DOI QR코드

DOI QR Code

Cloning and Characterization of a PI-like MADS-Box Gene in Phalaenopsis Orchid

  • Guo, Bin (Institute of Genetics, State Key Laboratory of Genetic Engineering, Research Center of Gene Diversity and Designed Agriculture, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, School of Life Science, Fudan University) ;
  • Hexige, Saiyin (Institute of Genetics, State Key Laboratory of Genetic Engineering, Research Center of Gene Diversity and Designed Agriculture, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, School of Life Science, Fudan University) ;
  • Zhang, Tian (Institute of Genetics, State Key Laboratory of Genetic Engineering, Research Center of Gene Diversity and Designed Agriculture, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, School of Life Science, Fudan University) ;
  • Pittman, Jon K. (Life Sciences, University of Manchester) ;
  • Chen, Donghong (Institute of Genetics, State Key Laboratory of Genetic Engineering, Research Center of Gene Diversity and Designed Agriculture, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, School of Life Science, Fudan University) ;
  • Ming, Feng (Institute of Genetics, State Key Laboratory of Genetic Engineering, Research Center of Gene Diversity and Designed Agriculture, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, School of Life Science, Fudan University)
  • Published : 2007.11.30

Abstract

The highly evolved flowers of orchids have colorful sepals and fused columns that offer an opportunity to discover new genes involved in floral development in monocotyledon species. In this investigation, we cloned and characterized the homologous PISTALLATA-like (PI-like) gene PhPI15 ($\underline{Ph}alaenopsis$ $\underline{PI}$ STILLATA # $\underline{15}$), from the Phalaenopsis hybrid cultivar. The protein sequence encoded by PhPI15 contains a typical PI-motif. Its sequence also formed a subclade with other monocot PI-type genes in phylogenetic analysis. Southern analysis showed that PhPI15 was present in the Phalaenopsis orchid genome as a single copy. Furthermore, it was expressed in all the whorls of the Phalaenopsis flower, while no expression was detected in vegetative organs. The flowers of transgenic tobacco plants ectopically expressing PhPI15 showed male-sterile phenotypes. Thus, as a Class-B MADS-box gene, PhPI15 specifies floral organ identity in orchids.

Keywords

References

  1. Ambrose, B. A., Lerner, D. R., Ciceri, P. and Padilla C. M., Yanofsky, M. F. and Schmidt, R. J. (2000) Molecular and genetic analyses of the silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Mol. Cells 5, 569-579. https://doi.org/10.1016/S1097-2765(00)80450-5
  2. Bowman, J. L., Smyth, D. R. and Meyerowitz, E. M. (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112, 1-20.
  3. Caliskan, M., Ozcan, B., Turan, C. and Cuming, A. C. (2004) Localization of germin genes and their products in developing wheat coleoptiles. J. Biochem. Mol. Biol. 37, 339-342. https://doi.org/10.5483/BMBRep.2004.37.3.339
  4. Coen, E. S. and Meyerowitz, E. M. (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353, 31-37. https://doi.org/10.1038/353031a0
  5. Davies, B. and Schwarz-Sommer, Z. (1994) Control of floral organ identity by homeotic MADS-box transcription factors. Results Probl. Cell Differ. 20, 235-258. https://doi.org/10.1007/978-3-540-48037-2_11
  6. Davies, B., Di Rosa, A., Eneva, T., Saedler, H. and Sommer, H. (1996) Alteration of tobacco floral organ identity by expression of combinations of Antirrhinum MADS-box genes. Plant J. 10, 663-677. https://doi.org/10.1046/j.1365-313X.1996.10040663.x
  7. Goto, K. and Meyerowitz, E. M. (1994) Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev. 8, 1548-1560. https://doi.org/10.1101/gad.8.13.1548
  8. Hama, E., Takumi, S., Ogihara, Y. and Murai, K. (2004) Pistillody is caused by alterations to the class-B MADS-box gene expression pattern in alloplasmic wheats. Planta 218, 712-720. https://doi.org/10.1007/s00425-003-1157-6
  9. Jack, T., Brockman, L. L. and Meyerowitz, E. M. (1992) The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell 68, 683-697. https://doi.org/10.1016/0092-8674(92)90144-2
  10. Jackson, D. P. (1991) In situ hybridization in plants; in molecular plant pathology: a practical approach, Bowles, D. J., Gurr, S. J. and McPhereson, M. (eds.), pp. 163-174, Oxford University Press, Oxford, UK.
  11. Jia, H., Chen, R., Cong, B., Cao, K., Sun, C. and Luo D. (2000) Characterization and transcriptional profiles of two rice MADSbox genes. Plant Sci. 155, 115-122. https://doi.org/10.1016/S0168-9452(00)00191-6
  12. Kang, H. G., Jang, S., Chung, J. E., Cho, Y. G. and An, G. (1997) Characterization of two rice MADS box genes that control flowering time. Mol. Cells 7, 559-566.
  13. Kang, H. G., Jeon, J. S., Lee, S. and An, G. (1998) Identification of class B and class C floral organ identity genes from rice plants. Plant Mol. Biol. 38, 1021-1029. https://doi.org/10.1023/A:1006051911291
  14. Kanno, A., Saeki, H., Kameya, T., Saedler, H. and 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. https://doi.org/10.1023/A:1025070827979
  15. Kim, S., Yoo, M. J., Albert, V. A., Farris, J. S., Soltis, P. S. and Soltis, D. E. (2004) Phylogeny and diversification of B-function MADSbox genes in angiosperms: evolutionary and functional implications of a 260-million-year-old duplication. Am. J. Bot. 91, 2102-2118. https://doi.org/10.3732/ajb.91.12.2102
  16. Kramer, E. M., Dorit, R. L. and Irish, V. F. (1998) Molecular evolution of genes controlling petal and stamen development: duplication and divergence within the APETALA3 and PISTILLATA MADS-box gene lineages. Gene 149, 765-783.
  17. Kramer, E. M. and Irish, V. F. (1999) Evolution of genetic mechanisms controlling petal development. Nature 399, 144-148.
  18. Kumar, S., Tamura, K. and Nei, M. (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform. 5, 150-163. https://doi.org/10.1093/bib/5.2.150
  19. Kyozuka, J., Kobayashi, T., Morita, M. and Shimamoto, K. (2000) Spatially and temporally regulated expression of rice MADS box genes with similarity to Arabidopsis class A, B and C genes. Plant Cell Physiol. 41, 710-718. https://doi.org/10.1093/pcp/41.6.710
  20. Lu, Z. X., Wu, M., Loh, C. S., Yeong, C. Y. and Goh, C. J. (1993) Nucleotide sequence of a flower-specific MADS box cDNA clone from orchid. Plant Mol. Biol. 23, 901-904. https://doi.org/10.1007/BF00021545
  21. Murray, M. G. and Thompson, W. F. (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res. 8, 4321-4325. https://doi.org/10.1093/nar/8.19.4321
  22. Prakash, A. P. and Kumar, P. P. (2002) PkMADS1 is a novel MADS box gene regulating adventitious shoot induction and vegetative shoot development in Paulownia kawakamii. Plant J. 29, 141-151. https://doi.org/10.1046/j.0960-7412.2001.01206.x
  23. Riechmann, J. L. And Meyerowitz, E. M. (1997) MADS domain proteins in plant development. Biol. Chem. 378, 1079-1101. https://doi.org/10.1515/bchm.1997.378.10.1079
  24. Rounsley, S. D., Ditta, G. S. and Yanofsky, M. F. (1995) Diverse roles for MADS box genes in Arabidopsis development. Plant Cell 7, 1259-1269. https://doi.org/10.1105/tpc.7.8.1259
  25. Sommer, H., Beltran, J. P., Huijser, P., Pape, H., Lonnig, W. E., Saedle, H. and 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.
  26. Song, I. J., Nakamura, T., Fukuda, T., Yokoyama, J., Ito, T., Ichikawa, H., Honiara, Y., Kameya, T. and Kanno, A. (2006) Spatiotemporal expression of duplicate AGAMOUS orthologues during floral development in Phalaenopsis. Dev. Genes Evol. 4, 1-13.
  27. Theissen, G., Becker, A., Di Rosa, A., Kanno, A., Kim, J. T., Munster, T., Winter, K. U. and Saedler, H. (2000) A short history of MADS-box genes in plants. Plant Mol. Biol. 42, 115-149. https://doi.org/10.1023/A:1006332105728
  28. 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. https://doi.org/10.1093/pcp/pch095
  29. Tsai, W. C., Lee, P. F., Chen, H. I., Hsiao, Y. Y., Wei, W. J., Pan, Z. J., Chuang, M. H., Kuoh, C. S., Chen, W. H. and Chen, H. H. (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. https://doi.org/10.1093/pcp/pci125
  30. Weigel, D. and Meyerowitz, E. M. (1994) The ABCs of floral homeotic genes. Cell 78, 203-209. https://doi.org/10.1016/0092-8674(94)90291-7
  31. 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. https://doi.org/10.1111/j.1365-313X.2006.02669.x
  32. Yang, Y., Fanning, L. and Jack, T. (2003) The K domain mediates heterodimerization of the Arabidopsis floral organ identity proteins, APETALA3 and PISTILLATA. Plant J. 33, 47-59. https://doi.org/10.1046/j.0960-7412.2003.01473.x
  33. Yu, H. and Goh, C. J. (2000) Identification and characterization of three orchid MADS-box genes of the AP1/AGL9 subfamily during floral transition. Plant Physiol. 123, 1325-1336. https://doi.org/10.1104/pp.123.4.1325

Cited by

  1. Molecular mechanisms of floral mimicry in orchids vol.13, pp.5, 2008, https://doi.org/10.1016/j.tplants.2008.02.008
  2. Cloning and Expression Analysis of a PISTILLATA Homologous Gene from Pineapple (Ananas comosus L. Merr) vol.13, pp.12, 2012, https://doi.org/10.3390/ijms13011039
  3. The OrcPI locus: Genomic organization, expression pattern, and noncoding regions variability in Orchis italica (Orchidaceae) and related species vol.434, pp.1-2, 2009, https://doi.org/10.1016/j.gene.2008.12.015
  4. Construction of a Full-Length cDNA Library of Gossypium hirsutum L. and Identification of Two MADS-Box Genes vol.10, pp.1, 2011, https://doi.org/10.1016/S1671-2927(11)60304-0
  5. Markers for ornamental traits in Phalaenopsis orchids: population structure, linkage disequilibrium and association mapping vol.30, pp.1, 2012, https://doi.org/10.1007/s11032-011-9620-8
  6. Flowering Newsletter bibliography for 2007 vol.64, pp.18, 2013, https://doi.org/10.1093/jxb/ern109
  7. Organ homologies in orchid flowers re-interpreted using the Musk Orchid as a model vol.1, 2013, https://doi.org/10.7717/peerj.26
  8. Establishment of an Agrobacterium-mediated genetic transformation procedure for the experimental model orchid Erycina pusilla vol.120, pp.1, 2015, https://doi.org/10.1007/s11240-014-0596-z
  9. Functional analysis reveals the possible role of the C-terminal sequences and PI motif in the function of lily (Lilium longiflorum) PISTILLATA (PI) orthologues vol.63, pp.2, 2012, https://doi.org/10.1093/jxb/err323
  10. Overexpression of Lilium formosanum MADS-box (LFMADS) Causing Floral Defects While Promoting Flowering in Arabidopsis thaliana, Whereas Only Affecting Floral Transition Time in Nicotiana tabacum vol.19, pp.8, 2018, https://doi.org/10.3390/ijms19082217