Parallel evolution of TCP and B-class genes in Commelinaceae flower bilateral symmetry

EvoDevo

Lena C Hileman¹  Jill C Preston¹ 

[1] Department of Ecology and Evolutionary Biology, University of Kansas,1200 Sunnyside Avenue, Lawrence, KS 66045, USA

关键词: teosinte branched1;    tepals;    monocots;    homeotic change;    CYCLOIDEA;    Commelinaceae;    B class genes;   

Others  :  810300
DOI  :  10.1186/2041-9139-3-6

 received in 2011-12-12, accepted in 2012-03-06,  发布年份 2012

【 摘 要 】

Background

Flower bilateral symmetry (zygomorphy) has evolved multiple times independently across angiosperms and is correlated with increased pollinator specialization and speciation rates. Functional and expression analyses in distantly related core eudicots and monocots implicate independent recruitment of class II TCP genes in the evolution of flower bilateral symmetry. Furthermore, available evidence suggests that monocot flower bilateral symmetry might also have evolved through changes in B-class homeotic MADS-box gene function.

Methods

In order to test the non-exclusive hypotheses that changes in TCP and B-class gene developmental function underlie flower symmetry evolution in the monocot family Commelinaceae, we compared expression patterns of teosinte branched1 (TB1)-like, DEFICIENS (DEF)-like, and GLOBOSA (GLO)-like genes in morphologically distinct bilaterally symmetrical flowers of Commelina communis and Commelina dianthifolia, and radially symmetrical flowers of Tradescantia pallida.

Results

Expression data demonstrate that TB1-like genes are asymmetrically expressed in tepals of bilaterally symmetrical Commelina, but not radially symmetrical Tradescantia, flowers. Furthermore, DEF-like genes are expressed in showy inner tepals, staminodes and stamens of all three species, but not in the distinct outer tepal-like ventral inner tepals of C. communis.

Conclusions

Together with other studies, these data suggest parallel recruitment of TB1-like genes in the independent evolution of flower bilateral symmetry at early stages of Commelina flower development, and the later stage homeotic transformation of C. communis inner tepals into outer tepals through the loss of DEF-like gene expression.

【 授权许可】

   
2012 Preston and Hileman; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Donoghue MJ, Ree RH, Baum DA: Phylogeny and the evolution of flower symmetry in the Asteridae. Trends Plant Sci 1998, 3:311-317.
• [2]Ree RH, Donoghue MJ: Inferring rates of change in flower symmetry in asterid angiosperms. Syst Biol 1999, 48:633-641.
• [3]Endress PK: Symmetry in flowers: diversity and evolution. Int J Plant Sci 1999, 160:S3-S23.
• [4]Sargent RD: Floral symmetry affects speciation rates in angiosperms. Proc R Soc Lond Biol Sci 2004, 271:603-608.
• [5]Knapp S: On 'various contrivances': pollination, phylogeny and flower form in the Solanaceae. Philos Transact R Soc Lond Biol Sci 2010, 365:449-460.
• [6]Vamosi JC, Vamosi SM: Key innovations within a geographical context in flowering plants: towards resolving Darwin's abominable mystery. Ecol Lett 2010, 13:1270-1279.
• [7]Cubas P: Floral zygomorphy, the recurring evolution of a successful trait. Bioessays 2004, 26:1175-1184.
• [8]Luo D, Carpenter R, Copsey L, Vincent C, Clark J, Coen E: Control of organ asymmetry in flowers of Antirrhinum. Cell 1999, 99:367-376.
• [9]Luo D, Carpenter R, Vincent C, Copsey L, Coen E: Origin of floral asymmetry in Antirrhinum. Nature 1996, 383:794-799.
• [10]Feng X, Zhao Z, Tian Z, Xu S, Luo Y, Cai Z, Wang Y, Yang J, Wang Z, Weng L, Chen J, Zheng L, Guo X, Luo J, Sato S, Tabata S, Ma W, Cao X, Hu X, Sun C, Luo D: Control of petal shape and floral zygomorphy in Lotus japonicus. Proc Natl Acad Sci USA 2006, 103:4970-4975.
• [11]Busch A, Zachgo S: Control of corolla monosymmetry in the Brassicaceae Iberis amara. Proc Natl Acad Sci USA 2007, 104:16714-16719.
• [12]Broholm SK, Tähtiharju S, Laitinen RAE, Albert VA, Teeri TH, Elomaa P: A TCP domain transcription factor controls flower type specification along the radial axis of the Gerbera (Asteraceae) inflorescence. Proc Natl Acad Sci USA 2008, 105:9117-9122.
• [13]Wang Z, Luo Y, Li X, Wang L, Xu S, Yang J, Weng L, Sato S, Tabata S, Ambrose M, Rameau C, Feng X, Hu X, Luo D: Genetic control of floral zygomorphy in pea (Pisum sativum L.). Proc Natl Acad Sci USA 2008, 105:10414-10419.
• [14]Cronk QC: Legume flowers bear fruit. Proc Natl Acad Sci USA 2006, 103:4801-4802.
• [15]Hileman LC, Cubas P: An expanded evolutionary role for flower symmetry genes. J Biol 2009, 8:90. BioMed Central Full Text
• [16]Preston JC, Hileman LC: Developmental genetics of floral symmetry evolution. Trends Plant Sci 2009, 14:147-154.
• [17]Yuan Z, Gao S, Xue DW, Luo D, Li LT, Ding SY, Yao X, Wilson ZA, Qian Q, Zhang DB: RETARDED PALEA1 controls palea development and floral zygomorphy in rice. Plant Physiol 2009, 149:235-244.
• [18]Bartlett ME, Specht CD: Changes in expression pattern of the TEOSINTE BRANCHED1-like genes in the Zingiberales provide a mechanism for evolutionary shifts in symmetry across the order. AmJ Bot 2011, 98:1-17.
• [19]Galego L, Almeida J: Role of DIVARICATA in the control of dorsoventral asymmetry in Antirrhinum flowers. Genes Dev 2002, 16:880-891.
• [20]Costa MMR, Fox S, Hanna AI, Baxter C, Coen E: Evolution of regulatory interactions controlling floral asymmetry. Development 2005, 132:5093-5101.
• [21]Almeida J, Rocheta M, Galego L: Genetic control of flower shape in Antirrhinum majus. Development 1997, 124:1387-1392.
• [22]Hileman LC, Baum DA: Why do paralogs persist? Molecular evolution of CYCLOIDEA and related floral symmetry genes in Antirrhineae (Veronicaceae). Mol Biol Evol 2003, 20:591-600.
• [23]Cubas P: An epigenetic mutation responsible for natural variation in floral symmetry. Nature 1999, 401:157-161.
• [24]Howarth DG, Donoghue MJ: Phylogenetic analysis of the "ECE" (CYC/TB1) clade reveals duplications predating the core eudicots. Proc Natl Acad Sci USA 2006, 103:9101-9106.
• [25]Tsai W-C, Kuoh C-S, Chuang M-H, Chen W-H, Chen H-H: Four DEF-like MADS box genes displayed distinct floral morphogenetic roles in Phalaenopsis orchid. Plant Cell Physiol 2004, 45:831-844.
• [26]Tsai W-C, Pan Z-J, Hsiao Y-Y, Yeng M-F, Wu T-F, Chen W-H, Chen H-H: Interactions of B-class complex proteins involved in tepal development in Phalaenopsis orchid. Plant Cell Physiol 2008, 49:814-824.
• [27]Mondragón-Palomino M, Theissen G: MADS about the evolution of orchid flowers. Trends Plant Sci 2008, 13:51-59.
• [28]Mondragón-Palomino M, Hiese L, Harter A, Koch MA, Theissen G: Positive selection and ancient duplications in the evolution of class B floral homeotic genes of orchids and grasses. BMC Evol Biol 2009, 9:81-106. BioMed Central Full Text
• [29]Bartlett ME, Specht CD: Evidence for the involvement of GLOBOSA-like gene duplications and expression divergence in the evolution of floral morphology in the Zingiberales. New Phytol 2010, 187:521-541.
• [30]Riechmann JL, Krizek BA, Meyerowitz EM: Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. Proc Natl Acad Sci USA 1996, 93:4793-4798.
• [31]McGonigle B, Bouhidel K, Irish VF: Nuclear localization of the Arabidopsis APETALA1 and PISTILLATA homeotic gene products depends on their simultaneous expression. Genes Dev 1996, 10:1812-1821.
• [32]Pelaz S, Ditta GS, Baumann E, Wisman E, Yanofsky MF: B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 2000, 405:200-203.
• [33]Honma T, Goto K: Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 2001, 409:525-529.
• [34]Theissen G, Saedler H: Plant biology. Floral quartets. Nature 2001, 409:469-471.
• [35]Melzer R, Verelst W, Theissen G: The class E floral homeotic protein SEPALLATA3 is sufficient to loop DNA in 'floral quartet'-like complexes in vitro. Nucleic Acids Res 2009, 37:144-157.
• [36]Smaczniak C, Immink RGH, Muino JM, Blanvillain R, Busscher M, Busscher-Lange J, Dinh QD, Liu S, Westphal AH, Boeren S, Parcy F, Xu L, Carles CC, Angenent GC, Kaufmann K: Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development. Proc Natl Acad Sci USA 2012, 109:1560-1565.
• [37]Sommer H, Beltran J, Huijser P, Pape H, Lonnig W, Saedler H, Schwarz-Sommer Z: Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus: The protein shows homology to transcription factors. EMBO J 1990, 9:605-613.
• [38]Jack T, Brockman LL, Meyerowitz EM: The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell 1992, 68:683-697.
• [39]Ambrose BA, Lerner DR, Ciceri P, Padilla CM, Yanofsky MF, Schmidt RJ: Molecular and genetic analyses of the Silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Mol Cell 2000, 5:569-579.
• [40]Whipple CJ, Ciceri P, Padilla CM, Ambrose BA, Bandong SL, Schmidt RJ: Conservation of B-class floral homeotic gene function between maize and Arabidopsis. Development 2004, 131:6083-6091.
• [41]Whipple CJ, Zanis MJ, Kellogg EA, Schmidt RJ: Conservation of B class gene expression in the second whorl of a basal grass and outgroups links the origin of lodicules and petals. Proc Natl Acad Sci USA 2006, 104:1081-1086.
• [42]Drea S, Hileman LC, de Martino G, Irish VF: Functional analyses of genetic pathways controlling petal specification in poppy. Development 2007, 134:4157-4166.
• [43]Hileman LC, Irish VF: More is better: the uses of developmental genetic data to reconstruct perianth evolution. Am J Bot 2009, 96:83-95.
• [44]Malcomber ST, Kellogg EA: SEPALLATA gene diversification: brave new whorls. Trends Plant Sci 2005, 10:427-435.
• [45]Litt A, Kramer EM: The ABC model and the diversification of floral organ identity. Semin Cell Dev Biol 2010, 21:129-137.
• [46]Davis JI, Petersen G, Seberg O, Stevenson DW, Hardy CR, Simmons MP, Michelangeli FA, Goldman DH, Campbell LM, Specht CD, Cohen JL: Are mitochondrial genes useful for the analysis of monocot relationships? Taxon 2006, 55:857-870.
• [47]Givinish TJ, Pires JC, Graham SW, McPherson MA, Prince LM, Patterson TB, Rai HS, Roalson EH, Evans TM, Hahn WJ, Millam KC, Meerow AW, Molvray M, Kores PJ, O'Brien HE, Hall JC, Kress WJ, Sytsma KJ: Phylogenetic relationships of monocots based on the highly informative plastid gene ndhF: evidence for widespread concerted convergence. Aliso 2006, 22:28-51.
• [48]Rudall PJ, Bateman RM: Evolution of zygomorphy in monocot flowers: iterative patterns and developmental constraints. New Phytol 2004, 162:25-44.
• [49]GPWG (Grass Phylogeny Working Group): Phylogeny and subfamilial classification of the grasses (Poaceae). Ann Mo Bot Gard 2001, 88:373-457.
• [50]Michelangeli F, Davis JI, Stevenson D: Phylogenetic relationships among Poaceae and related families as inferred from morphology, inversions in the plastid genome, and sequence data from the mitochondrial and plastid genomes. Am J Bot 2003, 90:93-106.
• [51]Givnish TJ, Evans TM, Pires JC, Sytsma KJ: Polyphyly and convergent morphological evolution in Commelinales and Commelinidae: evidence from rbcL sequence data. Mol Phylogenet Evol 1999, 12:360-385.
• [52]Evans TM, Sytsma KJ, Faden RB, Givnish TJ: Phylogenetic relationship in the Commelinaceae: II. A cladistics analysis of rbcL sequences and morphology. Syst Bot 2003, 28:270-292.
• [53]Ushimaru A, Dohzono I, Takami Y, Hyodo F: Flower orientation enhances pollen transfer in bilaterally symmetrical flowers. Oecologia 2009, 160:667-674.
• [54]Hardy CR, Sloat LL, Faden RB: Floral organogenesis and the developmental basis for pollinator deception in the Asiatic dayflower, Commelina communis (Commelinaceae). Am J Bot 2009, 96:1236-1244.
• [55]Burns JH, Faden RB, Steppan SJ: Phylogenetic studies in the Commelinaceae subfamily Commelinoideae inferred from nuclear ribosomal and chloroplast DNA sequences. Syst Bot 2011, 36:268-276.
• [56]Howarth DG, Donoghue MJ: Duplications in CYC-like genes from Dipsacales correlate with floral form. Int J Plant Sci 2005, 166:357-270.
• [57]Preston JC, Kost MA, Hileman LC: Conservation and diversification of the symmetry developmental program among close relatives of snapdragon with divergent floral morphologies. New Phytol 2009, 182:751-762.
• [58]Katoh T, Kuma M: MAAFT: a novel method for rapid multiple sequence alignment based on fast Fourier Transform. Nucleic Acids Res 2002, 30:3059-3066.
• [59]Katoh T: Recent developments in the MAAFT multiple sequence alignment program. Brief Bioinform 2008, 9:212.
• [60]Maddison DR, Maddison WP: MacClade 4: analysis of phylogeny and character evolution. Sinauer, Sunderland, MA; 2003. version 4.0.6
• [61]Mondragón-Palomino M, Trontin C: High time for a roll call: gene duplication and phylogenetic relationships of TCP-like genes in monocots. Ann Bot 2011, 107:1533-1544.
• [62]Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
• [63]Nylander JAA: MrModeltest v2. Program distributed by the author. In Evolutionary Biology Centre. Uppsala University; 2004.
• [64]Zwickl D: Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD thesis. University of Texas at Austin, Section of Integrative Biology, Texas, USA; 2006.
• [65]Ochiai T, Nakamura T, Mashiko Y, Fukuda T, Yokoyama J, Kanno A, Kameya T: The differentiation of sepal and petal morphologies in Commelinaceae. Gene 2004, 343:253-262.
• [66]Preston JC, Hileman LC: SQUAMOSA-PROMOTER BINDING PROTEIN 1 initiates flowering in Antirrhinum majus through activation of meristem identity genes. Plant J 2010, 62:704-712.
• [67]Rozen S, Skaletsky HJ: Primer3 on the WWW for general users and for biologist programmers. In Bioinformatics Methods and Protocols: Methods in Molecular Biology. Edited by Krawetz S, Misener S. New York, NY: Humana Press; 2000:365-386.
• [68]Jackson D: In situ hybridization in plants. In Molecular Plant Pathology: a Practical Approach. Edited by Bowles DJ, Gurr SJ, McPherson M. Oxford UK: Oxford University Press; 1991:163-174.
• [69]Preston JC, Kellogg EA: Conservation and divergence of APETALA1/FRUITFULL-like gene function in grasses: evidence from gene expression analyses. Plant J 2007, 52:69-81.
• [70]Endress PK: Evolution of flower symmetry. Curr Opin Plant Biol 2001, 4:86-91.
• [71]Hardy CR, Stevenson DW: Floral organogenesis in some species of Tradescantia and Callisia (Commelinaceae). Int J Plant Sci 2000, 161:551-562.
• [72]Weir I, Lu J, Cook H, Causier B, Schwarz-Sommer Z, Davies B: CUPULIFORMIS establishes lateral organ boundaries in Antirrhinum. Development 2004, 131:915-922.
• [73]Hsu H-F, Yang C-H: An orchid (Oncidium Gower Ramsey) AP3-like MADS gene regulates floral formation and initiation. Plant Cell Physiol 2002, 43:1198-1209.
• [74]Xu Y, Teo LL, Zhou J, Kumar PP, Yu H: Floral organ identity genes in the orchid Dendrobium crumenatum. Plant J 2006, 46:54-68.
• [75]Chang YY, Kao NH, Li JY, Hsu WH, Liang YL, Wu JW, Yang CH: Characterization of the possible roles for B class MADS box genes in regulation of perianth formation in orchid. Plant Physiol 2010, 152:837-853.
• [76]Preston JC: Evolutionary genetics of core eudicot inflorescence and flower development. Int J Plant Dev Biol 2010, 4:17-29.