Expression analysis of an APETALA1/FRUITFULL-like gene in Phalaenopsis sp. 'Hatsuyuki' (Orchidaceae)

Horticulture Environment and Biotechnology

Volumn 52, Issue 2, 2011, Pages 183-195

  Song, In Ja ^a   Fukuda, Tatsuya ^b   Ko, Suk Min ^a   Ito, Takuro ^c   Yokoyama, Jun ^d   Ichikawa, Hiroyuki ^e   Horikawa, Yoh ^f   Kameya, Toshiaki ^g   Kanno, Akira ^g   Lee, Hyo Yeon ^a  

^a Jeju National University   (South Korea)

^b KOCHI UNIVERSITY   (Japan)

^c KEIO UNIVERSITY   (Japan)

^d YAMAGATA UNIVERSITY   (Japan)

^e Akabira Orchid Corp   (Japan)

^f OBIHIRO UNIVERSITY OF AGRICULTURE AND VETERINARY MEDICINE   (Japan)

^g TOHOKU UNIVERSITY   (Japan)

Author keywords

A class; AP1 FUL like gene; floral organs

Indexed keywords

ANTIRRHINUM; ARABIDOPSIS; LILIOPSIDA; ORCHIDACEAE; PHALAENOPSIS; PHALAENOPSIS SP.;

EID: 84864485903     PISSN: 22113452     EISSN: 22113460     Source Type: Journal    
DOI: 10.1007/s13580-011-0199-0     Document Type: Article

References (92)

1. Baum, D. A. 2002. Identifying the genetic causes of phenotypic evolution: a review of experimental strategies. In: Developmental Genetics and Plant Evolution, (Cronk QCB, Bateman RM, Hawkins JA, eds.), Taylor and Francies, London, p. 493-507.
2. Becker, A., K. U. Winter, B. Meyer, H. Saedler, and G. Theissen. 2000. MADS-box gene diversity in seed plants 300 million years ago. Mol. Biol. Evol. 17: 1425-1434.
3. Becker, A. and G. Theissen. 2003. The major clade of MADS-box genes and their role in the development and evolution of flowering plants. Mol. Phylogenet. Evol. 29: 464-484.
4. Berbel, A., C. Navarro, C. Ferrandiz, L. A. Canas, F. Madueno, and J. P. Beltran. 2001. Analysis of PEAM4, the pea AP1 functional homologue, supports a model for AP1-like genes controlling both floral meristem and floral organ identity in different species. Plant J. 25: 441-451.
5. Bowman, J. L., D. R. Smyth, and E. M. Meyerowitz. 1989. Gene directing flower development in Arabidopsis. Plant Cell 1: 37-52.
6. Bowman, J. L., D. R. Smyth, and E. M. Meyerowitz. 1991. Genetic interactions among floral homeotic genes of Arabidopsis. Development 112: 1-20.
7. Bowman, J. L., J. Alvarez, D. Weigel, E. M. Meyerowitz, and D. R. Smyth. 1993. Control of flower development in Arabidopsis thaliana by APETALA1 and interacting genes. Development 119: 721-743.
8. Carpenter, R. and E. S. Coen. 1990. Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus. Gene Dev. 4: 1483-1493.
9. Carlsbecker, A., K. Tandre, I. J. Johanson, M. Englund, and P. Engström. 2004. The MADS-box gene DAL1 is a potential mediator of the juvenile-to-adult transition in Norway spruce (Picea abies). Plant J. 40: 546-557.
10. Cho, S., S. Jang, S. Chae, K. M. Chung, Y. H. Moon, G. An, and S. K. Jang. 1999. Analysis of the C-terminal region of Arabidopsis thaliana APETALA1 as a transcription activation domain. Plant Mol. Biol. 40: 419-429.
11. Coen, E. S. and E. M. Meyerowitz. 1991. The war of the whorls: genetic interactions controlling flower development. Nature 353: 31-37.
12. Cozzolino, S. and A. Widmer. 2005. Orchid diversity: an evolutionary consequence of deception? Trends Ecol. Evol. 20: 487-494.
13. Davies, B., M. Egea-Cortines, E. de Andrade Silva, H. Saedler, and H. Sommer. 1996. Multiple interactions amongst floral homeotic MADS box proteins. EMBO J. 15: 4330-4343.
14. Davies, B. and Z. Schwarz-Sommer. 1994. Control of floral organ identity by homeotic MADS box transcription factors. In: Nover L (ed.), Results and problems in cell differentiation. Springer, Berlin Heidelberg New York, p. 235-258.
15. Egea-Cortines, M., H. Saedler, and H. Sommer. 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.
16. Elo, A., J. Lemmetyinen, M. L. Turunen, L. Tikka, and T. Sopanen. 2001. Three MADS-box genes similar to APETALA1 and FRUITFULL from silver birch (Betula pendula). Physiol. Plant 112: 95-103.
17. Endress, P. K. 1994. Floral structure and evolution of primitive angiosperms: recent advances. Plant Syst. Evol. 192: 79-97.
18. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783-791.
19. Ferrandiz, C., Q. Gu, R. Martienssen, and M. F. Yanofsky. 2000. Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development 127: 725-734.
20. Fornara, F., L. Parenicova, G. Falasca, N. Pelucci, S. Masiero, S. Ciannamea, Z. Lopez-Dee, M. M. Altamura, L. Colombo, and M. M. Kater. 2004. Functional characterization of OsMADS18, a member of the AP1/SQUA subfamily of MADS box genes. Plant Physiol. 135: 2207-2219.
21. Freudenstein, J. V., E. M. Harris, and F. N. Rasmussen. 2002. The evolution of anther morphology in orchids: incumbent anthers, superposed pollinia, and the vandoid complex. Am. J. Bot. 89: 1747-1755.
22. Frohman, M. A., M. K. Dush, and G. R. Martin. 1988. Rapid production of full-length cDNA from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc. Natl. Acad. Sci. USA 85: 8998-9002.
23. Gerber, H. P., K. Seipel, O. Georgiev, M. Hofferer, M. Hug, S. Rusconi, and W. Schaffner. 1994. Transcriptional activation modulated by homopolymeric glutamine and proline stretches. Science 263: 808-811.
24. Gocal, G. F., R. W. King, C. A. Blundell, O. M. Schwartz, C. H. Andersen, and D. Weigel. 2001. Evolution of floral meristem identity genes. Analysis of Lolium temulentum genes related to APETALA1 and LEAFY of Arabidopsis. Plant Physiol. 125: 1788-1801.
25. Greco, R., L. Stagi, L. Colombo, G. C. Angenent, M. Sari-Gorla, M. E. Pé. 1997. MADS box genes expressed in developing inflorescences of rice and sorghum. Mol. Gen. Genet. 253: 615-623.
26. Gu, Q., C. Ferrandiz, M. F. Yanofsky, and R. Martienssen. 1998. The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development 125: 1509-1517.
27. Gustafson-Brown, C., B. Savidge, and M. F. Yanofsky. 1994. Regulation of the Arabidopsis homeotic gene APETALA1. Cell 76: 131-143.
28. Hardenack, S., D. Ye, H. Saedler, and S. Grant. 1994. Comparison of MADS-box gene expression in developing male and female flowers of the dioecious plant white campion. Plant Cell 6: 1775-1787.
29. Hasebe, M. 1999. Evolution of reproductive organs in land plants. J. Plant Res. 112: 463-474.
30. Hempel, F. D., D. Weigel, M. A. Mandel, G. Ditta, P. C. Zambryski, L. J. Feldman, and M. F. Yanofsky. 1997. Floral determination and expression of floral regulatory genes in Arabidopsis. Development 124: 3845-3853.
31. Heuer, S., S. Hansen, J. Bantin, R. Brettschneider, E. Kranz, H. Lörz, and T. Dresselhaus. 2001. The maize MADS box gene ZmMADS3 affects node number and spikelet development and is co-expressed with ZmMADS1 during flower development in egg cells and early embryogenesis. Plant Physiol. 127: 33-45.
32. Huijser, P., J. Klein, W. E. Lönnig, H. Meijer, H. Saedler, and H. Sommer. 1992. Bractomania, an inflorescence anomaly, is caused by the loss of function of the MADS-box gene SQUAMOSA in Antirrhinum majus. EMBO J. 11: 1239-1249.
33. Immink, R. G., D. J. Hannaple, S. Ferrario, M. Busscher, J. Franken, M. M. Lookeren Campagne, and G. C. Angenent. 1999. A petunia MADS box gene involved in the transition from vegetative to reproductive development. Development 126: 5117-5126.
34. Irish, V. F. and I. M. Sussex. 1990. Function of the apetala-1 gene during Arabidopsis floral development. Plant Cell 2: 741-753.
35. Irish, V. F. and Y. T. Yamamoto. 1995. Conservation of floral homeotic gene function between Arabidopsis and Antirrhinum. Plant Cell 7: 1635-1644.
36. Jeon, J. S., S. Lee, K. H. Jung, W. S. Yang, G. H. Yi, B. G. Oh, and G. An. 2000. Production of transgenic rice plants showing reduced heading data and plant height by ectopic expression of rice MADS box gene. Mol. Breed. 6: 581-592.
37. Johansen, B. and S. Frederiksen. 2002. Orchid flowers: evolution and molecular development. In: Q. C. B. Cronk, R. M. Bateman, J. A. Hawkins (eds.), Developmental Genetics and Plant Evolution. Taylor & Francis, London, p. 206-219.
38. Kato, Y., K. Aioi, Y. Omori, N. Takahata, and Y. Satta. 2003. Phylogenetic analyses of Zostera species based on rbcL and matK nucleotide sequences: Implications for the origin and diversification of seagrasses in Japanese waters. Genes Genet. Syst. 78: 329-342.
39. Kempin, S. A., B. Savidge, and M. F. Yanofsky. 1995. Molecular basis of the cauliflower phenotype in Arabidopsis. Science 267: 522-525.
40. Kramer, E. M., R. L. Dorit, and V. F. Irish. 1998. Molecular evolution of gene controlling petal and stamen development: duplicate and divergence within the APETALA3 and PISTILLATA MADS-Box gene lineages. Genetics 149: 765-783.
41. Kramer, E. M., M. Alejandra-Jaramillo, and V. S. Di Stilio. 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.
42. Krizek, B. A. and E. M. Meyerowitz. 1996. Mapping the protein regions responsible for the functional specificities of the Arabidopsis MADS domain organ-identity protein. Proc. Natl. Acad. Sci. USA 93: 4063-4070.
43. Kyozuka, J., R. Harcourt, W. J. Peacock, and E. S. Dennis. 1997. Eucalyptus has functional equivalents of the Arabidopsis AP1 gene. Plant Mol. Biol. 35: 573-584.
44. Li, G. S., Z. Meng, H. Z. Kong, Z. D. Chen, G. Theissen, and A. M. Lu. 2005. Characterization of candidate class A, B and E floral homeotic genes from the perianthless basal angiosperm Chloranthus spicatus (Chloranthaceae). Dev. Genes Evol. 215: 437-449.
45. Litt, A. and V. F. Irish. 2003. Duplication and diversification in the APETALA1/FRUITFULL floral homeotic gene lineage: implications for the evolution of floral development. Genetics 165: 821-833.
46. Maddison, W. P. 1991. The discovery and importance of multiple islands of most-parsimonious trees. Syst. Zool. 40: 315-328.
47. Maes, T., N. van de Steene, J. Zethof, M. Karimi, M. D'Hauw, G. Mares, M. van Montagu, and T. Gerats. 2001. Petunia AP2-like genes and their role in flower and seed development. Plant Cell 13: 229-244.
48. Mandel, M. A., C. Gustafson-Brown, B. Savidge, and M. F. Yanofsky. 1992. Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360: 273-277.
49. Mandel, M. A. and M. F. Yanofsky. 1995a. A gene trigging flower formation in Arabidopsis. Nature 377: 522-524.
50. Mandel, M. A. and M. F. Yanofsky. 1995b. The Arabidopsis AGL8 MADS box gene is expressed in inflorescence meristems and is negatively regulated by APETALA1. Plant Cell 7: 1763-1771.
51. Mathews, S. and D. J. Donoghue. 1999. The root of angiosperm phylogeny inferred from duplicate phytochrome genes. Science 286: 947-950.
52. Mena, M., M. A. Mandel, D. R. Lerner, M. F. Yanofsky, and R. J. Schmidt. 1995. A characterization of the MADS-box gene family in maize. Plant J. 8: 845-854.
53. Moon, Y. H., H. G. Kang, J. Y. Jung, J. S. Jeon, S. K. Sung, and G. An. 1999. Determination of the motif responsible for interaction between the rice APETALA1/AGAMOUS-like9 family proteins using a yeast two-hybrid system. Plant Physiol. 120: 1193-1204.
54. Müller, B. M., H. Saedler, and S. Zachgo. 2001. The MADS-box gene DEFH28 from Antirrhinum is involved in the regulation of floral meristem identity and fruit development. Plant J. 28: 169-179.
55. Münster, T., W. Deleu, L. U. Wingen, M. Ouzunova, J. Cacharron, W. Faigl, S. Werth, J. T. Kim, H. Saedler, and G. Theissen. 2002. Maize MADS-box genes galore. Maydica 47: 287-301.
56. Münster, T., J. Pahnke, A. Di Rosa, J. T. Kim, W. Martin, H. Saedler, and G. Theissen. 1997. Floral homeotic genes were recruited from homologous MADS-box genes preexisting in the common ancestor of ferns and seed plants. Proc. Natl. Acad. Sci. USA 94: 2415-2420.
57. Murai, K., M. Miyamae, H. Kato, S. Takumi, and Y. Ogihara. 2003. WAP1, a wheat APETALA1 homolog, plays a central role in the phase transition from vegetative to reproductive growth. Plant Cell Physiol. 44: 1255-1265.
58. Murray, M. G. and W. F. Thompson. 1980. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res. 8: 4321-4325.
59. Ng, M. and M. F. Yanofsky. 2001. Functional and evolution of the plant MADS-box gene family. Nat. Rev. Genet. 2: 186-195.
60. Nurrish, S. J. and R. Treisman. 1995. DNA binding specificity determinants in MADS-box transcriptional factors. Mol. Cell Biol. 15: 4076-4085.
61. Perrière, G. and M. Gouy. 1996. www-Query: An on-line retrieval system for biological sequence banks. Biochemie 78: 364-369.
62. Petersen, K., T. Didion, C. H. Andersen, K. K. Nielsen. 2004. MADS-box genes from perennial ryegrass differentially expressed during transition from vegetative to reproductive growth. J. Plant Physiol. 161: 439-447.
63. Pnueli, L., M. Abu-Abeid, D. Zamir, W. Nacken, Z. S. Schwarz-Sommer, and E. Lifschitz. 1991. The MADS box gene family in tomato: temporal expression during floral development, conserved secondary structures and homology with homeotic genes from Antirrhinum and Arabidopsis. Plant J. 1: 255-266.
64. Purugganan, M. D. 1997. The MADS-box floral homeotic gene lineages predate the origin of seed plants: phylogenetic and molecular clock estimates. J. Mol. Evol. 45: 392-396.
65. Purugganan, M. D. 1998. The molecular evolution of development. Bioessays 20: 700-711.
66. Purugganan, M. D. 2000 The molecular population genetics of regulatory genes. Mol. Ecol. 9: 1451-1461.
67. Purugganan, M. D., S. D. Rounsley, R. J. Schmidt, and M. Yanofsky. 1995. Molecular evolution of flower development: diversification of the plant MADS-box regulatory gene family. Genetics 140: 345-356.
68. Qiu, Y. L., J. Lee, F. Bernasconi-Quadroni, D. E. Soltis, P. S. Soltis, M. Zain, E. A. Zimmer, Z. Chen, V. Savolainen, and M. W. Chase. 1999. The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes. Nature 402: 404-407.
69. Schmitz, J., R. Franzen, T. Ngyuen, F. Garcia-Maroto, C. Pozzi, F. Salamini, and W. Rohde. 2000. Cloning, mapping and expression analysis of six barley MADS-box genes. Plant Mol. Biol. 42: 899-913.
70. Shepard, K. A. and M. D. Purugganan. 2002. The genetics of plant morphological evolution. Curr. Opin. Plant Biol. 5: 49-55.
71. Shore, P. and A. D. Sharrocks. 1995. The MADS-box family of transcription factors. Eur. J. Biochem. 229: 1-13.
72. Skipper, M., K. B. Pedersen, L. B. Johansen, S. Frederiksen, V. F. Irish, and B. B. Johansen. 2005. Identification and quantification of expression levels of three FRUITFULL-like MADS-box genes from the orchid Dendrobium thyrsiflorum (Reichb. f). Plant Sci. 169: 579-586.
73. Soltis, P. S., D. E. Soltis, and M. W. Chase. 1999. Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402: 402-404.
74. Sung, S. K., G. H. Yu, and G. An. 1999. Characterization of MdMADS2, a member of the SQUAMOSA subfamily of genes, in apple. Plant Physiol. 120: 969-978.
75. Swofford, D. L. 2000. PAUP: Phylogenetic analysis using persimony (and other methods). Sinauer Associates, Sunderland, MA.
76. Tamura, M. N., J. Yamashita, S. Fuse, and M. Haraguchi. 2004. Molecular phylogeny of monocotyledons inferred from combined analysis of plastid matK and rbcL gene sequences. J. Plant Res. 117: 109-120.
77. Theissen, G., A. Becker, A. Di Rosa, A. Kanno, J. T. Kim, T. Münster, K. U. Winter, and H. Saedler. 2000. A short history of MADS-box genes in plants. Plant Mol. Biol. 42: 115-149.
78. Theissen, G., A. Becker, K. U. Winter, T. Münster, C. Kirchner, and H. Saedler. 2002. How the land plants learned their floral ABCs: the role of MADS-box genes in the evolutionary origin of flowers. In: Cronk QCB, Bateman RM, Hawkins JA (eds.), Developmental Genetics and Plant Evolution. Taylor & Francis, London, p. 173-205.
79. Theissen, G., J. T. Kim, and H. Saedler. 1996. Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes. J. Mol. Evol. 43: 484-516.
80. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
81. Trevaskis, B., D. J. Bagnall, M. H. Ellis, W. J. Peacock, and E. S. Dennis. 2003. MADS box genes control vernalization-induced flowering in cereals. Proc. Natl. Acad. Sci. USA 100: 13099-13104.
82. Tsaftaris, A. S., K. Pasentsis, I. Iliopoulos, and A. N. Polidoros. 2004. Isolation of three homologous AP1-like MADS-box genes in crocus (Crocus sativus L.) and characterization of their expression. Plant Sci. 166: 1235-1243.
83. Vahala, T., B. Oxelman, and S. von Arnold. 2001. Two APETALA2-like genes of Picea abies are differentially expressing during development. J. Exp. Bot. 52: 1111-1115.
84. Vandenbussche, M., G. Theissen, Y. van de Peer, and T. Gerats. 2003. Structual diversification and neo-functionalization during floral MADS-box gene evolution by C-terminal frameshift mutations. Nucleic Acid Res. 31: 4401-4409.
85. Weigel, D. and E. M. Meyerowitz. 1994. The ABCs of floral homeotic genes. Cell 78: 203-209.
86. Yalovsky, S., M. Rodriguez-Concepcion, K. Bracha, G. Toledo-Ortiz, and W. Gruissem. 2000. Prenylation of the floral transcription factor APETALA1 modulates its function. Plant Cell 12: 1257-1266.
87. Yan, L., A. Loukoianov, G. Tranquilli, M. Helguera, T. Fahima, and J. Dubcovsky. 2003. Positional cloning of the wheat vernalization gene VRN1. Proc. Natl. Acad. Sci. USA 100: 6263-6268.
88. Yang, Y., L. Fanning, and T. Jack. 2003. The K domain mediates heterodimerization of the Arabidopsis floral organ identity protein APETALA3 and PISTILLATA. Plant J. 33: 47-59.
89. Yang, Y. and T. Jack. 2004. Defining subdomains of the K domain important for protein-protein interactions of plant MADS protein. Plant Mol. Biol. 55: 45-59.
90. Yu, H. and C. J. Goh. 2000. Identification and characterization of three orchid MADS-box genes of the AP1/AGL9 subfamily during floral transition. Plant Physiol. 123: 1325-1336.
91. Yun, P. Y., T. Ito, S. Y. Kim, A. Kanno, and T. Kameya. 2004a. AVAG1 gene is involved in the development of reproductive organs in ornamental asparagus, Asparagus virgatus. Sex. Plant Reprod. 17: 1-8.
92. Yun, P. Y., S. Y. Kim, T. Ochiai, T. Fukuda, T. Ito, A. Kanno, and T. Kameya. 2004b. AVAG2 is a putative D-class gene from an ornamental asparagus. Sex. Plant Reprod. 17: 107-116.