调控进化与形态多样性

doi:10.3724/SP.J.1003.2014.13247

摘要/Abstract

摘要：

揭示导致生物体形态和结构多样性产生的原因和机制, 是进化生物学研究的重要内容。进化发育生物学的研究表明, 许多复杂的形态结构及其多样性, 都是通过对古老调控网络的修饰或改造来完成的。也就是说, 生物体形态和结构的多样化并不是像以前认为的是由基因编码区的变化造成的, 而更多的是取决于基因的调控进化。作为控制基因表达的关键组分, 基因调控区的顺式调控元件通过与特定反式作用因子结合, 精细调控基因表达的时、空和量。因此, 调控元件的获得、丢失、修饰或者改变都能引起基因表达模式的变化, 是形态和结构多样性产生的主要原因。本文结合近年来国际上在基因的调控进化方面所取得的进展, 总结了真核生物中基因调控的方式和特点, 阐述了调控进化的基本式样, 揭示了调控进化在生物进化(特别是形态和结构多样化)中的作用。

关键词: 调控元件, 多效基因, 遗传开关, 平行演化, 进化发育生物学

Abstract

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

国春策, 张睿, 山红艳, 孔宏智 (2014) 调控进化与形态多样性. 生物多样性, 22, 72-79. DOI: 10.3724/SP.J.1003.2014.13247.

Chunce Guo,Rui Zhang,Hongyan Shan,Hongzhi Kong (2014) Effects of regulatory evolution on morphological diversity. Biodiversity Science, 22, 72-79. DOI: 10.3724/SP.J.1003.2014.13247.

导出引用管理器 EndNote|Ris|BibTeX

链接本文: https://www.biodiversity-science.net/CN/10.3724/SP.J.1003.2014.13247

https://www.biodiversity-science.net/CN/Y2014/V22/I1/72

图/表 1

参考文献 62

[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.

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	人 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

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	人 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