Biodiversity Science ›› 2014, Vol. 22 ›› Issue (1): 72-79.doi: 10.3724/SP.J.1003.2014.13247

Special Issue: From Genome to Diversity

• Orginal Article • Previous Article     Next Article

Effects of regulatory evolution on morphological diversity

Chunce Guo*(), Rui Zhang, Hongyan Shan, Hongzhi Kong   

  1. State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093
  • Received:2013-11-29 Accepted:2014-01-15 Online:2014-02-10
  • Guo Chunce E-mail:chunceguo@ibcas.ac.cn

An important task in evolutionary biology is to understand the reason for and mechanisms of morphological diversification. Studies in evolutionary developmental biology have revealed that, rather than being invented repeatedly from scratch, many complex morphological structures have evolved by modification of ancient regulatory networks. In other words, morphological diversity is not always produced by changes in the protein-coding region of regulatory genes; rather, it largely depends on the evolution of gene regulation. As the main components of the regulatory regions of a gene, cis regulatory elements bind to specific trans factors and determine the precise expression of the gene in time, place and amount. As a result, gain, loss, change or modification of cis regulatory elements may lead to shifts in gene expression, which, in turn, generate morphological diversity. Here, by reviewing recent progress in this and related fields, we summarize the basic features of gene regulation in eukaryotes, elucidating its fundamental evolutionary pattern and revealing its importance in generating morphological diversity.

Key words: regulatory element, pleiotropic gene, genetic switches, parallel evolution, evo-devo

Table 1

Examples of morphological changes caused by cis-regulatory mutations"

基因
Gene
基因产物的功能
Function of product
表型
Phenotype
类群
Taxon
参考文献
References
dll (distal-less) 转录因子
Transcription factor
翅膀上眼点的有无
Eyespot determination
七叶树蝴蝶
Buckeye butterfly
Carroll et al., 1994
e (ebony) 色素合成
Pigment synthesis
腹部的颜色式样
Color pattern of abdomen
果蝇
Fruitfly
Wittkopp et al., 2002a
EDA (ectodysplasin) 分泌型信号蛋白
Secreted signaling protein
侧骨板的数目
Number of lateral plates
棘鱼
Stickleback
Colosimo et al., 2005; Jones et al., 2012
Duffy 细胞表面受体
Cell surface receptor
红细胞的形状
Shape of red blood cell

Human
Tournamille et al., 1995
Optix 转录因子
Transcription factor
翅膀着色式样
Pattern of wing coloration
釉蛱蝶属
Heliconius
Dasmahapatra et al., 2012
pitx1 (paired-like homeodomain transcription factor 1) 转录因子
Transcription factor
腹鳍的式样
Skeletal patterning
棘鱼
Stickleback
Peichel et al., 2001; Cresko et al., 2004; Shapiro et al., 2004
sc (scute) 转录因子
Transcription factor
成体背部刚毛的式样
Bristle pattern on adult notum
果蝇
Fruitfly
Marcellini & Simpson, 2006
MPF2 转录因子
Transcription factor
花器官的形状
Shape of floral organ
毛酸浆
Physalis pubescens
He & Saedler, 2005
svb (shavenbaby) 转录因子
Transcription factor
幼虫体表刚毛的式样
Bristle pattern on larvae
果蝇
Fruitfly
Sucena et al., 2003; Frankel et al., 2012
tb1 (teosinte branched 1) 转录因子
Transcription factor
分枝结构
Branching structure
玉米
Maize
Clark et al., 2006
ubx (ultrabithorax) 转录因子
Transcription factor
成体腿部刚毛的式样
Bristle pattern on adult legs
果蝇
Fruitfly
Stern, 1998
wnt1 (wingless) 分泌型信号蛋白
Secreted signaling protein
体节分化式样
Segmentation
果蝇
Fruitfly
Pfeiffer et al., 2000
y (yellow) 色素合成
Pigment synthesis
表皮的颜色式样
Color pattern of cuticle
果蝇
Fruitfly
Gompel et al., 2005; Jeong et al., 2006; Prud’homme et al., 2006
[1] Brakefield PM, Gates J, Keys D, Kesbeke F, Wijngaarden PJ, Monteiro A, French V, Carroll SB (1996) Development, plasticity and evolution of butterfly eyespot patterns.Nature, 384, 236-242.
[2] Brunetti CR, Selegue JE, Monteiro A, French V, Brakefield PM, Carroll SB (2001) The generation and diversification of butterfly eyespot color patterns.Current Biology, 11, 1578-1585.
[3] Carroll SB (2005a) Endless Forms Most Beautiful: The New Science of Evo Devo and the Making of the Animal Kingdom. WW Norton & Company, New York.
[4] Carroll SB (2005b) Evolution at two levels: on genes and form.PLoS Biology, 3, e245.
[5] Carroll SB (2007) The Making of the Fittest: DNA and the Ultimate Forensic Record of Evolution. WW Norton & Company, New York.
[6] Carroll SB (2009) Endless forms: the evolution of gene regulation and morphological diversity. In: Philosophy of Biology: An Anthology (eds Rosenberg A, Arp R), pp. 193-197. Wiley-Blackwell, Malden.
[7] Carroll SB (2011) How great wings can look alike.Science, 333, 1100-1101.
[8] Carroll SB, Gates J, Keys DN, Paddock SW, Panganiban G, Selegue JE, Williams JA (1994) Pattern formation and eyespot determination in butterfly wings.Science, 265, 109-114.
[9] Carroll SB, Prud’Homme B, Gompel N (2008) Regulating evolution.Scientific American, 298, 60-67.
[10] Chervitz SA, Aravind L, Sherlock G, Ball CA, Koonin EV, Dwight SS, Harris MA, Dolinski K, Mohr S, Smith T (1998) Comparison of the complete protein sets of worm and yeast: orthology and divergence.Science, 282, 2022-2028.
[11] Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, Markow TA, Kaufman TC, Kellis M, Gelbart W, Iyer VN (2007) Evolution of genes and genomes on the Drosophila phylogeny.Nature, 450, 203-218.
[12] Clark RM, Wagler TN, Quijada P, Doebley J (2006) A distant upstream enhancer at the maize domestication gene tb1 has pleiotropic effects on plant and inflorescent architecture.Nature Genetics, 38, 594-597.
[13] Colosimo PF, Hosemann KE, Balabhadra S, Villarreal G, Dickson M, Grimwood J, Schmutz J, Myers RM, Schluter D, Kingsley DM (2005) Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles.Science, 307, 1928-1933.
[14] Cotney J, Leng J, Yin J, Reilly SK, DeMare LE, Emera D, Ayoub AE, Rakic P, Noonan JP (2013) The evolution of lineage-specific regulatory activities in the human embryonic limb.Cell, 154, 185-196.
[15] Cresko WA, Amores A, Wilson C, Murphy J, Currey M, Phillips P, Bell MA, Kimmel CB, Postlethwait JH (2004) Parallel genetic basis for repeated evolution of armor loss in Alaskan threespine stickleback populations. Proceedings of the National Academy of Sciences,USA, 101, 6050-6055.
[16] Dasmahapatra KK, Walters JR, Briscoe AD, Davey JW, Whibley A, Nadeau NJ, Zimin AV, Hughes DST, Ferguson LC, Martin SH, Salazar C, Lewis JJ, Adler S, Ahn SJ, Baker DA, Baxter SW, Chamberlain NL, Chauhan R, Counterman BA, Dalmay T, Gilbert LE, Gordon K, Heckel DG, Hines HM, Hoff KJ, Holland PWH, Jacquin-Joly E, Jiggins FM, Jones RT, Kapan DD, Kersey P, Lamas G, Lawson D, Mapleson D, Maroja LS, Martin A, Moxon S, Palmer WJ, Papa R, Papanicolaou A, Pauchet Y, Ray DA, Rosser N, Salzberg SL, Supple MA, Surridge A, Tenger-Trolander A, Vogel H, Wilkinson PA, Wilson D, Yorke JA, Yuan FR, Balmuth AL, Eland C, Gharbi K, Thomson M, Gibbs RA, Han Y, Jayaseelan JC, Kovar C, Mathew T, Muzny DM, Ongeri F, Pu LL, Qu JX, Thornton RL, Worley KC, Wu YQ, Linares M, Blaxter ML, Ffrench-Constant RH, Joron M, Kronforst MR, Mullen SP, Reed RD, Scherer SE, Richards S, Mallet J, McMillan WO, Jiggins CD, Consor- tium HG (2012) Butterfly genome reveals promiscuous exchange of mimicry adaptations among species.Nature, 487, 94-98.
[17] DiLeone RJ, Marcus GA, Johnson MD, Kingsley DM (2000) Efficient studies of long-distance Bmp5 gene regulation using bacterial artificial chromosomes. Proceedings of the National Academy of Sciences,USA, 97, 1612-1617.
[18] Doebley J, Stec A (1991) Genetic analysis of the morpholo- gical differences between maize and teosinte.Genetics, 129, 285-295.
[19] Doebley J, Stec A, Gustus C (1995) teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance.Genetics, 141, 333-346.
[20] Frankel N, Wang S, Stern DL (2012) Conserved regulatory architecture underlies parallel genetic changes and conve- rgent phenotypic evolution. Proceedings of the National Academy of Sciences,USA, 109, 20975-20979.
[21] Gaj T, Gersbach CA, Barbas CF (2013) ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering.Trends in Biotechnology, 31, 397-405.
[22] Gehring W (1998) Master Control Genes in Development and Evolution: The Homeobox Story. Yale University Press, New Haven.
[23] Gehring W, Ikeo K (1999) Pax 6: mastering eye morpho- genesis and eye evolution.Trends in Genetics, 15, 371-377.
[24] Gharib WH, Robinson-Rechavi M (2011) When orthologs diverge between human and mouse.Briefings in Bioinformatics, 12, 436-441.
[25] Gompel N, Prud’homme B, Wittkopp PJ, Kassner VA, Carroll SB (2005) Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila.Nature, 433, 481-487.
[26] Graham A, Papalopulu N, Krumlauf R (1989) The murine and Drosophila homeobox gene complexes have common features of organization and expression.Cell, 57, 367-378.
[27] He C, Saedler H (2005) Heterotopic expression of MPF2 is the key to the evolution of the Chinese lantern of Physalis, a morphological novelty in Solanaceae. Proceedings of the National Academy of Sciences,USA, 102, 5779-5784.
[28] Hendry AP, Peichel CL, Matthews B, Boughman JW, Nosil P (2013) Stickleback research: the now and the next.Evolutionary Ecology Research, 15, 1-31.
[29] Hoekstra HE, Coyne JA (2007) The locus of evolution: evo devo and the genetics of adaptation.Evolution, 61, 995-1016.
[30] Jeong S, Rokas A, Carroll SB (2006) Regulation of body pigmentation by the abdominal-B Hox protein and its gain and loss in Drosophila evolution.Cell, 125, 1387-1399.
[31] Jones FC, Grabherr MG, Chan YF, Russell P, Mauceli E, Johnson J, Swofford R, Pirun M, Zody MC, White S, Birney E, Searle S, Schmutz J, Grimwood J, Dickson MC, Myers RM, Miller CT, Summers BR, Knecht AK, Brady SD, Zhang HL, Pollen AA, Howes T, Amemiya C, Lander ES, Di Palma F, Lindblad-Toh K, Kingsley DM, Platf BIGS, Team WGA (2012) The genomic basis of adaptive evolution in threespine sticklebacks.Nature, 484, 55-61.
[32] King M-C, Wilson AC (1975) Evolution at two levels in humans and chimpanzees.Science, 188, 107-116.
[33] Kitano J, Bolnick DI, Beauchamp DA, Mazur MM, Mori S, Nakano T, Peichel CL (2008) Reverse evolution of armor plates in the threespine stickleback.Current Biology, 18, 769-774.
[34] Kozmik Z, Daube M, Frei E, Norman B, Kos L, Dishaw LJ, Noll M, Piatigorsky J (2003) Role of Pax genes in eye evolution: a cnidarian PaxB gene uniting Pax2 and Pax6 functions.Developmental Cell, 5, 773-785.
[35] Lawrence PA (1992) The Making of A Fly: The Genetics of Animal Design. Blackwell Scientific Publications, Oxford.
[36] Levine M, Tjian R (2003) Transcription regulation and animal diversity.Nature, 424, 147-151.
[37] Marcellini S, Simpson P (2006) Two or four bristles: functional evolution of an enhancer of scute in Drosophilidae.PLoS Biology, 4, e386.
[38] Mayr E (2001) What Evolution Is? Basic Books, New York.
[39] McGinnis W, Garber RL, Wirz J, Kuroiwa A, Gehring WJ (1984) A homologous protein-coding sequence in Drosophila homeotic genes and its conservation in other metazoans.Cell, 37, 403-408.
[40] McKinnon JS, Mori S, Blackman BK, David L, Kingsley DM, Jamieson L, Chou J, Schluter D (2004) Evidence for ecology’s role in speciation.Nature, 429, 294-298.
[41] McKinnon JS, Rundle HD (2002) Speciation in nature: the threespine stickleback model systems.Trends in Ecology and Evolution, 17, 480-488.
[42] Mikkelsen TS, Hillier LW, Eichler EE, Zody MC, Jaffe DB, Yang S-P, Enard W, Hellmann I, Lindblad-Toh K, Altheide TK (2005) Initial sequence of the chimpanzee genome and comparison with the human genome.Nature, 437, 69-87.
[43] Monteiro A, Podlaha O (2009) Wings, horns, and butterfly eyespots: How do complex traits evolve?PLoS Biology, 7, e1000037.
[44] Nijhout HF (1991) The Development and Evolution of Butterfly Wing Patterns. Smithsonian Institution Press, Washington, DC.
[45] Panganiban G, Nagy L, Carroll SB (1994) The role of the Distal-less gene in the development and evolution of insect limbs.Current Biology, 4, 671-675.
[46] Pearson JC, Lemons D, McGinnis W (2005) Modulating Hox gene functions during animal body patterning.Nature Reviews Genetics, 6, 893-904.
[47] Peichel CL, Nereng KS, Ohgi KA, Cole BLE, Colosimo PF, Buerkle CA, Schluter D, Kingsley DM (2001) The genetic architecture of divergence between threespine stickleback species.Nature, 414, 901-905.
[48] Pfeiffer S, Alexandre C, Calleja M, Vincent J-P (2000) The progeny of wingless-expressing cells deliver the signal at a distance in Drosophila embryos.Current Biology, 10, 321-324.
[49] Preston JC, Hileman LC (2009) Developmental genetics of floral symmetry evolution.Trends in Plant Science, 14, 147-154.
[50] Prud’homme B, Gompel N, Carroll SB (2007) Emerging principles of regulatory evolution. Proceedings of the National Academy of Sciences,USA, 104, 8605-8612.
[51] Prud’homme B, Gompel N, Rokas A, Kassner VA, Williams TM, Yeh SD, True JR, Carroll SB (2006) Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene.Nature, 440, 1050-1053.
[52] Shapiro MD, Bell MA, Kingsley DM (2006) Parallel genetic origins of pelvic reduction in vertebrates. Proceedings of the National Academy of Sciences,USA, 103, 13753-13758.
[53] Shapiro MD, Marks ME, Peichel CL, Blackman BK, Nereng KS, Jonsson B, Schluter D, Kingsley DM (2004) Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks.Nature, 428, 717-723.
[54] Shubin N, Tabin C, Carroll S (2009) Deep homology and the origins of evolutionary novelty.Nature, 457, 818-823.
[55] Soltis DE, Ma H, Frohlich MW, Soltis PS, Albert VA, Oppenh- eimer DG, Altman NS, dePamphilis C, Leebens-Mack J (2007) The floral genome: an evolutionary history of gene duplication and shifting patterns of gene expression.Trends in Plant Science, 12, 358-367.
[56] Stern DL (1998) A role of Ultrabithorax in morphological differences between Drosophila species.Nature, 396, 463-466.
[57] Sucena E, Delon I, Jones I, Payre F, Stern DL (2003) Regulatory evolution of shavenbaby/ovo underlies multiple cases of morphological parallelism.Nature, 424, 935-938.
[58] Tournamille C, Colin Y, Cartron JP, Le Van Kim C (1995) Disruption of a GATA motif in the Duffy gene promoter abolishes erythroid gene expression in Duffy-negative individuals.Nature Genetics, 10, 224-228.
[59] Wittkopp PJ, True JR, Carroll SB (2002a) Reciprocal functions of the Drosophila Yellow and Ebony proteins in the development and evolution of pigment patterns.Development, 129, 1849-1858.
[60] Wittkopp PJ, Vaccaro K, Carroll SB (2002b) Evolution of yellow gene regulation and pigmentation in Drosophila.Current Biology, 12, 1547-1556.
[61] Wray GA (2007) The evolutionary significance of cis- regulatory mutations.Nature Reviews Genetics, 8, 206-216.
[62] Yang X, Pang H, Liu B, Qiu Z, Gao Q, Wei L, Dong Y, Wang Y (2012) Evolution of double positive autoregulatory feedback loops in CYCLOIDEA2 clade genes is associated with the origin of floral zygomorphy.Plant Cell, 24, 1834-1847.
[1] Xueping Wei,Xianchun Zhang. (2016) Distributional patterns of the monolete and trilete ferns in China . Biodiv Sci, 24(10): 1129-1134.
[2] Haomin Lyu,Renchao Zhou,Suhua Shi. (2015) Recent advances in the study of ecological speciation . Biodiv Sci, 23(3): 398-407.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed