C-and D-class MADS-box genes from phalaenopsis equestris (orchidaceae) display functions in gynostemium and ovule development

Plant and Cell Physiology

Volumn 53, Issue 6, 2012, Pages 1053-1067

  Chen, You Yi ^a   Lee, Pei Fang ^b   Hsiao, Yu Yun ^a   Wu, Wan Lin ^a   Pan, Zhao Jun ^a   Lee, Yung I ^c   Liu, Ke Wei ^d,e   Chen, Li Jun ^d   Liu, Zhong Jian ^d,e,f   Tsai, Wen Chieh ^a  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b FOOYIN UNIVERSITY   (Taiwan)

^c NATIONAL MUSEUM OF NATURAL SCIENCE   (Taiwan)

^d National Orchid Conservation Center of China   (China)

^e TSINGHUA UNIVERSITY   (China)

^f SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

C cl ss MADS box gene; D class MADS box gene; Gynostemium; Orchid; Ovule; Phalaenopsis equestris

Indexed keywords

MADS DOMAIN PROTEIN; PLANT DNA; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; METABOLISM; MOLECULAR GENETICS; ORCHIDACEAE; OVULE; PHENOTYPE; PHYLOGENY; PLANT GENE; POLLINATION; PROTEIN ANALYSIS; SCANNING ELECTRON MICROSCOPY; TRANSGENIC PLANT; ULTRASTRUCTURE;

AMINO ACID SEQUENCE; DNA, PLANT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENETIC COMPLEMENTATION TEST; MADS DOMAIN PROTEINS; MICROSCOPY, ELECTRON, SCANNING; MOLECULAR SEQUENCE DATA; ORCHIDACEAE; OVULE; PHENOTYPE; PHYLOGENY; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; POLLINATION; PROTEIN INTERACTION MAPPING;

EID: 84862189456     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcs048     Document Type: Article

References (65)

1. Atwood, J.T. (1986) The size of Orchidaceae and the systematic distribution of epiphytic orchids. Selbyana 9: 171-186.
2. Bleecker, A.B. and Patterson, S.E. (1997) Last exit: senescence, abscission, and meristem arrest in Arabidopsis. Plant Cell 9: 1169-1179. (Pubitemid 28181064)
3. Boss, P.K., Vivier, M., Matsumoto, S., Dry, I.B. and Thomas, M.R. (2001) A cDNA from grapevine (Vitis vinifera L.), which shows homology to AGAMOUS and SHATTERPROOF, is not only expressed in flowers but also throughout berry development. Plant Mol. Biol. 45: 541-553. (Pubitemid 32515948)
4. Bowman, J.L., Smyth, D.R. and Meyerowitz, E.M. (1989) Genes directing flower development in Arabidopsis. Plant Cell 1: 37-52.
5. Bowman, J.L., Smyth, D.R. and Meyerowitz, E.M. (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112: 1-20.
6. Busi, M.V., Bustamante, C., D'Angelo, C., Hidalgo-Cuevas, M., Boggio, S.B., Valle, E.M. et al. (2003) MADS-box genes expressed during tomato seed and fruit development. Plant Mol. Biol. 52: 801-815. (Pubitemid 37065234)
7. Chang, Y.Y., Kao, N.H., Li, J.Y., Hsu, W.H., Liang, Y.L., Wu, J.W. et al. (2010) Characterization of the possible roles for B class MADS box genes in regulation of perianth formation in orchid. Plant Physiol. 152: 837-853.
8. Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
9. Colombo, L., Franken, J., Koetje, E., van Went, J., Dons, H.J.M., Angenent, G.C. et al. (1995) The petunia MADS box gene FBP11 determines ovule identity. Plant Cell 7: 1859-1868. (Pubitemid 3019804)
10. Cozzolino, S. and Widmer, A. (2005) Orchid diversity: an evolutionary consequence of deception? Trends Ecol. Evol. 20: 487-494. (Pubitemid 41207084)
11. Davies, B., Egea-Cortines, M., de Andrade Silva, E., Saedler, H. and Sommer, H. (1996) Multiple interactions amongst floral homeotic MADS box proteins. EMBO J. 15: 4330-4343. (Pubitemid 26278715)
12. Egea-Cortines, M., Saedler, H. and 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. (Pubitemid 29465586)
13. Favaro, R., Immink, R.G.H., Ferioli, V., Bernasconi, B., Byzova, M., Angenent, G.C. et al. (2002) Ovule-specific MADS-box proteins have conserved protein-protein interactions in monocot and dicot plants. Mol. Genet. Genomics 268: 152-159. (Pubitemid 35471766)
14. Favaro, R., Pinyopich, A., Battaglia, R., Kooiker, M., Borghi, L., Ditta, G. et al. (2003) MADS-box protein complexes control carpel and ovule development in Arabidopsis. Plant Cell 15: 2603-2611. (Pubitemid 37470661)
15. Ferrario, S., Immink, R.G.H., Shchennikova, A., Busscher-Lange, J. and Angenent, G.C. (2003) The MADS-box gene FBP2 is required for the SEPALLATA function in petunia. Plant Cell 15: 914-925. (Pubitemid 36453289)
16. Fu, C.H., Chen, Y.W., Hsiao, Y.Y., Pan, Z.J., Liu, Z.J., Huang, Y.M. et al. (2011) OrchidBase: a collection of sequences of transcriptome derived from orchids. Plant Cell Physiol. 52: 238-243.
17. Gietz, D., St. Jean, A., Wood, R.A. and Schiestl, R.H. (1992) Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 20: 1425.
18. Honma, T. and Goto, K. (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409: 525-529. (Pubitemid 32144359)
19. Hsiao, Y.Y., Chen, Y.W., Huang, S.C., Pan, Z.J., Fu, C.H., Chen, W.H. et al. (2011a) Gene discovery using next-generation pyrosequencing to develop ESTs for Phalaenopsis orchids. BMC Genomics 12: 360.
20. Hsiao, Y.Y., Pan, Z.J., Hsu, C.C., Yang, Y.P., Hsu, Y.C., Chuang, Y.C. et al. (2011b) Research on orchid biology and biotechnology. Plant Cell Physiol. 52: 1467-1486.
21. Hsu, H.F., Hsieh, W.P., Chen, M.K., Chang, Y.Y. and Yang, C.H. (2010) C/D class MADS box genes from two monocots, orchid (Oncidium Gower Ramsey) and lily (Lilium longiflorum), exhibit different effects on floral transition and formation in Arabidopsis thaliana. Plant Cell Physiol. 51: 1029-1045.
22. Kater, M.M., Colombo, L., Franken, J., Busscher, M., Masiero, S., Van Lookeren Campagne, M.M. et al. (1998) Multiple AGAMOUS homologs from cucumber and petunia differ in their ability to induce reproductive organ fate. Plant Cell 10: 171-182. (Pubitemid 28539889)
23. Kempin, S.A., Mandel, M.A. and Yanofsky, M.F. (1993) Conversion of perianth into reproductive organs by ectopic expression of the tobacco floral homeotic gene NAG1. Plant Physiol. 103: 1041-1046. (Pubitemid 2027440)
24. Kim, S.-Y., Yun, P.-Y., Fukuda, T., Ochiai, T., Yokoyama, J., Kameya, T. et al. (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)
25. Kitahara, K., Hibino, Y., Aida, R. and Matsumoto, S. (2004) Ectopic expression of the rose AGAMOUS-like MADS-box genes 'MASAKO C1 and D1' causes similar homeotic transformation of sepal and petal in Arabidopsis and sepal in Torenia. Plant Sci. 166: 1245-1252. (Pubitemid 38473386)
26. Kramer, E.M., Alejandra-Jaramillo, M.A. and Di Stilio, V.S. (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. (Pubitemid 38391758)
27. Liu, X., Zuo, K.-j., Xu, J.-t., Li, Y., Zhang, F., Yao, H.-y. et al. (2010) Functional analysis of GbAGL1, a D-lineage gene from cotton (Gossypium barbadense). J. Exp. Bot. 61: 1193-1203.
28. Lü, S., Du, X., Lu, W., Chong, K. and Meng, Z. (2007) Two AGAMOUSlike MADS-box genes from Taihangia rupestris (Rosaceae) reveal independent trajectories in the evolution of class C and class D floral homeotic functions. Evol. Dev. 9: 92-104. (Pubitemid 46072545)
29. Malcomber, S.T. and Kellogg, E.A. (2005) SEPELLATA gene diversification: brave new whorls. Trends Plant Sci. 10: 427-435. (Pubitemid 41725457)
30. Mizukami, Y. and Ma, H. (1992) Ectopic expression of the floral homeotic gene AGAMOUS in transgenic Arabidopsis plants alters floral organ identity. Cell 71: 119-131.
31. Mondragon-Palomino, M. and Theissen, G. (2008) MADS about the evolution of orchid flowers. Trends Plant Sci. 13: 51-59.
32. Mondragon-Palomino, M. and Theissen, G. (2011) Conserved differential expression of paralogous DEFICIENS-and GLOBOSAlike MADS-box genes in the flowers of Orchidaceae: refining the 'orchid code'. Plant J. 66: 1088-1019.
33. Münster, T., Pahnke, J., Di Rosa, A., Kim, J.T., Martin, W., Saedler, H. et al. (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. (Pubitemid 27136889)
34. Nitasaka, E. (2003) Insertion of an En/Spm-related transposable element into a floral homeotic gene DUPLICATED causes a double flower phenotype in the Japanese morning glory. Plant J. 36: 522-531. (Pubitemid 37457939)
35. Otero, J.T. and Flanagan, N.S. (2006) Orchid diversity-beyond deception. Trends Ecol. Evol. 21: 64-65.
36. Pan, Z.J., Cheng, C.C., Tsai, W.C., Chung, M.C., Chen, W.H., Hu, J.M. et al. (2011) The duplicated B-class MADS-box genes display dualistic characters in orchid floral organ identity and growth. Plant Cell Physiol. 52: 1515-1531.
37. Pnueli, L., Hareven, D., Rounsley, S.D., Yanofsky, M.F. and Lifschitz, E. (1994) Isolation of the tomato AGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants. Plant Cell 6: 163-173.
38. Rigola, D., Pe, M.E., Mizzi, L., Ciampolini, F. and Sari-Gorla, M. (2001) CaMADS1, an AGAMOUS homologue from hazelnut, produces floral homeotic conversion when expressed in Arabidopsis. Sex. Plant Repord. 13: 185-191. (Pubitemid 32200744)
39. Rutledge, R., Regan, S., Nicolas, O., Fobert, P., Côté, C., Bosnich, W. et al. (1998) Characterization of an AGAMOUS homologue from the conifer black spruce (Picea mariana) that produces floral homeotic conversions when expressed in Arabidopsis. Plant J. 15: 625-634.
40. Salemme, M., Sica, M., Gaudio, L. and 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.
41. Sambrook, J., Fritsch, E.F. and Maniatis, T. (2001) Molecular Cloning: A Laboratory Manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
42. Silvera, K., Santiago, L.S., Cushman, J.C. and Winter, K. (2009) Crassulacean acid metabolism and epiphytism linked to adaptive radiations in the Orchidaceae. Plant Physiol. 149: 1838-1847.
43. Skipper, M., Johansen, L.B., Pedersen, K.B., Frederiksen, S. and Johansen, B.B. (2006) Cloning and transcription analysis of an AGAMOUS-and SEEDSTICK ortholog in the orchid Dendrobium thyrsiflorum (Reichb. f.). Gene 366: 266-274. (Pubitemid 43227951)
44. Sleburth, L.E., Running, M.P. and Meyerowitz, E.M. (1995) Genetic separation of third and fourth whorl functions of AGAMOUS. Plant Cell 7: 1249-1258.
45. Song, I.-J., Nakamura, T., Fukuda, T., Yokoyama, J., Ito, T., Ichikawa, H. et al. (2006) Spatiotemporal expression of duplicate AGAMOUS orthologues during floral development in Phalaenopsis. Dev. Genes Evol. 216: 301-313. (Pubitemid 43733120)
46. Tandre, K., Svenson, M., Svensson, M.E. and Engström, P. (1998) Conservation of gene structure and activity in the regulation of reproductive organ development of conifers and angiosperms. Plant J. 15: 615-623.
47. Theissen, G., Becker, A., Di Rosa, A., Kanno, A., Kim, J.T., Münster, T. et al. (2000) A short history of MADS-box genes in plants. Plant Mol. Biol. 42: 115-49. (Pubitemid 30096114)
48. Theissen, G. and Saedler, H. (2001) Plant biology. Floral quartets. Nature 409: 469-71.
49. Thompson, J.D., Higgins, D.G. and Gibson, T.J. (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. (Pubitemid 24354800)
50. Tremblay, R.L., Ackerman, J.D., Zimmerman, J.K. and Calvo, R.N. (2005) Variation in sexual reproduction in orchids and its evolutionary consequence: a spasmodic journey to diversification. Biol. J. Linn. Soc. 84: 1-54. (Pubitemid 40181156)
51. Tsai, W.C., Hsiao, Y.Y., Lee, S.H., Tung, C.W., Wang, D.P., Wang, H.C. et al. (2006) Expression analysis of the ESTs derived from the flower buds of Phalaenopsis equestris. Plant Sci. 170: 426-432.
52. Tsai, W.C., Hsiao, Y.Y., Pan, Z.J., Hsu, C.C., Yang, Y.P., Chen, W.H. et al. (2008a) Molecular biology of orchid flower-with emphasis on Phalaenopsis. Adv. Bot. Res. 47: 99-145.
53. Tsai, W.C., Hsiao, Y.Y., Pan, Z.J., Kuoh, C.S., Chen, W.H. and Chen, H.H. (2008b) The role of ethylene in orchid ovule development. Plant Sci. 175: 98-105.
54. Tsai, W.C., Kuoh, C.S., Chuang, M.H., Chen, W.H. and Chen, H.H. (2004) Four DEF-like MADS box genes displayed distinct floral morphogenetic roles in Phalaenopsis orchid. Plant Cell Physiol. 45: 831-844.
55. Tsai, W.C., Lee, P.F., Chen, H.I., Hsiao, Y.Y., Wei, W.J., Pan, Z.J. et al. (2005) PeMADS6, a GLOBOSA/PISTILLATA-like gene in Phalaenopsis equestris involved in petaloid formation, and correlated with flower longevity and ovary development. Plant Cell Physiol. 46: 1125-1139.
56. Tsai, W.C., Pan, Z.J., Hsiao, Y.Y., Jeng, M.F., Wu, T.F., Chen, W.H. et al. (2008c) Interaction of B-class complex proteins involved in tepal development in Phalaenopsis orchid. Plant Cell Physiol. 49: 814-824.
57. Tzeng, T.Y., Chen, H.Y. and Yang, C.H. (2002) Ectopic expression of carpel-specific MADS box genes from lily and lisianthus causes similar homeotic conversion of sepal and petal in Arabidopsis. Plant Physiol. 130: 1827-1836.
58. Wang, S.Y., Lee, P.F., Lee, Y.I., Hsiao, Y.Y., Chen, Y.Y., Pan, Z.J. et al. (2011) Duplicated C-class MADS-box genes reveal distinct roles in gynostemium development in Cymbidium ensifolium (Orchidaceae). Plant Cell Physiol. 52: 563-577.
59. Weigel, D. and Meyerowitz, E.M. (1994) The ABCs of floral homeotic genes. Cell 78: 203-209. (Pubitemid 24241089)
60. Xu, Y., Teo, L.L., Zhou, J., Kumar, P.P. and Yu, H. (2006) Floral organ identity genes in the orchid Dendrobium crumenatum. Plant J. 46: 54-68. (Pubitemid 43773578)
61. Yamada, K., Saraike, T., Shitsukawa, N., Hirabayashi, C., Takumi, S. and Murai, K. (2009) Class D and Bsister MADS-box genes are associated with ectopic ovule formation in the pistil-like stamens of alloplasmic wheat (Triticum aestivum L.). Plant Mol. Biol. 71: 1-14.
62. Yamaguchi, T., Lee, D.Y., Miyao, A., Hirochika, H., An, G. and Hirano, H.Y. (2006) Functional diversification of the two C-class MADS box genes OSMADS3 and OSMADS58 in Oryza sativa. Plant Cell 18: 15-28. (Pubitemid 43951312)
63. Yu, H. and Goh, C.J. (2001) Molecular genetics of reproductive biology in orchids. Plant Physiol. 127: 1390-1393. (Pubitemid 34050004)
64. Yun, P.-Y., Kim, S.-Y., Ochiai, T., Fukuda, T., Ito, T., Kanno, A. et al. (2004) AVAG2 is a putative D-class gene from an ornamental asparagus. Sex. Plant Reprod. 17: 107-116. (Pubitemid 39385098)
65. Zahn, L.M., Leebens-Mack, J., DePamphilis, C.W., Ma, H. and Theissen, G. (2005) To B or Not to B a flower: the role of DEFICIENS and GLOBOSA orthologs in the evolution of the angiosperms. J. Hered. 96: 225-240. (Pubitemid 40434677)