HOX gene complement and expression in the planarian Schmidtea mediterranea

EvoDevo

Volumn 7, Issue 1, 2016, Pages

  Currie, Ko W ^a,b   Brown, David D R ^a,b   Zhu, Shujun ^a,b   Xu, ChangJiang ^b   Voisin, Veronique ^b   Bader, Gary D ^b   Pearson, Bret J ^a,b,c  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c ONTARIO INSTITUTE FOR CANCER RESEARCH   (Canada)

Author keywords

Body plan; Flatworm; Homeotic; HOX; In situ hybridization; Lophotrochozoan; Planarians; Schmidtea mediterranea

Indexed keywords

EID: 84962802389     PISSN: None     EISSN: 20419139     Source Type: Journal    
DOI: 10.1186/s13227-016-0044-8     Document Type: Article

References (72)

1. Wellik DM. Hox genes and vertebrate axial pattern. Curr Top Dev Biol. 2009;88:257-78.
2. Foronda D, de Navas LF, Garaulet DL, Sanchez-Herrero E. Function and specificity of Hox genes. Int J Dev Biol. 2009;53(8-10):1404-19.
3. Olson PD. Hox genes and the parasitic flatworms: new opportunities, challenges and lessons from the free-living. Parasitol Int. 2008;57(1):8-17.
4. Monteiro AS, Ferrier DE. Hox genes are not always colinear. Int J Biol Sci. 2006;2(3):95-103.
5. Morgan R. Hox genes: a continuation of embryonic patterning? Trends Genet. 2006;22(2):67-9.
6. Holland PW. Evolution of homeobox genes. Wiley Interdiscip Rev Dev Biol. 2013;2(1):31-45.
7. Postlethwait JH, Schneiderman HA. A clonal analysis of determination in Antennapedia a homoeotic mutant of Drosophila melanogaster. Proc Natl Acad Sci USA. 1969;64(1):176-83.
8. Durston AJ, Jansen HJ, der Rieden PI, Hooiveld MH. Hox collinearity-a new perspective. Int J Dev Biol. 2011;55(10-12):899-908.
9. Lewis EB. A gene complex controlling segmentation in Drosophila. Nature. 1978;276(5688):565-70.
10. Duboule D. The rise and fall of Hox gene clusters. Development. 2007;134(14):2549-60.
11. Albertin CB, Simakov O, Mitros T, Wang ZY, Pungor JR, Edsinger-Gonzales E, Brenner S, Ragsdale CW, Rokhsar DS. The octopus genome and the evolution of cephalopod neural and morphological novelties. Nature. 2015;524(7564):220-4.
12. Mallo M, Wellik DM, Deschamps J. Hox genes and regional patterning of the vertebrate body plan. Dev Biol. 2010;344(1):7-15.
13. Hughes CL, Kaufman TC. Hox genes and the evolution of the arthropod body plan. Evol Dev. 2002;4(6):459-99.
14. de Rosa R, Grenier JK, Andreeva T, Cook CE, Adoutte A, Akam M, Carroll SB, Balavoine G. Hox genes in brachiopods and priapulids and protostome evolution. Nature. 1999;399(6738):772-6.
15. De Robertis EM. Evo-devo: variations on ancestral themes. Cell. 2008;132(2):185-95.
16. Berriman M, Haas BJ, LoVerde PT, Wilson RA, Dillon GP, Cerqueira GC, Mashiyama ST, Al-Lazikani B, Andrade LF, Ashton PD, et al. The genome of the blood fluke Schistosoma mansoni. Nature. 2009;460(7253):352-8.
17. Zheng H, Zhang W, Zhang L, Zhang Z, Li J, Lu G, Zhu Y, Wang Y, Huang Y, Liu J, et al. The genome of the hydatid tapeworm Echinococcus granulosus. Nat Genet. 2013;45(10):1168-75.
18. Koziol U, Lalanne AI, Castillo E. Hox genes in the parasitic platyhelminthes Mesocestoides corti, Echinococcus multilocularis, and Schistosoma mansoni: evidence for a reduced Hox complement. Biochem Genet. 2009;47(1-2):100-16.
19. Aboobaker AA, Blaxter ML. Hox gene loss during dynamic evolution of the nematode cluster. Curr Biol. 2003;13(1):37-40.
20. Amores A, Force A, Yan YL, Joly L, Amemiya C, Fritz A, Ho RK, Langeland J, Prince V, Wang YL, et al. Zebrafish hox clusters and vertebrate genome evolution. Science. 1998;282(5394):1711-4.
21. Hoegg S, Meyer A. Hox clusters as models for vertebrate genome evolution. Trends Genet. 2005;21(8):421-4.
22. Barber BA, Rastegar M. Epigenetic control of Hox genes during neurogenesis, development, and disease. Ann Anat. 2010;192(5):261-74.
23. Di Bonito M, Glover JC, Studer M. Hox genes and region-specific sensorimotor circuit formation in the hindbrain and spinal cord. Dev Dyn. 2013;242(12):1348-68.
24. Ruiz-Trillo I, Riutort M, Littlewood DT, Herniou EA, Baguna J. Acoel flatworms: earliest extant bilaterian metazoans, not members of Platyhelminthes. Science. 1999;283(5409):1919-23.
25. Morgan TH. Regeneration in planarians. Archiv Entwick Mech. 1900;10:58-119.
26. Pearson BJ, Alvarado AS. A planarian p53 homolog regulates proliferation and self-renewal in adult stem cell lineages. Development. 2010;137(2):213-21.
27. Gurley KA, Rink JC, Alvarado AS. Beta-catenin defines head versus tail identity during planarian regeneration and homeostasis. Science. 2008;319(5861):323-7.
28. Hyman LH. The invertebrates vol 2: platyhelminthes and rhynchocoela the acoelomate bilateria. [S.l.]. New York: McGraw-Hill; 1951.
29. Newmark PA, Alvarado AS. Not your father's planarian: a classic model enters the era of functional genomics. Nat Rev Genet. 2002;3(3):210-9.
30. Hejnol A, Martindale MQ. Acoel development indicates the independent evolution of the bilaterian mouth and anus. Nature. 2008;456(7220):382-6.
31. Martin-Duran JM, Romero R. Evolutionary implications of morphogenesis and molecular patterning of the blind gut in the planarian Schmidtea polychroa. Dev Biol. 2011;352(1):164-76.
32. Bayascas JR, Castillo E, Munoz-Marmol AM, Salo E. Planarian Hox genes: novel patterns of expression during regeneration. Development. 1997;124(1):141-8.
33. Nogi T, Watanabe K. Position-specific and non-colinear expression of the planarian posterior (Abdominal-B-like) gene. Dev Growth Differ. 2001;43(2):177-84.
34. Orii H, Kato K, Umesono Y, Sakurai T, Agata K, Watanabe K. The planarian HOM/HOX homeobox genes (Plox) expressed along the anteroposterior axis. Dev Biol. 1999;210(2):456-68.
35. Balavoine G, Telford MJ. Identification of planarian homeobox sequences indicates the antiquity of most Hox/homeotic gene subclasses. Proc Natl Acad Sci USA. 1995;92(16):7227-31.
36. Iglesias M, Gomez-Skarmeta JL, Salo E, Adell T. Silencing of Smed-betacatenin1 generates radial-like hypercephalized planarians. Development. 2008;135(7):1215-21.
37. Martin-Duran JM, Amaya E, Romero R. Germ layer specification and axial patterning in the embryonic development of the freshwater planarian Schmidtea polychroa. Dev Biol. 2010;340(1):145-58.
38. van Wolfswinkel JC, Wagner DE, Reddien PW. Single-cell analysis reveals functionally distinct classes within the planarian stem cell compartment. Cell Stem Cell. 2014;15(3):326-39.
39. Witchley JN, Mayer M, Wagner DE, Owen JH, Reddien PW. Muscle cells provide instructions for planarian regeneration. Cell Rep. 2013;4(4):633-41.
40. Petersen CP, Reddien PW. Smed-betacatenin-1 is required for anteroposterior blastema polarity in planarian regeneration. Science. 2008;319(5861):327-30.
41. Alvarado AS, Newmark PA, Robb SM, Juste R. The Schmidtea mediterranea database as a molecular resource for studying platyhelminthes, stem cells and regeneration. Development. 2002;129(24):5659-65.
42. Currie KW, Pearson BJ. Transcription factors lhx1/5-1 and pitx are required for the maintenance and regeneration of serotonergic neurons in planarians. Development. 2013;140(17):3577-88.
43. Robb SM, Gotting K, Ross E, Alvarado AS. SmedGD 2.0: The Schmidtea mediterranea genome database. Genesis. 2015;53(8):535-46.
44. Labbe RM, Irimia M, Currie KW, Lin A, Zhu SJ, Brown DD, Ross EJ, Voisin V, Bader GD, Blencowe BJ, et al. A comparative transcriptomic analysis reveals conserved features of stem cell pluripotency in planarians and mammals. Stem Cells. 2012;30(8):1734-45.
45. Sandmann T, Vogg MC, Owlarn S, Boutros M, Bartscherer K. The head-regeneration transcriptome of the planarian Schmidtea mediterranea. Genome Biol. 2011;12(8):R76.
46. Zhu SJ, Hallows SE, Currie KW, Xu C, Pearson BJ. A mex3 homolog is required for differentiation during planarian stem cell lineage development. Elife. 2015;4:e07025.
47. Zhong YF, Butts T, Holland PW. HomeoDB: a database of homeobox gene diversity. Evol Dev. 2008;10(5):516-8.
48. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772-80.
49. Lauter G, Soll I, Hauptmann G. Two-color fluorescent in situ hybridization in the embryonic zebrafish brain using differential detection systems. BMC Dev Biol. 2011;11:43.
50. Pearson BJ, Eisenhoffer GT, Gurley KA, Rink JC, Miller DE, Alvarado AS. Formaldehyde-based whole-mount in situ hybridization method for planarians. Dev Dyn. 2009;238(2):443-50.
51. King RS, Newmark PA. In situ hybridization protocol for enhanced detection of gene expression in the planarian Schmidtea mediterranea. BMC Dev Biol. 2013;13:8.
52. Nikolayeva O, Robinson MD. edgeR for differential RNA-seq and ChIP-seq analysis: an application to stem cell biology. Methods Mol Biol. 2014;1150:45-79.
53. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26(1):139-40.
54. Robb SM, Ross E, Alvarado AS. SmedGD: the Schmidtea mediterranea genome database. Nucleic Acids Res. 2008;36(Database issue):D599-606.
55. Alvarado AS, Reddien PW, Newmark P, Nusbaum C: Proposal for the sequencing of a new target genome: white paper for a planarian genome project. 2003.
56. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19(12):1572-4.
57. Guindon S, Delsuc F, Dufayard JF, Gascuel O. Estimating maximum likelihood phylogenies with PhyML. Methods Mol Biol. 2009;537:113-37.
58. Falciani F, Hausdorf B, Schroder R, Akam M, Tautz D, Denell R, Brown S. Class 3 Hox genes in insects and the origin of zen. Proc Natl Acad Sci USA. 1996;93(16):8479-84.
59. Callaerts P, Lee PN, Hartmann B, Farfan C, Choy DW, Ikeo K, Fischbach KF, Gehring WJ, de Couet HG. HOX genes in the sepiolid squid Euprymna scolopes: implications for the evolution of complex body plans. Proc Natl Acad Sci USA. 2002;99(4):2088-93.
60. Kourakis MJ, Master VA, Lokhorst DK, Nardelli-Haefliger D, Wedeen CJ, Martindale MQ, Shankland M. Conserved anterior boundaries of Hox gene expression in the central nervous system of the leech Helobdella. Dev Biol. 1997;190(2):284-300.
61. Balavoine G, de Rosa R, Adoutte A. Hox clusters and bilaterian phylogeny. Mol Phylogenet Evol. 2002;24(3):366-73.
62. Kulakova MA, Kostyuchenko RP, Andreeva TF, Dondua AK. The abdominal-B-like gene expression during larval development of Nereis virens (polychaeta). Mech Dev. 2002;115(1-2):177-9.
63. Cook CE, Jimenez E, Akam M, Salo E. The Hox gene complement of acoel flatworms, a basal bilaterian clade. Evol Dev. 2004;6(3):154-63.
64. Kulakova M, Bakalenko N, Novikova E, Cook CE, Eliseeva E, Steinmetz PR, Kostyuchenko RP, Dondua A, Arendt D, Akam M, et al. Hox gene expression in larval development of the polychaetes Nereis virens and Platynereis dumerilii (Annelida, Lophotrochozoa). Dev Genes Evol. 2007;217(1):39-54.
65. Mango SE, Lambie EJ, Kimble J. The pha-4 gene is required to generate the pharyngeal primordium of Caenorhabditis elegans. Development. 1994;120(10):3019-31.
66. Kaestner KH. The hepatocyte nuclear factor 3 (HNF3 or FOXA) family in metabolism. Trends Endocrinol Metab. 2000;11(7):281-5.
67. Adler CE, Seidel CW, McKinney SA, Alvarado AS. Selective amputation of the pharynx identifies a FoxA-dependent regeneration program in planaria. Elife (Cambridge). 2014;3:e02238.
68. Koinuma S, Umesono Y, Watanabe K, Agata K. Planaria FoxA (HNF3) homologue is specifically expressed in the pharynx-forming cells. Gene. 2000;259(1-2):171-6.
69. Felix DA, Aboobaker AA. The TALE class homeobox gene Smed-prep defines the anterior compartment for head regeneration. PLoS Genet. 2010;6(4):e1000915.
70. Reuter H, Marz M, Vogg MC, Eccles D, Grifol-Boldu L, Wehner D, Owlarn S, Adell T, Weidinger G, Bartscherer K. Beta-catenin-dependent control of positional information along the AP body axis in planarians involves a teashirt family member. Cell Rep. 2015;10(2):253-65.
71. Handberg-Thorsager M, Salo E. The planarian nanos-like gene Smednos is expressed in germline and eye precursor cells during development and regeneration. Dev Genes Evol. 2007;217(5):403-11.
72. Wang Y, Zayas RM, Guo T, Newmark PA. Nanos function is essential for development and regeneration of planarian germ cells. Proc Natl Acad Sci USA. 2007;104(14):5901-6.