, Holland ND, Kreslova J, Oliveri D, Schubert M, Jonasova K, Holland LZ, Pestarino M, Benes V, Candiani S: Pax-Six-Eya-Dach network during amphioxus development: conservation in vitro but context specificity in vivo. Dev Biol 2007, 306:143-159.
• [56]Mahadevan NR, Horton AC, Gibson-Brown JJ: Developmental expression of the amphioxus Tbx1/ 10 gene illuminates the evolution of vertebrate branchial arches and sclerotome. Dev Genes Evol 2004, 214:559-566.
• [57]Gillis JA, Fritzenwanker JH, Lowe CJ: A stem-deuterostome origin of the vertebrate pharyngeal transcriptional network. Proc Biol Sci 2012, 279:237-246.
• [58]Smith AB: The pre-radial history of the echinoderms. Geol J 2005, 40:255-280.
• [59]Stollewerk A, Schoppmeier M, Damen WG: Involvement of Notch and Delta genes in spider segmentation. Nature 2003, 423:863-865.
• [60]Petersen CP, Reddien PW: Smed-betacatenin-1 is required for anteroposterior blastema polarity in planarian regeneration. Science 2008, 319:327-330.
• [61]Janssen R, Le Gouar M, Pechmann M, Poulin F, Bolognesi R, Schwager EE, Hopfen C, Colbourne JK, Budd GE, Brown SJ, Prpic N-M, Kosiol C, Vervoort M, Damen WGM, Balavoine G, McGregor AP: Conservation, loss, and redeployment of Wnt ligands in protostomes: implications for understanding the evolution of segment formation. BMC Evol Biol 2010, 10:374. BioMed Central Full Text