Evolution of petaloid sepals independent of shifts in B-class MADS box gene expression

Development Genes and Evolution

Volumn 222, Issue 1, 2012, Pages 19-28

  Landis, Jacob B ^a,b   Barnett, Laryssa L ^a,c   Hileman, Lena C ^a  

^a UNIVERSITY OF KANSAS   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c DUKE UNIVERSITY   (United States)

Author keywords

ABC model; Antirrhinum majus (snapdragon); B class genes; Petal identity; Rhodochiton atrosanguineum

Indexed keywords

ANTIRRHINUM; ANTIRRHINUM MAJUS; ARTICLE; FLORAL WHORL; GENE CONTROL; GENE EXPRESSION; MADS BOX GENE; MICROMORPHOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; PETAL; PETALIOD SEPAL; PLANT DEVELOPMENT; PLANT EVOLUTION; PLANT GENE; PLANT MODEL; PLANT STRUCTURES; PLANTAGINACEAE; PRIORITY JOURNAL; RHODOCHITON ATROSANGUINEUM; SCANNING ELECTRON MICROSCOPY; SEPAL; SPECIES IDENTIFICATION;

ANTIRRHINUM; FLOWERS; GENE EXPRESSION REGULATION, PLANT; MADS DOMAIN PROTEINS; PHYLOGENY; PLANT PROTEINS; SCROPHULARIACEAE;

ANIMALIA; ANTIRRHINUM; ANTIRRHINUM MAJUS; MAGNOLIOPHYTA; RHODOCHITON ATROSANGUINEUM;

EID: 84857897197     PISSN: 0949944X     EISSN: 1432041X     Source Type: Journal    
DOI: 10.1007/s00427-011-0385-1     Document Type: Article

References (78)

1. Ambrose B, Lerner D, Ciceri P, Padilla C, Yanofsky M, Schmidt R (2000) Molecular and genetic analyses of the silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Mol Cell 5:569-579
2. Borchert T, Eckardt K, Fuchs J, Krueger K, Hohe A (2009) 'Who's who' in two different flower types of Calluna vulgaris (Ericaceae): morphological and molecular analyses of flower organ identity. BMC Plant Biol 9:148
3. Bowman JL (1997) Evolutionary conservation of angiosperm flower development at the molecular and genetic levels. J Biosci 22:515-527
4. Bowman JL, Smyth DR, Meyerowitz EM (1989) Genes directing flower development in Arabidopsis. Plant Cell 1:37-52
5. Bowman JL, Smyth DR, Meyerowitz EM (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112:1-20
6. Brockington SF (2009) Evolution and development of petals in Aizoaceae (Caryophyllales). Dissertation, University of Florida
7. Brockington SF, Alexandre R, Ramdial J, Moore MJ, Crawley S, Dhingra A, Hilu K, Soltis DE, Soltis PS (2009) Phylogeny of the Caryophyllales sensu lato: revisiting hypotheses on pollination biology and perianth differentiation in the core Caryophyllales. Int J Plant Sci 170:627-643
8. Brockington SF, Rudall PJ, FrohlichMW, Oppenheimer DG, Soltis PS, Soltis DE (2011) "Living stones" reveal alternative petal identity programs within the core eudicots. Plant J. doi:10.1111/j.1365-313X.2011.04797.x
9. Broholm SK, Pollanen E, Ruokolainen S, Tahtiharju S, Kotilainen M, Albert VA, Elomaa P, Teeri TH (2010) Functional characterization of B class MADS-box transcription factors in Gerbera hybrida. J Exp Bot 61:75-85
10. Carpenter R, Coen E (1990) Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus. Genes Dev 4:1483-1493
11. Christensen K, Hansen H (1998) SEM-studies of epidermal patterns in the angiosperms. Opera Botanica 135:1-91
12. Coen E, Meyerowitz E (1991) The war of the whorls - genetic interactions controlling flower development. Nature 353:31-37 (Pubitemid 21912446)
13. Coen E, Doyle S, Romero J, Elliott R, Magrath R, Carpenter R (1991) Homeotic genes controlling flower development in Antirrhinum. Development 113:149-155
14. Cronk Q, Ojeda I (2008) Bird-pollinated flowers in an evolutionary and molecular context. J Exp Bot 59:715-727 (Pubitemid 351644665)
15. De Craene LPR (2007) Are petals sterile stamens or bracts? The origin and evolution of petals in the core eudicots. Ann Bot 100:621-630
16. De Craene LPR (2008) Homology and evolution of petals in the core eudicots. Syst Bot 33:301-325
17. de Martino G, Pan I, Emmanuel E, Levy A, Irish VF (2006) Functional analyses of two tomato APETALA3 genes demonstrate diversification in their roles in regulating floral development. Plant Cell 18:1833-1845 (Pubitemid 44260181)
18. Di Stilio VS, Martin C, Schulfer AF, Connelly CF (2009) An ortholog of MIXTA-like2 controls epidermal cell shape in flowers of Thalictrum. New Phytol 183:718-728
19. Drea S, Hileman LC, De Martino G, Irish VF (2007) Functional analyses of genetic pathways controlling petal specification in poppy. Development 134:4157-4166
20. Edgar R (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792-1797
21. Geuten K, Becker A, Kaufmann K, Caris P, Janssens S, Viaene T, Theissen G, Smets E (2006) Petaloidy and petal identity MADS-box genes in the balsaminoid genera Impatiens and Marcgravia. Plant J 47:501-518 (Pubitemid 44141698)
22. Glover BJ (2007) Understanding flowers and flowering: an integrated approach. Oxford University Press, Oxford
23. Glover B, Martin C (1998) The role of petal cell shape and pigmentation in pollination success in Antirrhinum majus. Heredity 80:778-784 (Pubitemid 28329396)
24. Goto K, Meyerowitz E (1994) Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev 8:1548-1560 (Pubitemid 24218289)
25. Hileman LC, Irish VF (2009) More is better: the uses of developmental genetic data to reconstruct perianth evolution. Am J Bot 96:83-95
26. Hileman LC, Sundstrom JF, Litt A, Chen M, Shumba T, Irish VF (2006) Molecular and phylogenetic analyses of the MADS-box gene family in tomato. Mol Biol Evol 23:2245-2258 (Pubitemid 44536830)
27. Howarth D, Baum D (2005) Genealogical evidence of homoploid hybrid speciation in an adaptive radiation of Scaevola (Goodeniaceae) in the Hawaiian Islands. Evolution 59:948-961 (Pubitemid 40728428)
28. Huelsenbeck J, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754-755 (Pubitemid 32851390)
29. Irish VF (2009) Evolution of petal identity. J Exp Bot 60:2517-2527
30. Jack T, Brockman L, Meyerowitz E (1992) The homeotic gene APETALA3 of Arabidopsis thaliana encodes a Mads-box and is expressed in petals and stamens. Cell 68:683-697
31. Jackson D (1991) In situ hybridization in plants. Mol Plant Pathol Pract Approach 1:163-174
32. Jaramillo M, Kramer E (2004) APETALA3 and PISTILLATA homologs exhibit novel expression patterns in the unique perianth of Aristolochia (Aristolochiaceae). Evol Dev 6:449-458 (Pubitemid 39554260)
33. Jaramillo MA, Kramer EM (2007) Molecular evolution of the petal and stamen identity genes, APETALA3 and PISTILLATA, after petal loss in the Piperales. Mol Phylogenet Evol 44:598-609 (Pubitemid 47048933)
34. Kang H, Jeon J, Lee S, An G (1998) Identification of class B and class C floral organ identity genes from rice plants. Plant Mol Biol 38:1021-1029 (Pubitemid 29000314)
35. Kanno A, Saeki H, Kameya T, Saedler H, Theissen G (2003) Heterotopic expression of class B floral homeotic genes supports a modified ABC model for tulip (Tulipa gesneriana). Plant Mol Biol 52:831-841 (Pubitemid 37065235)
36. Kay Q, Daoud H, Stirton C (1981) Pigment distribution, light reflection and cell structure in petals. Bot J Linn Soc 83:57-83
37. Kim S, Yun P, Fukuda T, Ochiai T, Yokoyama J, Kameya T, Kanno A (2007) Expression of a DEFICIENS-like gene correlates with the differentiation between sepal and petal in the orchid, Habenaria radiata (Orchidaceae). Plant Sci 172:319-326 (Pubitemid 46091709)
38. Kramer EM (2007) Understanding the genetic basis of floral diversity. Bioscience 57:479-487
39. Kramer E, Di Stilio V, Schluter P (2003) Complex patterns of gene duplication in the APETALA3 and PISTILLATA lineages of the Ranunculaceae. Int J Plant Sci 164:1-11 (Pubitemid 36198804)
40. 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 (Pubitemid 46953225)
41. Krizek B, Meyerowitz E (1996) The Arabidopsis homeotic genes APETALA3 and PISTILLATA are sufficient to provide the B class organ identity function. Development 122:11-22 (Pubitemid 26038414)
42. Litt A, Kramer EM (2010) The ABC model and the diversification of floral organ identity. Semin Cell Dev Biol 21:129-137
43. Liu Y, Nakayama N, Schiff M, Litt A, Irish V, Dinesh-Kumar S (2004) Virus induced gene silencing of a DEFICIENS ortholog in Nicotiana benthamiana. Plant Mol Biol 54:701-711
44. Maddison D, Maddison W (2005) MacClade 4: analysis of phylogeny and character evolution. 4.08
45. Maturen N (2008) Genetic analysis of the evolution of petaloid bracts in dogwoods. Dissertation, University of Michigan
46. Nakamura T, Fukuda T, Nakano M, Hasebe M, Kameya T, Kanno A (2005) The modified ABC model explains the development of the petaloid perianth of Agapanthus praecox ssp. orientalis (Agapanthaceae) flowers. Plant Mol Biol 58:435-445 (Pubitemid 41125996)
47. Noda K, Glover B, Linstead P, Martin C (1994) Flower color intensity depends on specialized cell-shape controlled by a Myb-related transcription factor. Nature 369:661-664 (Pubitemid 24199471)
48. Park J, Ishikawa Y, Yoshida R, Kanno A, Kameya T (2003) Expression of AoDEF, a B-functional MADS-box gene, in stamens and inner tepals of the dioecious species Asparagus officinalis L. Plant Mol Biol 51:867-875 (Pubitemid 36573166)
49. Park J, Ishikawa Y, Ochiai T, Kanno A, Kameya T (2004) Two GLOBOSA-like genes are expressed in second and third whorls of homochlamydeous flowers in Asparagus officinalis L. Plant Cell Physiol 45:325-332 (Pubitemid 38473461)
50. Perez-Rodriguez M, Jaffe F, Butelli E, Glover B, 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 (Pubitemid 40268285)
51. Prasad K, Vijayraghavan U (2003) Double-stranded RNA interference of a rice PI/GLO paralog, OsMADS2, uncovers its second-whorl-specific function in floral organ patterning. Genetics 165:2301-2305 (Pubitemid 38040310)
52. Prasad K, Sriram P, Kumar C, Kushalappa K, Vijayraghavan U (2001) Ectopic expression of rice OsMADS1 reveals a role in specifying the lemma and palea, grass floral organs analogous to sepals. Dev Genes Evol 211:281-290 (Pubitemid 32821514)
53. Preston JC, Kellogg EA (2007) Conservation and divergence of APETALA1/FRUITFULL-like gene function in grasses: evidence from gene expression analyses. Plant J 52:69-81 (Pubitemid 47476159)
54. Rasmussen DA, Kramer EM, Zimmer EA (2009) One size fits all? Molecular evidence for a commonly inherited petal identity program in Ranunculales. Am J Bot 96:96-109
55. Rijpkema AS, Royaert S, Zethof J, van der Weerden G, Gerats T, Vandenbussche M (2006) Analysis of the Petunia TM6 MADS-box gene reveals functional divergence within the DEF/AP3 lineage. Plant Cell 18:1819-1832 (Pubitemid 44260180)
56. Ronquist F, Huelsenbeck J (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574 (Pubitemid 37038874)
57. Schwarz-Sommer Z, Huijser P, Nacken W, Saedler H, Sommer H (1990) Genetic control of flower development by homeotic genes in Antirrhinum majus. Science 250:931-936 (Pubitemid 120031791)
58. Sharma B, Guo C, Kong H, Kramer EM (2011) Petal-specific subfunctionalization of an APETALA3 paralog in the Ranunculales and its implications for petal evolution. New Phytol 191:870-883
59. Soltis PS, Brockington SF, Yoo M, Piedrahita A, Latvis M, Moore MJ, Chanderbali AS, Soltis DE (2009) Floral variation and floral genetics in basal Angiosperms. Am J Bot 96:110-128
60. Sommer H, Beltran JP, Huijser P, Pape H, Lonnig WE, Saedler H, Schwarz-Sommer Z (1990) DEFICIENS, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus - the protein shows homology to transcription factors. EMBO J 9:605-613
61. Sutton DA (1988) A revision of the tribe Antirrhineae. British Museum Natural History. Oxford University Press, London
62. Swofford D (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods) 4
63. Trobner W, Ramirez L, Motte P, Hue I, Huijser P, Lonnig WE, Saedler H, Sommer H, Schwarz-Sommer Z (1992) GLOBOSA - a homeotic gene which interacts with DEFICIENS in the control of Antirrhinum floral organogenesis. EMBO J 11:4693-4704 (Pubitemid 23023411)
64. Tzeng TY, Yang CH (2001) A MADS-box gene from lily (Lilium longiflorum) is sufficient to generate dominant negative mutation by interacting with PISTILLATA (PI) in Arabidopsis thaliana. Plant Cell Physiol 42:1156-1168 (Pubitemid 33037884)
65. Vandenbussche M, Zethof J, Royaert S, Weterings K, Gerats T (2004) The duplicated B-class heterodimer model: whorl-specific effects and complex genetic interactions in Petunia hybrida flower development. Plant Cell 16:741-754 (Pubitemid 38335283)
66. Vargas P, Rossello JA, Oyama R, Guemes J (2004) Molecular evidence for naturalness of genera in the tribe Antirrhineae (Scrophulariaceae) and three independent evolutionary lineages from the New World and the Old. Plant Syst Evol 249:151-172 (Pubitemid 40047488)
67. Weiss D (2000) Regulation of flower pigmentation and growth: multiple signaling pathways control anthocyanin synthesis in expanding petals. Physiol Plant 110:152-157
68. Whipple CJ, Ciceri P, Padilla CM, Ambrose BA, Bandong SL, Schmidt RJ (2004) Conservation of B-class floral homeotic gene function between maize and Arabidopsis. Development 131:6083-6091 (Pubitemid 40123922)
69. Whitney HM, Glover BJ (2007) Morphology and development of floral features recognised by pollinators. Arthropod-Plant Interact 1:147-158
70. Whitney HM, Chittka L, Bruce TJA, Glover BJ (2009) Conical epidermal cells allow bees to grip flowers and increase foraging efficiency. Curr Biol 19:948-953
71. Whittall JB, Voelckel C, Kliebenstein DJ, Hodges SA (2006) Convergence, constraint and the role of gene expression during adaptive radiation: floral anthocyanins in Aquilegia. Mol Ecol 15:4645-4657 (Pubitemid 44749576)
72. Wu H, Su H, Hu J (2007) The identification of A-, B-, C-, and E-class MADS-box genes and implications for perianth evolution in the basal eudicot Trochodendron aralioides (Trochodendraceae). Int J Plant Sci 168:775-799 (Pubitemid 47105616)
73. Xiao H, Wang Y, Liu DF, Wang WM, Li XB, Zhao XF, Xu JC, Zhai WX, Zhu LH (2003) Functional analysis of the rice AP3 homologue OsMADS16 by RNA interference. Plant Mol Biol 52:957-966 (Pubitemid 37181489)
74. Yang YZ, Fanning L, Jack T (2003) The K domain mediates heterodimerization of the Arabidopsis floral organ identity proteins, APETALA3 and PISTILLATA. Plant J 33:47-59 (Pubitemid 36117289)
75. Yoo M, Soltis PS, Soltis DE (2010) Expression of floral MADS-box genes in two divergent water lilies: Nymphaeales and Nelumbo. Int J Plant Sci 171:121-146
76. Zanis MJ, Soltis PS, Qiu YL, Zimmer E, Soltis DE (2003) Phylogenetic analyses and perianth evolution in basal angiosperms. Ann Mo Bot Gard 90:129-150 (Pubitemid 36726022)
77. Zhang W, Xiang Q, Thomas DT, Wiegmann BM, Frohlich MW, Soltis DE (2008) Molecular evolution of PISTILLATA-like genes in the dogwood genus Cornus (Cornaceae). Mol Phylogenet Evol 47:175-195
78. Zwickl D (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Dissertation, University of Texas-Austin