Multicellularity arose several times in the evolution of eukaryotes

BioEssays

Volumn 35, Issue 4, 2013, Pages 339-347

  Parfrey, Laura Wegener ^a   Lahr, Daniel J G ^b  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Amoebozoa; Catenin; Dictyostelium; Metazoa; Microbial eukaryote; Opisthokonta; Vinculin

Indexed keywords

ALPHA CATENIN; BETA CATENIN; CADHERIN; WNT PROTEIN;

ARTICLE; CELL ADHESION; CELL AGGREGATION; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL DIVISION; CELL ELONGATION; CELL FUNCTION; CELL INTERACTION; CELL JUNCTION; CELL LINEAGE; CELL MOTILITY; CELL STRUCTURE; CLADISTICS; DICTYOSTELIUM; EUKARYOTE EVOLUTION; HUMAN; NONHUMAN; PHYLOGENY; SEQUENCE HOMOLOGY; STRUCTURE ANALYSIS;

ANIMALS; CELL POLARITY; DICTYOSTELIUM; EPITHELIAL CELLS; HUMANS;

ACRASIDA; AMOEBOZOA; ANIMALIA; DICTYOSTELIIDA; DICTYOSTELIUM; EUKARYOTA; FUNGI; FUNGI/METAZOA GROUP; METAZOA; UNIKONTA;

EID: 84874958863     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201200143     Document Type: Article

References (75)

1. Kessin R. 2001. Dictyostelium: Evolution, Cell Biology, and the Development of Multicellularity. Cambridge: Cambridge University Press. 284 p.
2. Williams RS, Boeckeler K, Graf R, Muller-Taubenberger A, et al. 2006. Towards a molecular understanding of human diseases using Dictyostelium discoideum. Trends Mol Med 12: 415- 24.
3. Urushihara H. 2008. Developmental biology of the social amoeba: history, current knowledge and prospects. Dev Growth Differ 50: S277- 81.
4. Romeralo M, Escalante R, Baldauf SL. 2012. Evolution and diversity of dictyostelid social amoebae. Protist 163: 327- 43.
5. Lahr DJ, Grant J, Nguyen T, Lin JH, et al. 2011. Comprehensive phylogenetic reconstruction of amoebozoa based on concatenated analyses of SSU-rDNA and actin genes. PLoS ONE 6: e22780.
6. Heidel AJ, Lawal HM, Felder M, Schilde C, et al. 2011. Phylogeny-wide analysis of social amoeba genomes highlights ancient origins for complex intercellular communication. Genome Res 21: 1882- 91.
7. Dickinson DJ, Nelson WJ, Weis WI. 2012. An epithelial tissue in Dictyostelium challenges the traditional origin of metazoan multicellularity. BioEssays 34: 833- 40.
8. Parfrey LW, Lahr DJ, Knoll AH, Katz LA. 2011. Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc Natl Acad Sci USA 108: 13624- 9.
9. Eichinger L, Pachebat JA, Glockner G, Rajandream MA, et al. 2005. The genome of the social amoeba Dictyostelium discoideum. Nature 435: 43- 57.
10. Abedin M, King N. 2010. Diverse evolutionary paths to cell adhesion. Trends Cell Biol 20: 734- 42.
11. Dickinson DJ, Nelson WJ, Weis WI. 2011. A polarized epithelium organized by beta- and alpha-catenin predates cadherin and metazoan origins. Science 331: 1336- 9.
12. Knoll AH. 2011. The multiple origins of complex multicellularity. Annu Rev Earth Pl Sci 39: 217- 39.
13. Grosberg RK, Strathmann RR. 2007. The evolution of multicellularity: a minor major transition? Annu Rev Ecol Evol Syst 38: 621- 54.
14. Leys SP, Nichols SA, Adams ED. 2009. Epithelia and integration in sponges. Integr Comp Biol 49: 167- 77.
15. Magie CR, Martindale MQ. 2008. Cell-cell adhesion in the cnidaria: insights into the evolution of tissue morphogenesis. Biol Bull 214: 218- 32.
16. Niessen CM. 2007. Tight junctions/adherens junctions: basic structure and function. J Invest Dermatol 127: 2525- 32.
17. Grimson MJ, Coates JC, Reynolds JP, Shipman M, et al. 2000. Adherens junctions and [beta]-catenin-mediated cell signalling in a non-metazoan organism. Nature 408: 727- 31.
18. Coates JC, Harwood AJ. 2001. Cell-cell adhesion and signal transduction during Dictyostelium development. J Cell Sci 114: 4349- 58.
19. Coates JC, Grimson MJ, Williams RS, Bergman W, et al. 2002. Loss of the beta-catenin homologue aardvark causes ectopic stalk formation in Dictyostelium. Mech Dev 116: 117- 27.
20. Zhao Z-M, Reynolds A, Gaucher E. 2011. The evolutionary history of the catenin gene family during metazoan evolution. BMC Evol Biol 11: 198.
21. Schneider SQ, Finnerty JR, Martindale MQ. 2003. Protein evolution: structure-function relationships of the oncogene beta-catenin in the evolution of multicellular animals. J Exp Zool B Mol Dev Evol 295: 25- 44.
22. Kobielak A, Fuchs E. 2004. Alpha-catenin: at the junction of intercellular adhesion and actin dynamics. Nat Rev Mol Cell Biol 5: 614- 25.
23. Sebe-Pedros A, Roger AJ, Lang FB, King N, et al. 2010. Ancient origin of the integrin-mediated adhesion and signaling machinery. Proc Natl Acad Sci USA 107: 10142- 7.
24. Wikramanayake AH, Hong M, Lee PN, Pang K, et al. 2003. An ancient role for nuclear [beta]-catenin in the evolution of axial polarity and germ layer segregation. Nature 426: 446- 50.
25. Katoh K, Toh H. 2008. Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9: 286- 98.
26. Penn O, Privman E, Ashkenazy H, Landan G, et al. 2010. GUIDANCE: a web server for assessing alignment confidence scores. Nucleic Acids Res 38: W23- 8.
27. Abascal F, Zardoya R, Posada D. 2005. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104- 5.
28. Stamatakis A, Hoover P, Rougemont J. 2008. A rapid bootstrap algorithm for the RAxML Web-servers. Syst Biol 57: 758- 71.
29. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572- 4.
30. Miller MA, Pfeiffer W, Schwartz T. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov 2010, New Orleans, LA pp. 1- 8.
31. Shimodaira H. 2002. An approximately unbiased test of phylogenetic tree selection. Syst Biol 51: 492- 508.
32. Shimodaira H. 2004. Approximately unbiased tests of regions using multistep-multiscale bootstrap resampling. Ann Stat 32: 2616- 41.
33. Shimodaira H, Hasegawa M. 2001. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17: 1246- 7.
34. Liu Y, Cotton JA, Shen B, Han X, et al. 2010. Convergent sequence evolution between echolocating bats and dolphins. Curr Biol 20: R53- 4.
35. Kornegay JR, Schilling JW, Wilson AC. 1994. Molecular adaptation of a leaf-eating bird: stomach lysozyme of the hoatzin. Mol Biol Evol 11: 921- 8.
36. Coates JC, Laplaze L, Haseloff J. 2006. Armadillo-related proteins promote lateral root development in Arabidopsis. Proc Natl Acad Sci USA 103: 1621- 6.
37. Moody L, Saidi Y, Smiles E, Bradshaw S, et al. 2012. ARABIDILLO gene homologues in basal land plants: species-specific gene duplication and likely functional redundancy. Planta 236: 1927- 41.
38. Patterson DJ. 1999. The diversity of eukaryotes. Am Nat 154: S96- 124.
39. Parfrey LW, Grant J, Tekle YI, Lasek-Nesselquist E, et al. 2010. Broadly sampled multigene analyses yield a well-resolved eukaryotic tree of life. Syst Biol 59: 518- 33.
40. Adl SM, Simpson AGB, Farmer MA, Andersen RA, et al. 2005. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 52: 399- 451.
41. Burki F, Okamoto N, Pombert JF, Keeling PJ. 2012. The evolutionary history of haptophytes and cryptophytes: phylogenomic evidence for separate origins. Proc Biol Sci 279: 2246- 54.
42. Adl SM, Simpson AGB, Lane CE, Lukeš J, et al. 2012. The revised classification of eukaryotes. J Euk Microbiol 59: 429- 514.
43. Bonner JT. 1998. The origins of multicellularity. Integrative Biol 1: 27- 36.
44. Blanton RL. 1990. Phylum acrasea. In Margulis L, Corliss JO, Melkonian M, Chapman DJ, eds; Handbook of Protoctista. Boston, MA: Jones and Bartlett. p. 75- 87.
45. Brown MW, Kolisko M, Silberman JD, Roger AJ. 2012. Aggregative multicellularity evolved independently in the eukaryotic supergroup Rhizaria. Curr Biol 22: 1123- 7.
46. Cavalier-Smith T. 2003. Protist phylogeny and the high-level classification of Protozoa. Euro J Protistol 39: 338- 48.
47. Roger AJ, Simpson AGB. 2009. Evolution: revisiting the root of the eukaryote tree. Curr Biol 19: R165- 7.
48. Katz LA, Grant J, Parfrey LW, Gant A, et al. 2011. Subulatomonas tetraspora nov. gen. nov. sp. is a member of a previously unrecognized major clade of eukaryotes. Protist 162: 762- 73.
49. Stechmann A, Cavalier-Smith T. 2002. Rooting the eukaryote tree by using a derived gene fusion. Science 297: 89- 91.
50. Katz LA, Grant JR, Parfrey LW, Burleigh JG. 2012. Turning the crown upside down: gene tree parsimony roots the eukaryotic tree of life. Syst Biol 61: 653- 60.
51. Stechmann A, Cavalier-Smith T. 2003. The root of the eukaryote tree pinpointed. Curr Biol 13: R665- 6.
52. Derelle R, Lang F. 2012. Rooting the eukaryotic tree with mitochondrial and bacterial proteins. Mol Biol Evol 29: 1277- 89.
53. Brown MW, Spiegel FW, Silberman JD. 2009. Phylogeny of the "forgotten" cellular slime mold, Fonticula alba, reveals a key evolutionary branch within Opisthokonta. Mol Biol Evol 26: 2699- 709.
54. Medina M, Collins A, Taylor J, Valentine J, et al. 2003. Phylogeny of Opisthokonta and the evolution of multicellularity and complexity in Fungi and Metazoa. Int J Astrobiol 2: 203- 11.
55. Torruella G, Derelle R, Paps J, Lang BF, et al. 2012. Phylogenetic relationships within the Opisthokonta based on phylogenomic analyses of conserved single-copy protein domains. Mol Biol Evol 29: 531- 44.
56. Hibbett DS, Binder M, Bischoff JF, Blackwell M, et al. 2007. A higher-level phylogenetic classification of the Fungi. Mycol Res 111: 509- 47.
57. Smirnov AV, Chao E, Nassonova ES, Cavalier-Smith T. 2011. A revised classification of naked lobose amoebae (Amoebozoa: lobosa). Protist 162: 545- 70.
58. Brown MW, Silberman JD, Spiegel FW. 2011. " Slime molds" among the Tubulinea (Amoebozoa): molecular systematics and taxonomy of Copromyxa. Protist 162: 277- 87.
59. Frederick L. 1990. Phylum plasmodial slime molds, class Myxomycota. In Margulis L, Corliss JO, Melkonian M, Chapman DJ, eds; Handbook of Protoctista. Boston: Jones and Bartlett. p. 467- 83.
60. Ratcliff WC, Denison RF, Borrello M, Travisano M. 2012. Experimental evolution of multicellularity. Proc Natl Acad Sci USA 109: 1595- 600.
61. Nichols SA, Roberts BW, Richter DJ, Fairclough SR, et al. 2012. Origin of metazoan cadherin diversity and the antiquity of the classical cadherin/beta-catenin complex. Proc Natl Acad Sci USA 109: 13046- 51.
62. Suga H, Dacre M, de Mendoza A, Shalchian-Tabrizi K, et al. 2012. Genomic survey of Premetazoans shows deep conservation of cytoplasmic tyrosine kinases and multiple radiations of receptor tyrosine kinases. Sci Signal 5: ra35.
63. Sebe-Pedros A, de Mendoza A, Lang BF, Degnan BM, et al. 2011. Unexpected repertoire of metazoan transcription factors in the unicellular holozoan Capsaspora owczarzaki. Mol Biol Evol 28: 1241- 54.
64. Sebe-Pedros A, Ruiz-Trillo I. 2010. Integrin-mediated adhesion complex: cooption of signaling systems at the dawn of Metazoa. Commun Integr Biol 3: 475- 7.
65. Mikhailov KV, Konstantinova AV, Nikitin MA, Troshin PV, et al. 2009. The origin of Metazoa: a transition from temporal to spatial cell differentiation. BioEssays 31: 758- 68.
66. Ohno S. 1970. Evolution by Gene Duplication. New York: Spinger-Verlag.
67. Zhang J. 2003. Evolution by gene duplication: an update. Trends Ecol Evol 18: 292- 8.
68. Lynch M, Conery JS. 2000. The evolutionary fate and consequences of duplicate genes. Science 290: 1151- 5.
69. Walsh JB. 1995. How often do duplicated genes evolve new functions? Genetics 139: 421- 8.
70. Nei M, Rogozin IB, Piontkivska H. 2000. Purifying selection and birth-and-death evolution in the ubiquitin gene family. Proc Natl Acad Sci USA 97: 10866- 71.
71. De Smet R, Van de Peer Y. 2012. Redundancy and rewiring of genetic networks following genome-wide duplication events. Curr Opin Plant Biol 15: 168- 76.
72. Qiu H, Yang EC, Bhattacharya D, Yoon HS. 2012. Ancient gene paralogy may mislead inference of plastid phylogeny. Mol Biol Evol 29: 3333- 43.
73. Maddison WP. 1997. Gene trees in species trees. Syst Biol 46: 523- 36.
74. Olive LS, Blanton RL. 1980. Aerial sorocarp development by the aggregative ciliate Sorogena stoianovitchae. J Protozool 27: 293- 9.
75. Dykstra MJ, Olive LS. 1975. Sorodiplophrys - unusual sorocarp producing protist. Mycologia 67: 873- 9.