The number of cell types, information content, and the evolution of complex multicellularity

• Autorzy: Niklas K. J. , Cobb E. D. , Dunker A. K.
• Języki publikacji: EN

Abstrakty

EN

The number of different cell types (NCT) characterizing an organism is often used to quantify organismic complexity. This method results in the tautology that more complex organisms have a larger number of different kinds of cells, and that organisms with more different kinds of cells are more complex. This circular reasoning can be avoided (and simultaneously tested) when NCT is plotted against different measures of organismic information content (e.g., genome or proteome size). This approach is illustrated by plotting the NCT of representative diatoms, green and brown algae, land plants, invertebrates, and vertebrates against data for genome size (number of base-pairs), proteome size (number of amino acids), and proteome functional versatility (number of intrinsically disordered protein domains or residues). Statistical analyses of these data indicate that increases in NCT fail to keep pace with increases in genome size, but exceed a one-to-one scaling relationship with increasing proteome size and with increasing numbers of intrinsically disordered protein residues. We interpret these trends to indicate that comparatively small increases in proteome (and not genome size) are associated with disproportionate increases in NCT, and that proteins with intrinsically disordered domains enhance cell type diversity and thus contribute to the evolution of complex multicellularity.

Słowa kluczowe

EN

cell type; information content; evolution; multicellularity; alga; embryophyte; genome size; land plant

• Wydawca: -
• Czasopismo: Acta Societatis Botanicorum Poloniae
• Rocznik: 2014
• Tom: 83
• Numer: 4
• Opis fizyczny: p.337-347,fig.,ref.

Twórcy

autor

Niklas K. J.

• Section of Plant Biology, School of Integrative Plant Science, Cornell University, Ithaca, NY 14853, USA

autor

Cobb E. D.

• Section of Plant Biology, School of Integrative Plant Science, Cornell University, Ithaca, NY 14853, USA

autor

Dunker A. K.

• Center for Computational Biology and Bioinformatics, School of Medicine, Indiana University, Indianapolis, IN 46202, USA

Bibliografia

• 1. Valentine JW, Collins AG, Meyer CP. Morphological complexity increase in metazoans. Paleobiology. 1994;20(2):131–142.
• 2. Bell G. Size and complexity among multicellular organisms. Biol J Linn Soc. 1997;60(3):345–363. http://dx.doi.org/10.1006/bijl.1996.0108
• 3. Erwin DH. Early origin of the bilaterian developmental toolkit. Phil Trans R Soc B. 2009;364(1527):2253–2261. http://dx.doi.org/10.1098/rstb.2009.0038
• 4. Chen L, Bush SJ, Tovar-Corona JM, Castillo-Morales A, Urrutia AO. Correcting for differential transcript coverage reveals a strong relationshipbetween alternative splicing and organism complexity. Mol BiolEvol. 2014;31:1402–1413. http://dx.doi.org/10.1093/molbev/msu083
• 5. Schad E, Tompa P, Hegyi H. The relationship between proteome size, structural disorder and organism complexity. Genome Biol. 2011;12:R120. http://dx.doi.org/10.1186/gb-2011-12-12-r120
• 6. Liu J, Perumal NB, Oldfield CJ, Su EW, Uversky VN, Dunker AK. Intrinsic disorder in transcription factors. Biochemistry (Mosc). 2006;45(22):6873–6888. http://dx.doi.org/10.1021/bi0602718
• 7. Oldfield CJ, Meng J, Yang JY, Yang MQ, Uversky VN, Dunker AK. Flexible nets: disorder and induced fit in the associations of p53 and14-3-3 with their partners. BMC Genomics. 2008;9(1 suppl):S1. http://dx.doi.org/10.1186/1471-2164-9-S1-S1
• 8. Tompa P, Fuxreiter M. Fuzzy complexes: polymorphism and structural disorder in protein-protein interactions. Trends Biochem Sci. 2008;33(1):2–8. http://dx.doi.org/10.1016/j.tibs.2007.10.003
• 9. Bonner JT. First signals: the evolution of multicellular development. Princeton, NJ: Princeton University Press; 2000.
• 10. Kirk DL. A twelve-step program for evolving multicellularity and a division of labor. Bioessays. 2005;27(3):299–310. http://dx.doi.org/10.1002/bies.20197
• 11. Herron MD, Michod RE. Evolution of complexity in the volvocine algae: transitions in individuality through Darwin’s eye. Evolution. 2008;62(2):436–451. http://dx.doi.org/10.1111/j.1558-5646.2007.00304.x
• 12. Folse HJ, Roughgarden J. What is an individual organism? A multilevel selection perspective. Q Rev Biol. 2010;85(4):447–472.
• 13. Niklas KJ. The evolutionary-developmental origins of multicellularity. Am J Bot. 2014;101(1):6–25. http://dx.doi.org/10.3732/ajb.1300314
• 14. Silberfeld T, Leigh JW, Verbruggen H, Cruaud C, de Reviers B, Rousseau F. A multi-locus time-calibrated phylogeny of the brownalgae (Heterokonta, Ochrophyta, Phaeophyceae): investigatingthe evolutionary nature of the “brown algal crown radiation”. MolPhylogenet Evol. 2010;56(2):659–674. http://dx.doi.org/10.1016/j.ympev.2010.04.020
• 15. Andersen RA. Biology and systematics of heterokont and haptophyte algae. Am J Bot. 2004;91(10):1508–1522. http://dx.doi.org/10.3732/ajb.91.10.1508
• 16. Graham LE. Algae. 2nd ed. San Francisco, CA: Pearson/Benjamin Cummings; 2009.
• 17. Parker BC. Translocation in the giant kelp Macrocystis. I. Rates, direction, quantity of C14-labeled products and fluorescein. J Phycol.1965;1(2):41–46. http://dx.doi.org/10.1111/j.1529-8817.1965.tb04554.x
• 18. Parker BC. Translocation in Macrocystis. III. Composition of sieve tube exudate and identification of the major C14-labeled products. J Phycol.1966;2(1):38–41. http://dx.doi.org/10.1111/j.1529-8817.1966.tb04590.x
• 19. Buggeln RG, Fensom DS, Emerson CJ. Translocation of 14C-photoassimilate in the blade of Macrocystis pyrifera (Phaeophyceae). J Phycol.1985;21(1):35–40. http://dx.doi.org/10.1111/j.0022-3646.1985.00035.x
• 20. Ruhfel BR, Gitzendanner MA, Soltis PS, Soltis DE, Burleigh JG. From algae to angiosperms-inferring the phylogeny of green plants(Viridiplantae) from 360 plastid genomes. BMC Evol Biol. 2014;14:23.http://dx.doi.org/10.1186/1471-2148-14-23
• 21. Cook M, Graham L, Botha C, Lavin C. Comparative ultrastructure of plasmodesmata of Chara and selected bryophytes: toward an elucidation of the evolutionary origin of plant plasmodesmata. Am J Bot. 1997;84(9):1169–1178.
• 22. Boot KJM, Libbenga KR, Hille SC, Offringa R, van Duijn B. Polar auxin transport: an early invention. J Exp Bot. 2012;63(11):4213–4218.http://dx.doi.org/10.1093/jxb/ers106
• 23. Foster AS. Comparative morphology of vascular plants. 2nd ed. San Francisco, CA: W.H. Freeman; 1974.
• 24. Govindarajalu E. The systematic anatomy of south Indian Cyperaceae. Bot J Linn Soc. 1969;62:27–40.
• 25. Adoutte A, Balavoine G, Lartillot N, Lespinet O, Prud’homme B, de Rosa R. The new animal phylogeny: reliability and implications. ProcNatl Acad Sci USA. 2000;97(9):4453–4456. http://dx.doi.org/10.1073/pnas.97.9.4453
• 26. Chang CY, Lin WD, Tu SL. Genome-wide analysis of heat-sensitive alternative splicing in Physcomitrella patens. Plant Physiol. 2014;165:826–840. http://dx.doi.org/10.1104/pp.113.230540
• 27. Pan Q, Shai O, Lee LJ, Frey BJ, Blencowe BJ. Deep surveying of alternative splicing complexity in the human transcriptome by highthroughput sequencing. Nat Genet. 2008;40(12):1413–1415. http://dx.doi.org/10.1038/ng.259
• 28. Johnson JM, Castle J, Garrett-Engele P, Kan Z, Loerch PM, Armour CD, et al. Genome-wide survey of human alternative pre-mRNA splicingwith exon junction microarrays. Science. 2003;302(5653):2141–2144.http://dx.doi.org/10.1126/science.1090100
• 29. Liu J, Perumal NB, Oldfield CJ, Su EW, Uversky VN, Dunker AK. Intrinsic disorder in transcription factors. Biochemistry (Mosc). 2006;45(22):6873–6888. http://dx.doi.org/10.1021/bi0602718
• 30. Niklas KJ. Plant allometry: the scaling of form and process. Chicago, IL: University of Chicago Press; 1994.
• 31. Hahn MW, Wray GA. The g-value paradox. Evol Dev. 2002;4(2):73–75. http://dx.doi.org/10.1046/j.1525-142X.2002.01069.x
• 32. Lang D, Weiche B, Timmerhaus G, Richardt S, Riaño-Pachón DM, Corrêa LGG, et al. Genome-wide phylogenetic comparative analysisof plant transcriptional regulation: a timeline of loss, gain, expansion,and correlation with complexity. Genome Biol Evol. 2010;2:488–503.http://dx.doi.org/10.1093/gbe/evq032
• 33. Niklas KJ, Cobb ED, Crawford DR. The evo-devo of multinucleate cells, tissues, and organisms, and an alternative route to multicellularity.Evol Dev. 2013;15(6):466–474. http://dx.doi.org/10.1111/ede.12055
• 34. Niklas KJ, Newman SA. The origins of multicellular organisms. Evol Dev. 2013;15(1):41–52. http://dx.doi.org/10.1111/ede.12013
• 35. Buss LW. The evolution of individuality. Princeton, NJ: Princeton University Press; 1987.
• 36. Michod RE. Evolution of the individual. Am Nat. 1997;150 suppl 1:S5–S21. http://dx.doi.org/10.1086/286047
• 37. Schlichting CD. Origins of differentiation via phenotypic plasticity. Evol Dev. 2003;5(1):98–105.
• 38. Knoll AH. The multiple origins of complex multicellularity. Annu Rev Earth Planet Sci. 2011;39(1):217–239. http://dx.doi.org/10.1146/annurev.earth.031208.100209
• 39. Britten RJ, Davidson EH. Gene regulation for higher cells: a theory. Science. 1969;165(3891):349–357.
• 40. Laurent M, Kellershohn N. Multistability: a major means of differentiation and evolution in biological systems. Trends Biochem Sci.1999;24(11):418–422.
• 41. Jaeger J, Monk N. Bioattractors: dynamical systems theory and the evolution of regulatory processes. J Physiol. 2014;592(11):2267–2281. http://dx.doi.org/10.1113/jphysiol.2014.272385
• 42. Ispolatov I, Ackermann M, Doebeli M. Division of labour and the evolution of multicellularity. Proc R Soc B. 2012;274:1768–1776.http://dx.doi.org/10.1098/rspb.2011.1999
• 43. Yao Q, Gao J, Bollinger C, Thelen JJ, Xu D. Predicting and analyzing protein phosphorylation sites in plants using musite. Front Plant Sci. 2012;3:186. http://dx.doi.org/10.3389/fpls.2012.00186
• 44. Yruela I, Contreras-Moreira B. Protein disorder in plants: a view from the chloroplast. BMC Plant Biol. 2012;12(1):165. http://dx.doi. org/10.1186/1471-2229-12-165
• 45. Peng K, Radivojac P, Vucetic S, Dunker AK, Obradovic Z. Lengthdependent prediction of protein intrinsic disorder. BMC Bioinformatics.2006;7(1):208. http://dx.doi.org/10.1186/1471-2105-7-208
• 46. Oates ME, Romero P, Ishida T, Ghalwash M, Mizianty MJ, Xue B, et al. D2P2: database of disordered protein predictions. Nucl Acids Res.2012;41:D508–516. http://dx.doi.org/10.1093/nar/gks1226
• 47. Ito Y, Hirochika H, Kurata N. Organ-specific alternative transcripts of KNOX family class 2 homeobox genes of rice. Gene.2002;288(1–2):41–47.
• 48. Qin Q, Wang W, Guo X, Yue J, Huang Y, Xu X, et al. Arabidopsis DELLA protein degradation is controlled by a type-one protein phosphatase,TOPP4. PLoS Genet. 2014;10(7):e1004464. http://dx.doi.org/10.1371/journal.pgen.1004464
• 49. Minezaki Y, Homma K, Nishikawa K. Genome-wide survey of transcription factors in prokaryotes reveals many bacteria-specificfamilies not found in archaea. DNA Res. 2005;12(5):269–280. http://dx.doi.org/10.1093/dnares/dsi016
• 50. Lynch M. The origins of eukaryotic gene structure. Mol Biol Evol. 006;23(2):450–468. http://dx.doi.org/10.1093/molbev/msj050
• 51. Azevedo RBR, Lohaus R, Braun V, Gumbel M, Umamaheshwar M, Agapow PM, et al. The simplicity of metazoan cell lineages. Nature. 2005;433(7022):152–156. http://dx.doi.org/10.1038/nature0317852. Peng ZL, Kurgan L. Comprehensive comparative assessment ofin-silico predictors of disordered regions. Curr Protein Pept Sci. 2012;13(1):6–18.

Identyfikatory

DOI

10.5586/asbp.2014.034