title: The role of self-organization in developmental evolution.
abstract: In developmental and evolutionary biology, particular emphasis has been given to the relationship between transcription factors and the cognate cis-regulatory elements of their target genes. These constitute the gene regulatory networks that control expression and are assumed to causally determine the formation of structures and body plans. Comparative analysis has, however, established a broad sequence homology among species that nonetheless display quite different anatomies. Transgenic experiments have also confirmed that many developmentally important elements are, in fact, functionally interchangeable. Although dependent upon the appropriate degree of gene expression, the actual construction of specific structures appears not directly linked to the functions of gene products alone. Instead, the self-formation of complex patterns, due in large part to epigenetic and non-genetic determinants, remains a persisting theme in the study of ontogeny and regenerative medicine. Recent evidence indeed points to the existence of a self-organizing process, operating through a set of intrinsic rules and forces, which imposes coordination and a holistic order upon cells and tissue. This has been repeatedly demonstrated in experiments on regeneration as well as in the autonomous formation of structures in vitro. The process cannot be wholly attributed to the functional outcome of protein-protein interactions or to concentration gradients of diffusible chemicals. This phenomenon is examined here along with some of the methodological and theoretical approaches that are now used in understanding the causal basis for self-organization in development and its evolution.
authors.affiliation: Laboratory of Systems Biology and Bioinformatics, Manchester, UK, bozorgmehr@tiscali.co.uk.
authors.forename: Joseph E Hannon
authors.initials: JE
authors.lastname: Bozorgmehr
mesh_terms: D000818:Animals; D044127:Epigenesis, Genetic / Q000235:genetics*; D019143:Evolution, Molecular; D018507:Gene Expression Regulation, Developmental / Q000235:genetics*; D006801:Humans; D008957:Models, Genetic; D009024:Morphogenesis / Q000235:genetics*; D009154:Mutation / Q000235:genetics; D020543:Proteome / Q000235:genetics*; D015398:Signal Transduction / Q000235:genetics*
chemical_list: D020543:Proteome
references.citation: Nat Rev Mol Cell Biol. 2008 Mar;9(3):255-62
references.pmid: 18292780
references.citation: Nat Rev Mol Cell Biol. 2011 Jun;12(6):392-8
references.pmid: 21602907
references.citation: Bioessays. 2012 Jan;34(1):17-25
references.pmid: 22052700
references.citation: Development. 2012 Jan;139(2):313-23
references.pmid: 22159581
references.citation: Heredity (Edinb). 2006 Sep;97(3):139-47
references.pmid: 16850038
references.citation: Bioessays. 2012 Mar;34(3):205-17
references.pmid: 22237730
references.citation: Science. 2012 Feb 24;335(6071):943-7
references.pmid: 22363002
references.citation: Development. 2011 Oct;138(20):4387-98
references.pmid: 21937596
references.citation: Phys Biol. 2008 Apr 10;5(1):015008
references.pmid: 18403826
references.citation: Proc Natl Acad Sci U S A. 2000 Jul 18;97(15):8364-8
references.pmid: 10880562
references.citation: Evolution. 2007 May;61(5):995-1016
references.pmid: 17492956
references.citation: Cell. 2007 Jul 27;130(2):205-9
references.pmid: 17662932
references.citation: Dev Biol. 1996 Feb 1;173(2):357-72
references.pmid: 8605997
references.citation: Dev Cell. 2012 Dec 11;23(6):1219-29
references.pmid: 23237954
references.citation: IEEE Trans Med Imaging. 1988;7(4):321-7
references.pmid: 18230485
references.citation: Science. 2014 Feb 14;343(6172):791-795
references.pmid: 24407478
references.citation: J Theor Biol. 1980 Aug 21;85(4):757-70
references.pmid: 7442290
references.citation: Development. 2003 Nov;130(21):5133-42
references.pmid: 12944426
references.citation: Development. 2007 Jan;134(1):93-103
references.pmid: 17164415
references.citation: J Chem Phys. 2005 Aug 1;123(5):054901
references.pmid: 16108687
references.citation: Science. 2012 Dec 14;338(6113):1406
references.pmid: 23239707
references.citation: Commun Integr Biol. 2009 Nov;2(6):467-70
references.pmid: 20195452
references.citation: J Cell Biol. 1995 Mar;128(6):1111-9
references.pmid: 7896875
references.citation: Proc Natl Acad Sci U S A. 2005 Aug 16;102(33):11571-2
references.pmid: 16091458
references.citation: Biol Reprod. 2005 Mar;72(3):510-5
references.pmid: 15469998
references.citation: Bioessays. 2000 Aug;22(8):753-60
references.pmid: 10918306
references.citation: Cell. 2008 Jan 25;132(2):185-95
references.pmid: 18243095
references.citation: Nature. 2004 Apr 15;428(6984):717-23
references.pmid: 15085123
references.citation: Proc Natl Acad Sci U S A. 2013 Jun 25;110(26):10473-4
references.pmid: 23749870
references.citation: Exp Physiol. 2013 Aug;98(8):1235-43
references.pmid: 23585325
references.citation: HFSP J. 2008 Apr;2(2):72-8
references.pmid: 19404474
references.citation: Bioessays. 2005 Mar;27(3):235-8
references.pmid: 15714555
references.citation: Proc Natl Acad Sci U S A. 2011 Jun 21;108(25):10202-7
references.pmid: 21633009
references.citation: Nature. 2006 Nov 23;444(7118):499-502
references.pmid: 17086198
references.citation: Proc Natl Acad Sci U S A. 2006 Sep 12;103(37):13753-8
references.pmid: 16945911
references.citation: J Theor Biol. 1969 Oct;25(1):1-47
references.pmid: 4390734
references.citation: Trends Genet. 2010 Feb;26(2):66-74
references.pmid: 20083321
references.citation: Dev Biol. 2006 Mar 15;291(2):193-206
references.pmid: 16515781
references.citation: J Biol Dyn. 2012;6 Suppl 1:31-41
references.pmid: 22873673
references.citation: J Genet. 2012;91(1):1-8
references.pmid: 22546821
references.citation: Nature. 1999 Apr 29;398(6730):814-8
references.pmid: 10235264
references.citation: Dev Biol. 2012 Feb 15;362(2):282-94
references.pmid: 22185795
references.citation: J Orthop Res. 2005 Sep;23(5):1211-8
references.pmid: 15908162
references.citation: Microbiol Mol Biol Rev. 2005 Dec;69(4):544-64
references.pmid: 16339735
references.citation: Nature. 2011 Mar 10;471(7337):216-9
references.pmid: 21390129
references.citation: Bioessays. 1998 Feb;20(2):116-25
references.pmid: 9631657
references.citation: Dev Dyn. 2009 Aug;238(8):1974-83
references.pmid: 19618469
references.citation: Development. 1989;107 Suppl:3-12
references.pmid: 2699855
references.citation: Proc Natl Acad Sci U S A. 1998 Mar 3;95(5):2355-60
references.pmid: 9482889
references.citation: Nat Rev Mol Cell Biol. 2009 Feb;10(2):104-15
references.pmid: 19165213
references.citation: Genome Biol. 2011;12(1):101
references.pmid: 21241524
references.citation: Nature. 2011 Jun 29;474(7353):598-603
references.pmid: 21720363
references.citation: Science. 2012 Apr 13;336(6078):187-91
references.pmid: 22499940
references.citation: Evolution. 2011 Nov;65(11):3332-5
references.pmid: 22023597
references.citation: Proc Natl Acad Sci U S A. 2013 Dec 10;110(50):20284-9
references.pmid: 24277810
references.citation: Development. 2005 Feb;132(4):797-803
references.pmid: 15677727
references.citation: Acta Biotheor. 1987;36(2):61-120
references.pmid: 3122478
references.citation: J Theor Biol. 1976 May 21;58(2):455-76
references.pmid: 940335
references.citation: Dev Dyn. 2011 Aug;240(8):1889-904
references.pmid: 21761475
references.citation: Int J Dev Biol. 2002 Jan;46(1):65-73
references.pmid: 11902689
references.citation: PLoS Biol. 2010 Nov 09;8(11):e1000537
references.pmid: 21085690
references.citation: Nat Rev Mol Cell Biol. 2013 Jul;14(7):452-9
references.pmid: 23778971
references.citation: Dev Dyn. 1995 Feb;202(2):101-14
references.pmid: 7734729
references.citation: Cell Res. 2005 May;15(5):301-16
references.pmid: 15916718
references.citation: Am J Hum Genet. 2012 Mar 9;90(3):478-85
references.pmid: 22341974
references.citation: Cell Cycle. 2010 Oct 1;9(19):3880-3
references.pmid: 20890116
references.citation: Histol Histopathol. 2013 Feb;28(2):155-74
references.pmid: 23275300
references.citation: Biosystems. 2012 Sep;109(3):243-61
references.pmid: 22542702
references.citation: PLoS Genet. 2013;9(9):e1003763
references.pmid: 24039605
references.citation: Mech Dev. 2004 Jun;121(6):519-26
references.pmid: 15172683
references.citation: PLoS Genet. 2012 Sep;8(9):e1002932
references.pmid: 23028347
references.citation: Cell. 2005 Dec 16;123(6):1147-60
references.pmid: 16360041
references.citation: Evolution. 2008 Sep;62(9):2155-77
references.pmid: 18616572
references.citation: Curr Opin Cell Biol. 2010 Feb;22(1):14-20
references.pmid: 20074926
references.citation: Genome Res. 2008 Feb;18(2):201-5
references.pmid: 18245453
references.citation: Prog Retin Eye Res. 2010 Nov;29(6):543-55
references.pmid: 20638484
references.citation: J Theor Biol. 2011 Jan 21;269(1):359-65
references.pmid: 21044633
references.citation: Nature. 2012 Sep 6;489(7414):57-74
references.pmid: 22955616
references.citation: Science. 2012 Oct 12;338(6104):217-9
references.pmid: 23066074
references.citation: Cardiovasc Res. 2004 Jun 1;62(3):548-57
references.pmid: 15158147
references.citation: BMC Biol. 2010 Sep 24;8:127
references.pmid: 20868489
references.citation: Curr Opin Cell Biol. 1993 Jun;5(3):513-20
references.pmid: 8352970
references.citation: Science. 2012 Dec 14;338(6113):1476-80
references.pmid: 23239739
references.citation: Cold Spring Harb Perspect Biol. 2009 Sep;1(3):a001255
references.pmid: 20066104
references.citation: Alzheimers Dement. 2016 Jan;12(1):1
references.pmid: 26710324
references.citation: Dev Biol. 2001 Jan 15;229(2):287-306
references.pmid: 11203696
references.citation: Nature. 2004 Apr 15;428(6984):703-4
references.pmid: 15085113
references.citation: Development. 2006 Jun;133(12):2291-302
references.pmid: 16720874
references.citation: Science. 2010 Sep 24;329(5999):1616-20
references.pmid: 20929839
references.citation: PLoS Biol. 2009 Feb 24;7(2):e37
references.pmid: 19243218
references.citation: Cell. 2002 Sep 20;110(6):673-87
references.pmid: 12297042
references.citation: Science. 2002 Aug 16;297(5584):1183-6
references.pmid: 12183631
references.citation: Science. 2012 May 11;336(6082):721-4
references.pmid: 22499809
references.citation: Anat Rec. 1983 Nov;207(3):435-49
references.pmid: 6650874
references.citation: Syst Biol. 2001 Jun;50(3):367-90
references.pmid: 12116581
references.citation: Nature. 2011 Apr 7;472(7341):51-6
references.pmid: 21475194
references.citation: Proc Natl Acad Sci U S A. 2008 Dec 23;105(51):20063-6
references.pmid: 19104053
references.citation: Dev Dyn. 2012 May;241(5):863-78
references.pmid: 22411736
references.citation: Science. 2013 Oct 25;342(6157):1241006
references.pmid: 24159046
references.citation: Dev Biol. 2006 May 1;293(1):116-26
references.pmid: 16546158
references.citation: Biomatter. 2013 Jul-Sep;3(3):
references.pmid: 23719257
references.citation: Proc Natl Acad Sci U S A. 2011 Aug 2;108(31):12782-6
references.pmid: 21765002
references.citation: Tissue Eng. 2007 Apr;13(4):721-35
references.pmid: 17341161
references.citation: Nat Genet. 2003 Mar;33 Suppl:245-54
references.pmid: 12610534
references.citation: Int J Dev Biol. 1997 Dec;41(6):771-7; comment 778-9
references.pmid: 9449452
references.citation: Science. 2011 May 13;332(6031):811-6
references.pmid: 21566185
references.citation: Bull Math Biol. 2002 Jul;64(4):747-69
references.pmid: 12216419
references.citation: Neuron. 2014 Jan 22;81(2):321-32
references.pmid: 24373884
references.citation: Nature. 2001 Jan 25;409(6819):517-21
references.pmid: 11206548
references.citation: Development. 2010 Mar;137(6):845-57
references.pmid: 20179091
references.citation: Science. 1995 Mar 24;267(5205):1788-92
references.pmid: 7892602
references.citation: Nature. 2003 Jan 23;421(6921):444-8
references.pmid: 12540920
references.citation: Biophys Chem. 2004 Aug 1;110(3):231-8
references.pmid: 15228959
references.citation: Exp Cell Res. 2000 Nov 25;261(1):91-103
references.pmid: 11082279
references.citation: Int J Dev Biol. 2010;54(8-9):1241-50
references.pmid: 20563988
references.citation: Curr Biol. 2010 Sep 14;20(17):R754-63
references.pmid: 20833320
references.citation: Science. 1977 Jun 10;196(4295):1161-6
references.pmid: 860134
references.citation: Dev Dyn. 2011 May;240(5):1063-86
references.pmid: 21416555
references.citation: Nat Rev Genet. 2005 Sep;6(9):709-15
references.pmid: 16094311
references.citation: Cell Stem Cell. 2008 Nov 6;3(5):519-32
references.pmid: 18983967
references.citation: PLoS One. 2011;6(12):e28766
references.pmid: 22163331
references.citation: Nat Commun. 2011 Jul 12;2:384
references.pmid: 21750538
references.citation: Annu Rev Biomed Eng. 2012;14:295-323
references.pmid: 22809139
references.citation: Theor Biol Med Model. 2011 Jun 03;8:17
references.pmid: 21635789
references.citation: Evolution. 2001 Nov 11;55(11):2342-52
references.pmid: 11794792
references.citation: Proc Natl Acad Sci U S A. 2011 Nov 15;108(46):18726-31
references.pmid: 22065759
references.citation: Genome Biol. 2001;2(11):COMMENT2008
references.pmid: 11737938
references.citation: Bioessays. 1990 Sep;12(9):441-6
references.pmid: 1979486
references.citation: Development. 2003 May;130(10):2027-37
references.pmid: 12668618
references.citation: J Cell Sci. 2001 Feb;114(Pt 4):629-41
references.pmid: 11171368
references.citation: Nat Rev Genet. 2011 Feb;12(2):136-49
references.pmid: 21245830
references.citation: Prog Biophys Mol Biol. 1997;68(2-3):145-205
references.pmid: 9652171
references.citation: Science. 2005 Sep 23;309(5743):2033-7
references.pmid: 16179473
references.citation: Nat Genet. 2014 Jan;46(1):88-92
references.pmid: 24270359
references.citation: Differentiation. 1991 Mar;46(2):117-33
references.pmid: 1648522
references.citation: Philos Trans R Soc Lond B Biol Sci. 2011 Jul 27;366(1574):2069-75
references.pmid: 21690125
references.citation: Prog Biophys Mol Biol. 2013 May;112(1-2):33-43
references.pmid: 23562476
references.citation: Science. 2006 Feb 10;311(5762):796-800
references.pmid: 16469913
references.citation: Dev Cell. 2005 Jan;8(1):75-84
references.pmid: 15621531
references.citation: J Cell Biol. 2001 Oct 15;155(2):181-5
references.pmid: 11604416
references.citation: Nature. 2013 Apr 18;496(7445):311-6
references.pmid: 23598338
references.citation: Differentiation. 2003 Apr;71(3):171-205
references.pmid: 12694202
references.citation: Regen Med. 2011 Nov;6(6):667-73
references.pmid: 22050517
references.citation: FEMS Microbiol Rev. 2009 Jan;33(1):133-51
references.pmid: 19076632
references.citation: Science. 2013 Dec 13;342(6164):1375-9
references.pmid: 24337297
references.citation: Proc Natl Acad Sci U S A. 1989 Jul;86(13):4938-42
references.pmid: 2740333
references.citation: Curr Top Dev Biol. 2003;53:1-114
references.pmid: 12509125
references.citation: J Anat. 2008 Jun;212(6):707-19
references.pmid: 18510501
references.citation: PLoS Biol. 2014 Jan;12(1):e1001773
references.pmid: 24465181
references.citation: Mol Biol Evol. 2012 Mar;29(3):1047-57
references.pmid: 22075116
references.citation: Int J Biol Sci. 2005;1(1):19-23
references.pmid: 15951846
references.citation: Prog Biophys Mol Biol. 2012 May;109(1-2):16-32
references.pmid: 22564772
references.citation: Nature. 2011 Aug 28;477(7364):295-300
references.pmid: 21874018
references.citation: BMC Dev Biol. 2012 Jan 11;12:2
references.pmid: 22235805
references.citation: Proc Natl Acad Sci U S A. 2011 Feb 22;108(8):3264-9
references.pmid: 21300877
references.citation: Int J Dev Biol. 2012;56(6-8):447-62
references.pmid: 22451044
references.citation: J Med Life. 2011 Jan-Mar;4(1):82-90
references.pmid: 21505578
references.citation: Am J Physiol. 1991 Dec;261(6 Pt 1):L361-9
references.pmid: 1767856
references.citation: Cell. 2008 Jul 11;134(1):25-36
references.pmid: 18614008
references.citation: Cell Mol Life Sci. 2005 Feb;62(4):397-409
references.pmid: 15719167