Co-modification of class B genes TfDEF and TfGLO in Torenia fournieri Lind. alters both flower morphology and inflorescence architecture

Plant Molecular Biology

Volumn 86, Issue 3, 2014, Pages 319-334

  Sasaki, Katsutomo ^a   Yamaguchi, Hiroyasu ^a   Nakayama, Masayoshi ^a   Aida, Ryutaro ^a   Ohtsubo, Norihiro ^a  

^a NATIONAL INSTITUTE OF VEGETABLE AND TEA SCIENCE   (Japan)

Author keywords

Anthocyanin; Class B gene; MADS; TfDEF; TfGLO; Torenia

Indexed keywords

ANATOMY AND HISTOLOGY; ANGIOSPERM; CELL SHAPE; FLOWER; GENETICS; GROWTH, DEVELOPMENT AND AGING; PHYSIOLOGY; PLANT GENE; TRANSGENIC PLANT;

ANGIOSPERMS; CELL SHAPE; FLOWERS; GENES, PLANT; PLANTS, GENETICALLY MODIFIED;

EID: 84928586577     PISSN: 01674412     EISSN: 15735028     Source Type: Journal    
DOI: 10.1007/s11103-014-0231-8     Document Type: Article

References (60)

1. Aida R (2008) Torenia fournieri (torenia) as a model plant for transgenic studies. Plant Biotechnol 25:541–545
2. Ambrose BA, Lerner DR, Ciceri P, Padilla CM, Yanofsky MF, Schmidt RJ (2000) Molecular and genetic analyses of the silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Mol Cell 5:569–579
3. Bey M, Stüber K, Fellenberg K, Schwarz-Sommer Z, Sommer H, Saedler H, Zachgo S (2004) Characterization of antirrhinum petal development and identification of target genes of the class B MADS box gene DEFICIENS. Plant Cell 16:3197–3215
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. Broholm SK, Pöllänen E, Ruokolainen S, Tähtiharju S, Kotilainen M, Albert VA, Elomaa P, Teeri TH (2010) Functional characterization of B class MADS-box transcription factors in Gerbera hybridada. J Exp Bot 61:75–85
7. Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37
8. Davies B, Motte P, Keck E, Saedler H, Sommer H, Schwarz-Sommer Z (1999) PLENA and FARINELLI: redundancy and regulatory interactions between two Antirrhinum MADS-box factors controlling flower development. EMBO J 18:4023–4034
9. Ditta G, Pinyopich A, Robles P, Pelaz S, Yanofsky MF (2004) The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Curr Biol 14:1935–1940
10. Egea-Cortines M, Saedler H, Sommer H (1999) Ternary complex formation between the MADS-box proteins SQUAMOSA, DEFICIENS and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus. EMBO J 18:5370–5379
11. 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 (2006) Control of petal shape and floral zygomorphy in Lotus japonicus. Proc Natl Acad Sci USA 103:4970–4975
12. Galego L, Almeida J (2002) Role of DIVARICATA in the control of dorsoventral asymmetry in Antirrhinum flowers. Genes Dev 16:880–891
13. Gallie DR, Feder JN, Schimke RT, Walbot V (1991) Post-transcriptional regulation in higher eukaryotes: the role of the reporter gene in controlling expression. Mol Gen Genet 228:258–264
14. Goto K, Meyerowitz EM (1994) Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev 8:1548–1560
15. Hiratsu K, Matsui K, Koyama T, Ohme-Takagi M (2003) Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant J 34:733–739
16. Honma T, Goto K (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409:525–529
17. Jack T, Fox GL, Meyerowitz EM (1994) Arabidopsis homeotic gene APETALA3 ectopic expression: transcriptional and posttranscriptional regulation determine floral organ identity. Cell 76:703–716
18. Kater MM, Dreni L, Colombo L (2006) Functional conservation of MADS-box factors controlling floral organ identityin rice and Arabidopsis. J Exp Bot 57:3433–3444
19. Kim S, Koh J, Yoo MJ, Kong H, Hu Y, Ma H et al (2005) Expression of floral MADS-box genes in basal angiosperms: implications for the evolution of floral regulators. Plant J 43:724–744
20. Kramer EM, Irish VF (1999) Evolution of genetic mechanisms controlling petal development. Nature 399:144–148
21. Kramer EM, Dorit RL, Irish VF (1998) Molecular evolution of genes controlling petal and stamen development: duplication and divergence within the APETALA3 and PISTILLATA MADS-box gene lineages. Genetics 149:765–783
22. 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
23. Krizek BA, Meyerowitz EM (1996) The Arabidopsis homeotic genes APETALA3 and PISTILLATA are sufficient to provide the B class organ identity function. Development 122:11–22
24. Luo D, Carpenter R, Vincent C, Copsey L, Coen E (1996) Origin of floral asymmetry in Antirrhinum. Nature 383:794–799
25. 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
26. Ma H (1994) The unfolding drama of flower development: recent results from genetic and molecular analyses. Genes Dev 8:745–756
27. Melzer R, Theissen G (2009) Reconstitution of ‘floral quartets’ in vitro involving class B and class E floral homeotic proteins. Nucleic Acids Res 37:2723–2736
28. Mitsuda N, Ohme-Takagi M (2009) Functional analysis of transcription factors in Arabidopsis. Plant Cell Physiol 50:1232–1248
29. Mitsuda N, Matsui K, Ikeda M, Nakata M, Oshima Y, Nagatoshi Y, Ohme-Takagi M (2011a) CRES-T, an effective gene silencing system utilizing chimeric repressors. Methods Mol Biol 754:87–105
30. Mitsuda N, Takiguchi Y, Shikata M, Sage-Ono K, Ono M, Sasaki K, Yamaguchi H, Narumi T, Tanaka Y, Sugiyama M, Yamamura T, Terakawa T, Gion K, Suzuri R, Tanaka Y, Nakatsuka T, Kimura S, Nishihara M, Sakai T, Endo-Onodera R, Saitoh K, Isuzugawa K, Oshima Y, Koyama T, Ikeda M, Narukawa M, Matsui K, Nakata M, Ohtsubo N, Ohme-Takagi M (2011b) The new FioreDB database provides comprehensive information on plant transcription factors and phenotypes induced by CRES-T in ornamental and model plants. Plant Biotechnol 28:123–130
31. Mitsuhara I, Ugaki M, Hirochika H, Ohshima M, Murakami T, Gotoh Y, Katayose Y, Nakamura S, Honkura R, Nishimiya S, Ueno K, Mochizuki A, Tanimoto H, Tsugawa H, Otsuki Y, Ohashi Y (1996) Efficient promoter cassettes for enhanced expression of foreign gene in dicotyledonous and monocotyledonous plants. Plant Cell Physiol 37:39–59
32. Mondragón-Palomino M, Hiese L, Härter A, Koch MA, Theissen G (2009) Positive selection and ancient duplications in the evolution of class B floral homeotic genes of orchids and grasses. BMC Evol Biol 9:81. doi:10.1186/1471-2148-9-81
33. Moore RC, Purugganan MD (2005) The evolutionary dynamics of plant duplicate genes. Curr Opin Plant Biol 8:122–128
34. Narumi T, Aida R, Niki T, Nishijima T, Mitsuda N, Hiratsu K, Ohme-Takagi M, Ohtsubo N (2008) Chimeric AGAMOUS repressor induces serrated petal phenotype in Torenia fournieri similar to that induced by cytokinin application. Plant Biotechnol 25:45–53
35. Pelaz S, Ditta GS, Baumann E, Wisman E, Yanofsky MF (2000) B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405:200–203
36. Preston JC, Hileman LC (2009) Developmental genetics of floral symmetry evolution. Trends Plant Sci 14:147–154
37. Riechmann JL, Meyerowitz EM (1997) MADS domain proteins in plant development. Biol Chem 378:1079–1101
38. Riechmann JL, Krizek BA, Meyerowitz EM (1996) Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. Proc Natl Acad Sci USA 93:4793–4798
39. Riechmann JL, Heard J, Martin G, Reuber L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu G (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110
40. 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
41. Rijpkema AS, Gerats T, Vandenbussche M (2007) Evolutionary complexity of MADS complexes. Curr Opin Plant Biol 10:32–38
42. Sablowski RW, Meyerowitz EM (1998) A homolog of NO APICAL MERISTEM is an immediate target of the floral homeotic genes APETALA3/PISTILLATA. Cell 92:93–103
43. Salemme M, Sica M, Gaudio L, Aceto S (2011) Expression pattern of two paralogs of the PI/GLO-like locus during Orchis italica (Orchidaceae, Orchidinae) flower development. Dev Genes Evol 221:241–246
44. Sasaki K, Aida R, Yamaguchi H, Shikata M, Niki T, Nishijima T, Ohtsubo N (2010) Functional divergence within class B MADS-box genes TfGLO and TfDEF in Torenia fournieri Lind. Mol Genet Genomics 284:399–414
45. Shikata M, Ohme-Takagi M (2008) The utility of transcription factors for manipulation of floral traits. Plant Biotechnol 25:31–36
46. Shirasawa-Seo N, Sano Y, Nakamura S, Murakami T, Gotoh Y, Naito Y, Hsia CN, Seo S, Mitsuhara I, Kosugi S, Ohashi Y (2005) The promoter of Milk vetch dwarf virus component 8 confers effective gene expression in both dicot and monocot plants. Plant Cell Rep 24:155–163
47. Sleat DE, Gallie DR, Jefferson RA, Bevan MW, Turner PC, Wilson TMA (1987) Characterisation of the 5ʹ-leader sequence of tobacco mosaic virus RNA as a general enhancer of translation in vitro. Gene 217:217–225
48. Smaczniak C, Immink RG, Muiño 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 (2012) Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development. Proc Natl Acad Sci USA 109:1560–1565
49. Soltis DE, Ma H, Frohlich MW, Soltis PS, Albert VA, Oppenheimer 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 Plant Sci 12:358–367
50. Sommer H, Beltrán JP, Huijser P, Pape H, Lönnig 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
51. Theissen G (2001) Development of floral organ identity: stories from the MADS house. Curr Opin Plant Biol 4:75–85
52. Theissen G, Saedler H (2001) Plant biology. Floral quartets. Nature 409:469–471
53. Tröbner W, Ramirez L, Motte P, Hue I, Huijser P, Lönnig WE, Saedler H, Sommer H, Schwarz-Sommer Z (1992) GLOBOSA: homeotic gene which interact with DEFICIENS in the control of Antirrhinum floralor ganogenesis. EMBO J 11:4693–4704
54. 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
55. Wellmer F, Riechmann JL, Alves-Ferreira M, Meyerowitz EM (2004) Genome-wide analysis of spatial gene expression in Arabidopsis flowers. Plant Cell 16:1314–1326
56. 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
57. 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. Proc Natl Acad Sci USA 109:13452–13457
58. Yang X, Pang HB, Liu BL, Qiu ZJ, Gao Q, Wei L, Dong Y, Wang YZ (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
59. Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM (1990) The protein encoded by the Arabidopsis homeotic gene AGAMOUS resembles transcription factors. Nature 346:35–39
60. Zik M, Irish VF (2003) Global identification of target genes regulated by APETALA3 and PISTILLATA floral homeotic gene action. Plant Cell 15:207–222