Adaptation in flower form: A comparative evodevo approach

New Phytologist

Volumn 206, Issue 1, 2015, Pages 74-90

  Specht, Chelsea D ^a   Howarth, Dianella G ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b ST JOHN'S UNIVERSITY   (United States)

Author keywords

Boundary formation; Evodevo; Floral organ development; Flower morphology; Organ fusion; Plant development; Symmetry; TCP genes

Indexed keywords

ADAPTATION; COMPARATIVE STUDY; DEVELOPMENTAL BIOLOGY; EVOLUTIONARY BIOLOGY; FLOWER; GENE FLOW; GENETIC VARIATION; GENOTYPE; PHENOTYPE;

ADAPTATION; ANATOMY AND HISTOLOGY; DEVELOPMENTAL BIOLOGY; EVOLUTION; FLOWER; GENE REGULATORY NETWORK; GENETIC SELECTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; PHENOTYPE; PHYSIOLOGY;

ADAPTATION, PHYSIOLOGICAL; BIOLOGICAL EVOLUTION; DEVELOPMENTAL BIOLOGY; FLOWERS; GENE REGULATORY NETWORKS; PHENOTYPE; SELECTION, GENETIC;

EID: 84923511055     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13198     Document Type: Review

References (124)

1. Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M. 1997. Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell 9: 841-857.
2. Almeida J, Rocheta M, Galego L, Anonymous. 1997. Genetic control of flower shape in Antirrhinum majus. Development 124: 1387-1392.
3. Armbruster WS, Debevec EM, Willson MF. 2002. Evolution of syncarpy in angiosperms: theoretical and phylogenetic analyses of the effects of carpel fusion on offspring quantity and quality. Journal of Evolutionary Biology 15: 657-672.
4. Baker CC, Sieber P, Wellmer F, Meyerowitz EM. 2005. The early extra petals1 mutant uncovers a role for microRNA miR164c in regulating petal number in Arabidopsis. Current Biology 15: 303-315.
5. Barrier M, Robichaux RH, Purugganan MD. 2001. Accelerated regulatory gene evolution in an adaptive radiation. Proceedings of the National Academy of Sciences, USA 98: 10208-10213.
6. Barrio RÁ, Hernández-Machado A, Varea C, Romero-Arias JR, Alvarez-Buylla E. 2010. Flower development as an interplay between dynamical physical fields and genetic networks. PLoS ONE 5: e13523.
7. Bartlett M, Specht CD. 2011. Changes in expression pattern of the teosinte branched-1 like genes in the Zingiberales provide a mechanism for evolutionary shifts in symmetry across the order. American Journal of Botany 98: 227-243.
8. Baumann K, Perez-Rodriguez M, Bradley D, Venail J, Bailey P, Jin H, Koes R, Roberts K, Martin C. 2007. Control of cell and petal morphogenesis by R2R3 MYB transcription factors. Development 134: 1691-1701.
9. Blanc G, Wolfe KH. 2004. Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. The Plant Cell 16: 1679-1691.
10. Boyden GS, Donoghue MJ, Howarth DG. 2012. Duplications and expression of RADIALIS-like genes in Dipsacales. International Journal of Plant Sciences 173: 971-983.
11. Brockington SF, Alvarez-Fernandez R, Landis JB, Alcorn K, Walker RH, Thomas MM, Hileman LC, Glover BJ. 2013. Evolutionary analysis of the MIXTA gene family highlights potential targets for the study of cellular differentiation. Molecular Biology and Evolution 30: 526-540.
12. Broholm SK, Tähtiharju S, Laitinen RAE, Albert VA, Teeri TH, Elomaa P. 2008. A TCP domain transcription factor controls flower type specification along the radial axis of the Gerbera (Asteraceae) inflorescence. Proceedings of the National Academy of Sciences, USA 105: 9117-9122.
13. de Bruijn S, Angenent GC, Kaufmann K. 2012. Plant "evo-devo" goes genomic: from candidate genes to regulatory networks. Trends in Plant Science 17: 441-447.
14. Byrne ME. 2012. Making leaves. Current Opinion in Plant Biology 15: 24-30.
15. Carlson SE, Howarth DG, Donoghue MJ. 2011. Diversification of CYCLOIDEA-like genes in Dipsacaceae (Dipsacales): implications for the evolution of capitulum inflorescences. BMC Evolutionary Biology 11: 325.
16. Carretero-Paulet L, Fares MA. 2012. Evolutionary dynamics and functional specialization of plant paralogs formed by whole and small-scale genome duplications. Molecular Biology and Evolution 29: 3541-3551.
17. Carroll SB. 2006. Endless forms most beautiful: the new science of evo devo and the making of the animal kingdom. New York, NY, USA: W. W. Norton.
18. Carroll SB. 2008. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134: 25-36.
19. Chapman MA, Leebens-Mack JH, Burke JM. 2008. Positive selection and expression divergence following gene duplication in the sunflower CYCLOIDEA gene family. Molecular Biology and Evolution 25: 1260-1273.
20. Cho E, Zambryski PC. 2011. ORGAN BOUNDARY1 defines a gene expressed at the junction between the shoot apical meristem and lateral organs. Proceedings of the National Academy of Sciences, USA 108: 2154-2159.
21. Citerne HL, Jabbour F, Nadot S, Damerval C. 2010. The evolution of floral symmetry. Advances in Botanical Research 54: 85-137.
22. Citerne HL, Luo D, Pennington RT, Coen E, Cronk QCB. 2003. A phylogenomic investigation of CYCLOIDEA-like TCP genes in the Leguminosae. Plant Physiology 131: 1042-1053.
23. Colautti RI, Lee C-R, Mitchell-Olds T. 2012. Origin, fate, and architecture of ecologically relevant genetic variation. Current Opinion in Plant Biology 15: 199-204.
24. Corley SB, Carpenter R, Copsey L, Coen E. 2005. Floral asymmetry involves an interplay between TO and MYB transcription factors in Antirrhinum. Proceedings of the National Academy of Sciences, USA 102: 5068-5073.
25. Cubas P, Coen E, Zapater JM, Anonymous. 2001. Ancient asymmetries in the evolution of flowers. Current Biology 11: 1050-1052.
26. Donoghue MJ, Ree RH, Baum DA, Anonymous. 1998. Phylogeny and the evolution of flower symmetry in the Asteridae. Trends in Plant Science 3: 311-317.
27. Endress P, Matthews M. 2006. Elaborate petals and staminodes in eudicots: diversity, function, and evolution. Organisms Diversity & Evolution 6: 257-293.
28. Endress PK. 1982. Syncarpy and alternative modes of escaping disadvantages of apocarpy in primitive angiosperms. Taxon 31: 48-52.
29. Endress PK. 2001a. Origins of flower morphology. Journal of Experimental Zoology 291: 105-115.
30. Endress PK. 2001b. Origins of flower morphology. In: Wagner GP, ed. The character concept in evolutionary biology. San Diego, CA, USA: Academic Press, 493-510.
31. Endress PK. 2008. Perianth biology in the basal grade of extant angiosperms. International Journal of Plant Sciences 169: 844-862.
32. Endress PK. 2011. Evolutionary diversification of the flowers in angiosperms. American Journal of Botany 98: 370-396.
33. Endress PK, Doyle JA. 2009. Reconstructing the ancestral angiosperm flower and its initial specializations. American Journal of Botany 96: 22-66.
34. Eyre-Walker A. 2006. The genomic rate of adaptive evolution. Trends in Ecology & Evolution 21: 569-575.
35. Feng X, Zhao Z, Tian Z, Xu S, Luo Y, Cai Z, Wang Y, Yang J, Wang Z, Weng L et al. 2006. Control of petal shape and floral zygomorphy in Lotus japonicus. Proceedings of the National Academy of Sciences, USA 103: 4970-4975.
36. Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thompson JD. 2004. Pollination syndromes and floral specialization. Annual Review of Ecology, Evolution and Systematics 35: 375-403.
37. Filkov V. 2006. Identifying gene regulatory networks from gene expression data. In: Aluru S, ed. Handbook of Computational Molecular Biology. Boca Raton, FL, USA: Chapman & Hall/CRC Computer and Information Science Series.
38. Galego L, Almeida J. 2002. Role of DIVARICATA in the control of dorsoventral asymmetry in Antirrhinum flowers. Genes and Development 16: 880-891.
39. Garfield DA, Runcie DE, Babbitt CC, Haygood R, Nielsen WJ, Wray GA. 2013. The impact of gene expression variation on the robustness and evolvability of a developmental gene regulatory network. PLoS Biology 11: e1001696.
40. Ha CM, Jun JH, Fletcher JC. 2010. Control of Arabidopsis leaf morphogenesis through regulation of the YABBY and KNOX families of transcription factors. Genetics 186: 197-206.
41. Harrison CJ, Corley SB, Moylan EC, Alexander DL, Scotland RW, Langdale JA. 2005. Independent recruitment of a conserved developmental mechanism during leaf evolution. Nature 434: 509-514.
42. Hileman LC. 2014a. Trends in flower symmetry evolution revealed through phylogenetic and developmental genetic advances. Philosophical Transactions of the Royal Society B: Biological Sciences 369: 20130348.
43. Hileman LC. 2014b. Bilateral flower symmetry - how, when and why? Current Opinion in Plant Biology 17: 146-152.
44. Hileman LC, Baum DA. 2003. Why do paralogs persist? Molecular evolution of CYCLOIDEA and related floral symmetry genes in Antirrhineae (Veroniacaceae). Molecular Biology and Evolution 20: 591-600.
45. Hoekstra HE, Coyne JA. 2007. The locus of evolution: evo devo and the genetics of adaptation. Evolution 61: 995-1016.
46. Howarth DG, Donoghue MJ. 2005. Duplications in CYC-like genes from Dipsacales correlate with floral form. International Journal of Plant Sciences 166: 357-370.
47. Howarth DG, Donoghue MJ. 2006. Phylogenetic analysis of the "ECE" (CYC/TB1) clade reveals duplications predating the core eudicots. Proceedings of the National Academy of Sciences, USA 103: 9101-9106.
48. Howarth DG, Donoghue MJ. 2009. Duplications and expression of DIVARICATA-like genes in dipsacales. Molecular Biology and Evolution 26: 1245-1258.
49. Howarth DG, Martins T, Chimney E, Donoghue MJ. 2011. Diversification of CYCLOIDEA expression in the evolution of bilateral flower symmetry in Caprifoliaceae and Lonicera (Dipsacales). Annals of Botany 107: 1521-1532.
50. Huang T, López-Giráldez F, Townsend JP, Irish VF. 2012. RBE controls microRNA164 expression to effect floral organogenesis. Development 139: 2161-2169.
51. Igersheim A, Buzgo M, Endress PK. 2001. Gynoecium diversity and systematics in basal monocots. Botanical Journal of the Linnean Society 136: 1-65.
52. Jaillon O, Aury J-M, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C et al. 2007. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449: 463-467.
53. Jiang W, Liu Y, Xia E, Gao L. 2013. Prevalent role of gene features in determining evolutionary fates of whole-genome duplication duplicated genes in flowering plants. Plant Physiology 161: 1844-1861.
54. Jiao Y, Paterson AH. 2014. Polyploidy-associated genome modifications during land plant evolution. Philosophical Transactions of the Royal Society B: Biological Sciences 369: 20130355.
55. Jiao Y, Wickett N, Ayyampalayam S, Chanderbali A, Landherr L, Ralph PE, Soltis PS, Soltis DE, Clifton SE, Ma H et al. 2011. Phylogenomic analysis reveals ancient genome duplications in seed plant and angiosperm history. Nature 473: 97-100.
56. Kaufmann K, Pajoro A, Angenent GC. 2010. Regulation of transcription in plants: mechanisms controlling developmental switches. Nature Reviews. Genetics 11: 830-842.
57. Kersting AR, Bornberg-Bauer E, Moore AD, Grath S. 2012. Dynamics and adaptive benefits of protein domain emergence and arrangements during plant genome evolution. Genome Biology and Evolution 4: 316-329.
58. Koyama T, Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M. 2010. TCP transcription factors regulate the activities of ASYMMETRIC LEAVES1 and miR164, as well as the auxin response, during differentiation of leaves in Arabidopsis. The Plant Cell 22: 3574-3588.
59. Kramer EM, Holappa L, Gould B, Jaramillo MA, Setnikov D, Santiago PM. 2007. Elaboration of B gene function to include the identity of novel floral organs in the lower eudicot Aquilegia. Plant Cell 19: 750-766.
60. Kramer EM, Jaramillo MA, Di Stilio VS. 2004. Patterns of gene duplication and functional evolution during the diversification of the AGAMOUS subfamily of MADS box genes in angiosperms. Genetics 166: 1011-1023.
61. Krizek BA, Lewis MW, Fletcher JC. 2006. RABBIT EARS is a second-whorl repressor of AGAMOUS that maintains spatial boundaries in Arabidopsis flowers. Plant Journal 45: 369-383.
62. Lampugnani ER, Kilinc A, Smyth DR. 2012. PETAL LOSS is a boundary gene that inhibits growth between developing sepals in Arabidopsis thaliana. Plant Journal: For Cell and Molecular Biology 71: 724-735.
63. Lang D, Weiche B, Timmerhaus G, Richardt S, Riaño-Pachón DM, Corrêa LGG, Reski R, Mueller-Roeber B, Rensing SA. 2010. Genome-wide phylogenetic comparative analysis of plant transcriptional regulation: a timeline of loss, gain, expansion, and correlation with complexity. Genome Biology and Evolution 2: 488-503.
64. Lee D-K, Geisler M, Springer PS. 2009. LATERAL ORGAN FUSION1 and LATERAL ORGAN FUSION2 function in lateral organ separation and axillary meristem formation in Arabidopsis. Development 136: 2423-2432.
65. Luo D, Carpenter R, Copsey L, Vincent C, Clark J, Coen E. 1999. Control of organ asymmetry in flowers of Antirrhinum. Cell 99: 367-376.
66. Luo D, Carpenter R, Vincent C, Copsey L, Coen E. 1996. Origin of floral asymmetry in Antirrhinum. Nature 383: 794-799.
67. Mackay TFC, Stone EA, Ayroles JF. 2009. The genetics of quantitative traits: challenges and prospects. Nature Reviews. Genetics 10: 565-577.
68. Malcomber ST, Kellogg EA. 2004. Heterogeneous expression patterns and separate roles of the SEPALLATA gene LEAFY HULL STERILE1 in Grasses. Plant Cell 16: 1692-1706.
69. Maleszka R, Mason PH, Barron AB. 2013. Epigenomics and the concept of degeneracy in biological systems. Briefings in Functional Genomics 13: 191-202.
70. Mallory AC, Dugas DV, Bartel DP, Bartel B. 2004. MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs. Current Biology 14: 1035-1046.
71. Martin C, Glover BJ. 2007. Functional aspects of cell patterning in aerial epidermis. Current Opinion in Plant Biology 10: 20-70.
72. Ming R, Hou S, Feng Y, Yu Q, Dionne-Laporte A, Saw JH, Senin P, Wang W, Ly BV, Lewis KL et al. 2008. The draft genome of the transgenic tropical fruit tree papaya (Carica papaya L.). Nature 452: 991-996.
73. Mondragón-Palomino M, Theissen G. 2011. Conserved differential expression of paralogous DEFICIENS- and GLOBOSA-like MADS-box genes in the flowers of Orchidaceae: refining the "orchid code". Plant Journal 66: 1008-1019.
74. Moon J, Hake S. 2011. How a leaf gets its shape. Current Opinion in Plant Biology 14: 24-30.
75. Moyroud E, Kusters E, Monniaux M, Koes R, Parcy F. 2010. LEAFY blossoms. Trends in Plant Science 15: 346-352.
76. Moyroud E, Minguet EG, Ott F, Yant L, Posé D, Monniaux M, Blanchet S, Bastien O, Thévenon E, Weigel D et al. 2011. Prediction of regulatory interactions from genome sequences using a biophysical model for the Arabidopsis LEAFY transcription factor. The Plant Cell 23: 1293-1306.
77. Nadeau NJ, Jiggins CD. 2010. A golden age for evolutionary genetics? Genomic studies of adaptation in natural populations. Trends in Genetics 26: 484-492.
78. O'Maoileidigh DS, Graciet E, Wellmer F. 2014. Tansley review: gene networks controlling Arabidopsis thaliana flower development. New Phytologist 201: 16-30.
79. Palatnik JF, Wollmann H, Schommer C, Schwab R, Boisbouvier J, Rodriguez R, Warthmann N, Allen E, Dezulian T, Huson D et al. 2007. Sequence and expression differences underlie functional specialization of Arabidopsis MicroRNAs miR159 and miR319. Developmental Cell 13: 115-125.
80. Perez-Rodriguez M, Jaffe FW, Butelli E, Glover BJ, Martin C. 2005. Development of three different cell types is associated with the activity of a specific MYB transcription factor in the ventral petal of Antirrhinum majus flowers. Development 132: 359-370.
81. Pires ND, Dolan L. 2012. Morphological evolution in land plants: new designs with old genes. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 367: 508-518.
82. Posé D, Yant L, Schmid M. 2012. The end of innocence: flowering networks explode in complexity. Current Opinion in Plant Biology 15: 45-50.
83. Preston JC, Hileman LC. 2009. Developmental genetics of floral symmetry evolution. Trends in Plant Science 14: 147-154.
84. Prud'homme B, Gompel N, Carroll SB. 2007. Emerging principles of regulatory evolution. Proceedings of the National Academy of Sciences, USA 104(Suppl): 8605-8612.
85. Raimundo J, Sobral R, Bailey P, Azevedo H, Galego L, Almeida J, Coen E, Costa MMR. 2013. A subcellular tug of war involving three MYB-like proteins underlies a molecular antagonism in Antirrhinum flower asymmetry. Plant Journal 75: 527-538.
86. Ramsey J, Schemske DW. 1998. Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annual Review of Ecology and Systematics 29: 467-501.
87. Rast MI, Simon R. 2008. The meristem-to-organ boundary: more than an extremity of anything. Current Opinion in Genetics & Development 18: 287-294.
88. Rast MI, Simon R. 2012. Arabidopsis JAGGED LATERAL ORGANS acts with ASYMMETRIC LEAVES2 to coordinate KNOX and PIN expression in shoot and root meristems. Plant Cell 24: 2917-2933.
89. Remington DL, Purugganan MD. 2003. Candidate genes, quantitiative trait loci, and functional trait evolution in plants. International Journal of Plant Sciences 164: S7-S20.
90. Ren M, Tang J. 2010. Anther fusion enhances pollen removal in Campsis grandiflora, a hermaphroditic flower with didynamous stamens. International Journal of Plant Sciences 171: 275-282.
91. Ren M-X. 2008. Stamen fusion in plants: diversity, adaptive significance, and taxonomic implications. Journal of Systematics and Evolution 46: 452-466.
92. Rensing SA. 2014. Gene duplication as a driver of plant morphogenetic evolution. Current Opinion in Plant Biology 17: 43-48.
93. Rosin FM, Kramer EM. 2009. Old dogs, new tricks: regulatory evolution in conserved genetic modules leads to novel morphologies in plants. Developmental Biology 332: 25-35.
94. Sakai H, Medrano LJ, Meyerowitz EM. 1995. Role of SUPERMAN in maintaining Arabidopsis floral whorl boundaries. Nature 378: 199-203.
95. Schmidt D, Wilson MD, Ballester B, Schwalie PC, Brown GD, Marshall A, Kutter C, Watt S, Martinez-Jimenez CP, Mackay S et al. 2010. Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding. Science 328: 1036-1040.
96. Sharma B, Yant L, Hodges Sa, Kramer EM. 2014. Understanding the development and evolution of novel floral form in Aquilegia. Current Opinion in Plant Biology 17C: 22-27.
97. Sieber P, Wellmer F, Gheyselinck J, Riechmann JL, Meyerowitz EM. 2007. Redundancy and specialization among plant microRNAs: role of the MIR164 family in developmental robustness. Development (Cambridge, England) 134: 1051-1060.
98. Soltis PS, Brockington SF, Yoo M-J, Piedrahita A, Latvis M, Moore MJ, Chanderbali AS, Soltis DE. 2009. Floral variation and floral genetics in basal angiosperms. American Journal of Botany 96: 110-128.
99. Soltis PS, Soltis DE. 2014. Flower diversity and angiosperm diversification. In: Riechmann JL, Wellmer F, eds. Flower development: methods and protocols. New York, NY, USA: Springer, 85-102.
100. Stern DL, Orgogozo V. 2008. The loci of evolution: how predictable is genetic evolution? Evolution; International Journal of Organic Evolution 62: 2155-2177.
101. Takeda S, Hanano K, Kariya A, Shimizu S, Zhao L, Matsui M, Tasaka M, Aida M. 2011. CUP-SHAPED COTYLEDON1 transcription factor activates the expression of LSH4 and LSH3, two members of the ALOG gene family, in shoot organ boundary cells. Plant Journal 66: 1066-1077.
102. Takeda S, Matsumoto N, Okada K. 2004. RABBIT EARS, encoding a SUPERMAN-like zinc finger protein, regulates petal development in Arabidopsis thaliana. Development (Cambridge, England) 131: 425-434.
103. Vandenbussche M, Horstman A, Zethof J, Koes R, Rijpkema AS, Gerats T. 2009. Differential recruitment of WOX transcription factors for lateral development and organ fusion in Petunia and Arabidopsis. Plant Cell 21: 2269-2283.
104. Vekemans D, Proost S, Vanneste K, Coenen H, Viaene T, Ruelens P, Maere S, Van de Peer Y, Geuten K. 2012. Gamma paleohexaploidy in the stem lineage of core eudicots: significance for MADS-Box gene and species diversification. Molecular Biology and Evolution 29: 3793-3806.
105. Wagner A. 2008. Gene duplications, robustness and evolutionary innovations. BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology 30: 367-373.
106. Wake DB, Wake MH, Specht CD. 2011. Homoplasy: from detecting pattern to determining process and mechanism of evolution. Science 331: 1032-1035.
107. Wang Z, Luo YH, Li X, Wang LP, Xu SL, Yang J, Weng L, Sato SS, Tabata S, Ambrose M et al. 2008. Genetic control of floral zygomorphy in pea (Pisum sativum L.). Proceedings of the National Academy of Sciences, USA 105: 10414-10419.
108. Wellmer F, Bowman JL, Davies B, Ferrandiz C, Fletcher JC, Franks RG, Graciet E, Gregis V, Ito T, Jack TP et al. 2014. Flower development: open questions and future directions. Flower Development: Methods and Protocols. Methods in Molecular Biology 1110: 103-124.
109. Wellmer F, Riechmann JL. 2010. Gene networks controlling the initiation of flower development. Trends in Genetics 26: 519-527.
110. Wessinger CA, Rausher MD. 2012. Lessons from flower colour evolution on targets of selection. Journal of Experimental Botany 63: 5741-5749.
111. Whitacre JM. 2010. Degeneracy: a link between evolvability, robustness and complexity in biological systems. Theoretical Biology & Medical Modelling 7: 6.
112. Whitacre JM. 2011. Genetic and environment-induced pathways to innovation: on the possibility of a universal relationship between robustness and adaptation in complex biological systems. Evolutionary Ecology 25: 965-975.
113. Williams JH, McNeilage RT, Lettre MT, Taylor ML. 2010. Pollen tube growth and the pollen-tube pathway of Nymphaea odorata (Nymphaeaceae). Botanical Journal of the Linnean Society 162: 581-593.
114. Winter CM, Austin RS, Blanvillain-Baufumé S, Reback Ma, Monniaux M, Wu M-F, Sang Y, Yamaguchi A, Yamaguchi N, Parker JE et al. 2011. LEAFY target genes reveal floral regulatory logic, cis motifs, and a link to biotic stimulus response. Developmental Cell 20: 430-443.
115. Wollmann H, Mica E, Todesco M, Long JA, Weigel D. 2010. On reconciling the interactions between APETALA2, miR172 and AGAMOUS with the ABC model of flower development. Development (Cambridge, England) 137: 3633-3642.
116. Wuest SE, O'Maoileidigh DS, Rae L, Kwasniewska K, Raganelli A, Hanczaryk K, Lohan AJ, Loftus B, Graciet E, Wellmer F. 2012. Molecular basis for the specification of floral organs by APETALA3 and PISTILLATA. Proceedings of the National Academy of Sciences, USA 109: 13452-13457.
117. Xu B, Li Z, Zhu Y, Wang H, Ma H, Dong A, Huang H. 2008. Arabidopsis genes AS1, AS2, and JAG negatively regulate boundary-specifying genes to promote sepal and petal development. Plant Physiology 146: 566-575.
118. Yant L. 2012. Genome-wide mapping of transcription factor binding reveals developmental process integration and a fresh look at evolutionary dynamics. American Journal of Botany 99: 277-290.
119. Yockteng R, Almeida AMR, Morioka K, Alvarez-Buylla ER, Specht CD. 2013. Molecular evolution and patterns of duplication in the SEP/AGL6-like lineage of the zingiberales: a proposed mechanism for floral diversification. Molecular Biology and Evolution 30: 2401-2422.
120. Žádníková P, Simon R. 2014. How boundaries control plant development. Current Opinion in Plant Biology 17: 116-125.
121. Zhang W, Steinmann VW, Nikolov L, Kramer EM, Davis CC. 2013. Divergent genetic mechanisms underlie reversals to radial floral symmetry from diverse zygomorphic flowered ancestors. Frontiers in Plant Science 4: 302.
122. Zhang WH, Xiang QY, Thomas DT, Wiegmann BM, Frohlich MW, Soltis DE. 2008. Molecular evolution of PISTILLATA-like genes in the dogwood genus Cornus (Cornaceae). Molecular Phylogenetics and Evolution 47: 175-195.
123. Zhou X-R, Wang Y-Z, Smith JF, Chen R. 2008. Altered expression patterns of TCP and MYB genes relating to the floral developmental transition from initial zygomorphy to actinomorphy in Bournea (Gesneriaceae). New Phytologist 178: 532-543.
124. Zhu Y, Lin Z, Nakhleh L. 2013. Evolution after whole-genome duplication: a network perspective. G3: Genes, Genomes, Genetics 3: 2049-2057.