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Isolation and Characterization of Three MADS-box Genes from Alpinia hainanensis (Zingiberaceae)

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Abstract

Three complementary DNA clones, AhMADS5, AhMADS6, and AhMADS8 were isolated from the young inflorescences of Alpinia hainanensis. Sequence comparisons and phylogenetic analyses indicated that AhMADS5 and AhMADS8 are highly homologous to AP3 and PI family, respectively, and AhMADS6 is an AG homologue. In situ hybridization analyses showed that AhMADS5 and AhMADS8 genes are expressed in the second and third whorls, whereas, the AhMADS6 signal is present in the third and fourth whorls. The expression patterns of AhMADS5, AhMADS8, and AhMADS6 genes are very similar to those of AP3-, PI-, and AG-like genes in other plant species, respectively. These results suggest that while AhMADS5 and AhMADS8 belong to the B-class MADS-box gene family, AhMADS6 belongs to a different category, the C-class MADS-box gene family. Present studies strongly support the hypothesis that the labellum of A. hainanensis originated from stamens.

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References

  • Adam H, Jouannic S, Morcillo F, Richaud F, Duval Y, Tregear JW (2006) MADS box genes in oil palm (Elaeis guineensis): patterns within the evolution of the SQUAMOSA, DEFICIENS, GLOBOSA, AGAMOUS and SEPALLATA subfamilies. J Mol Evol 62:15–31

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Angenent GC, Colombo L (1996) Molecular control of ovule development. Trends Plant Sci 1:228–232

    Google Scholar 

  • Angenent GC, Franken J, Busscher M et al (1995) A nove1 class of MADS box genes is involved in ovule development in petunia. Plant Cell 7:1569–1582

    Article  CAS  PubMed  Google Scholar 

  • Bowman JL, Smith DR, Meyerowitz EM (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112:1–20

    CAS  PubMed  Google Scholar 

  • Bradley D, Carpenter R, Sommer H, Hartley N, Coen E (1993) Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of Antirrhinum. Cell 72:85–95

    Article  CAS  PubMed  Google Scholar 

  • Burtt BL (1972) General introduction of papers on Zingiberaceae. Notes R Bot Gard Edinburgh 31:155–165

    Google Scholar 

  • Chung YY, Kim SR, Kang HG, Noh YS, Park MC, Finkel D et al (1995) Characterization of two rice MADS box genes homologous to GLOBOSA. Plant Sci 109:45–56

    Article  CAS  Google Scholar 

  • Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37

    Article  CAS  PubMed  Google Scholar 

  • Coen ES, Romero JM, Doyle S, Elliot R, Murphy G, Carpenter R (1990) Floricaula: a homeotic gene required for flower development in Antirrhinum majus. Cell 63:1311–1322

    Article  CAS  PubMed  Google Scholar 

  • Colombo L, Franken J, Koetje E et al (1995) The Petunia MADS Box Gene FBP11 Determines Ovule ldentity. Plant Cell 7:1859–1868

    Article  CAS  PubMed  Google Scholar 

  • Colombo L, Van Tunen AJ, Dons HJM, Angenent GC (1997) Molecular control of flower development in Petunia hybrida. Adv Bot Res 26:229–250

    Article  CAS  Google Scholar 

  • Dahlgren R, Rasmussen FN (1983) Monocotyledon evolution: characters and phylogenetic estimation. Evol Bio 16:255–395

    Google Scholar 

  • Fornara F, Parenicova L, Falasca G, Pelucchi N, Masiero S, Ciannamea S et al (2004) Functional characterization of OsMADS18, a member of the AP1/SQUA subfamily of MADS-box genes. Plant Physiol 135:2207–2219

    Article  CAS  PubMed  Google Scholar 

  • Gao XM, Xia YM, Li QJ (2006) Isolation of two putative homologues of PISTILLATA and AGAMOUS from Alpinia oblongifolia (Zingiberaceae) and characterization of their expression. Plant Sci 170:674–684

    Article  CAS  Google Scholar 

  • Goto K, Meyerowitz EM (1994) Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev 8:1548–1560

    Article  CAS  PubMed  Google Scholar 

  • Gregory PJ (1936) The floral morphology and cytology of Elettaria cardamomum Maton. J Linn Soc Bot 50:363–391

    Google Scholar 

  • Gustafson-Brown C, Savidge B, Yanofsky MF (1994) Regulation of the Arabidopsis floral homeotic gene APETALA1. Cell 76:131–143

    Article  CAS  PubMed  Google Scholar 

  • Hama E, Takumi S, Ogihara Y, Murai K (2004) Pistillody is caused by alterations to the class-B MADS-box gene expression pattern in alloplasmic wheats. Planta 218:712–720

    Article  CAS  PubMed  Google Scholar 

  • Honma T, Goto K (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409:525–529

    Article  CAS  PubMed  Google Scholar 

  • Hsu HF, Yang CH (2002) An Orchid (Oncidium Gower Ramsey) AP3-like MADS gene regulates floral formation and initiation. Plant Cell Physiol 43:1198–1209

    Article  CAS  PubMed  Google Scholar 

  • Huijser PW, Klein J, Lonnig WE, Meijer H, Saedler H, Sommer H (1992) Bracteomania, an inflorescence anomaly, is caused by the loss of function of the MADS-box gene squamosa in Antirrhinum majus. EMBO J 11:1239–1249

    CAS  PubMed  Google Scholar 

  • Jack T, Brockman LL, Meyerowitz EM (1992) The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell 68:683–697

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Jofuku KD, den Boer BGW, Van Montagu M, Okamuro JK (1994) Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6:1211–1225

    Article  CAS  PubMed  Google Scholar 

  • Kang HG, Noh YS, Chung YY, Costa MA, An K, An G (1995) Phenotypic alterations of petal and sepal by ectopic expression of a rice MADS box gene in tobacco. Plant Mol Biol 29:1–10

    Article  CAS  PubMed  Google Scholar 

  • Kang HG, Jeon JS, Lee S, An G (1998) Identification of class B and class C floral organ identity genes from rice. Plant Mol Biol 38:1021–1029

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kempin SA, Mandel MA, Yanofsky MF (1993) Conversion of perianth into reproductive organs by ectopic expression of the tobacco floral homeotic gene NAG1. Plant Physiol 103:1041–1046

    Article  CAS  PubMed  Google Scholar 

  • Kim SY, Yun PY, Fukuda 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

    Article  CAS  Google Scholar 

  • Kirchoff BK (1997) Inflorescence and flower development in the Hedychieae (Zingiberaceae): Hedychium. Can J Bot 75:518–594

    Article  Google Scholar 

  • Kirchoff BK (1998) Inflorescence and flower development in the Hedychieae (Zingiberaceae): Scaphochlamys kunstleri (Barker) Holttum. Int J Plant Sci 159:261–273

    Article  Google Scholar 

  • Kress WJ, Prince LM, Williams KJ (2002) The phylogeny and a new classification of gingers (Zingiberaceae): evidence from molecular data. Am J Bot 89:1682–1696

    Article  CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Kyozuka J, Kobayashi T, Morita M, Shimamoto K (2000) Spatially and temporally regulated expression of rice MADS box genes with similarity to Arabidopsis calss A, B and C genes. Plant Cell Physiol 41:710–718

    CAS  PubMed  Google Scholar 

  • Liao JP, Zou P, Tang YJ, Song JJ, Xie ZY, Wu QG et al (2006) Floral vasculature in Alpinia hainanensis in relation to the nature of the labellum in gingers. Nord J Bot 23:545–553

    Article  Google Scholar 

  • Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360:273–277

    Article  CAS  PubMed  Google Scholar 

  • Meguro A, Takumi S, Ogihara Y, Murai K (2003) WAG, a wheat AGAMOUS homolog, is associated with development of pistillike stamens in alloplasmic wheats. Sex Plant Reprod 15:221–230

    CAS  Google Scholar 

  • Mena M, Mandel MA, Lerner DR, Yanofsky MF, Schmidt RJ (1995) A characterization of the MADS-box gene family in maize. Plant J 8:845–854

    CAS  PubMed  Google Scholar 

  • Mena M, Ambrose BA, Meeley RB, Briggs SP, Yanofsky MF, Schmidt RJ (1996) Diversification of C-function activity in maize flower development. Science 274:1537–1540

    Article  CAS  PubMed  Google Scholar 

  • Mondragon-Palomino M, Theißen G (2008) MADS about the evolution of orchid flowers. Trends Plant Sci 13:51–59

    CAS  PubMed  Google Scholar 

  • Moon YH, Jung JY, Kang HG, An G (1999) Identification of a rice APETALA3 homologue by yeast two-hybrid. Plant Mol Biol 40:167–177

    Article  CAS  PubMed  Google Scholar 

  • Munster T, Wingen LU, Faigl W, Werth S, Saedler H, Theissen G (2001) Characterization of three GLOBOSA-like MADS-box genes from maize: evidence for ancient paralogy in one class of floral homeotic B-function genes of grasses. Gene 262:1–13

    Article  CAS  PubMed  Google Scholar 

  • Nakada M, Komatsu M, Ochiai T et al (2006) Isolation of MaDEF from Muscari armeniacum and analysis of its expression using laser microdissection. Plant Sci 170:143–150

    Article  CAS  Google Scholar 

  • Nakamura T, Fukuda T, Nakano M et al (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

    Article  CAS  PubMed  Google Scholar 

  • Park JH, 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

    Article  CAS  PubMed  Google Scholar 

  • Park JH, 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Pnueli L, Hareven D, Rounsley SD, Yanofsky MF, Lifschitz E (1994) Isolation of the tomato AGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants. Plant Cell 6:163–173

    Article  CAS  PubMed  Google Scholar 

  • Raghavan TS, Venkatasubban KR (1941) A contribution to the morphology and cytology of Alpinia calcarata Rosc. with special reference to the theory on Zingiberous flowering. Proceedings of the Indian Academy of Sciences B13:325

    Google Scholar 

  • Rao PJM (1963) The epigynous glands of Zingiberaceae. New Phytol 62:342–349

    Article  Google Scholar 

  • Schmidt RJ, Veit B, Mandel MA, Mena M, Hake S, Yanofsky MF (1993) Identification and molecular characterization of ZAG1, the maize homolog of the Arabidopsis floral homeotic gene AGAMOUA. Plant Cell 5:729–737

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Sommer H, Beltran JP, Huijser P et al (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

    CAS  PubMed  Google Scholar 

  • Song JJ, Zou P, Liao JP, Tang YJ, Chen ZY (2007) Floral ontogeny in Alpinia oxyphylla Miq. (Zingiberaceae) and its systematic significance. Gard Bull Singapore 59:221–230

    Google Scholar 

  • Theissen G (2001) Development of floral organ identity: stories from the MADS house. Curr Opin Plant Biol 4:75–85

    Article  CAS  PubMed  Google Scholar 

  • Tomlinson PB (1982) Phylogeny of the Scitamineae-morphological and anatomical considerations. Evolution 16:192–213

    Article  Google Scholar 

  • Trobner W, Ramirez L, Motte P, Hue I, Huijser P, Lonnig WE et al (1992) GLOBOSA: a homeotic gene which interacts with DEFICIENS in the control of Antirrhinum floral organogenesis. EMBO J 11:4693–4704

    CAS  PubMed  Google Scholar 

  • Tsai WC, Kuoh CS, Chuang MH et al (2004) Four DEF-like MADS box genes displayed distinct floral morphogenetic roles in Phalaenopsis orchid. Plant Cell Physiol 45:831–844

    Article  CAS  PubMed  Google Scholar 

  • van Tunen AJ, Eikelboom W, Angenent GC (1993) Floral organogenesis in Tulipa. Flow Newsl 16:33–37

    Google Scholar 

  • Weigel D, Meyerowitz EM (1994) The ABCs of floral homeotic genes. Cell 78:203–209

    Article  CAS  PubMed  Google Scholar 

  • Winter KU, Weiser C, Kaufmann K et al (2002) Evolution of class B floral homeotic proteins: obligate heterodimerization originated from homodimerization. Mol Biol Evol 19:587–596

    CAS  PubMed  Google Scholar 

  • Wu TL, Kress WH (2000) Zingiberaceae. In: ZY Wu, PH Raven (ed.). Flora of China, Science, Beijing & Missouri Botanical Garden, St. Louis 24:322–377

    Google Scholar 

  • Xu YF, Teo LL, Zhou J, Kumar PP, Yu H (2006) Floral organ identity genes in the orchid Dendrobium crumenatum. Plant J 46:54–68

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We are grateful to Dr. Zhong Zhao and Dr. Zhicheng Dong of Shanghai Institute of Plant Physiology and Ecology for providing excellent technical assistance. We also thank Ms. Yongmei Xia of Xishuangbanna Tropical Botanical Garden for her assistance in this research. We thank Dr. Pu Zou, Mr. Yuhua Yu, and Mr. Yushi Ye of South China Botanical Garden for help in plant tissue collection and photo taking. Furthermore, we like to thank Professor Qigen Wu and Beijian Mei for their help on the revision of this manuscript.

This research was supported by grants for systematic and evolutionary biology, from Chinese Academy of Sciences, National Natural Science Foundation of China (39870087, 30370099, 40332021), National Key Program for Basic Research of China (2001CCA00300) and China postdoctoral Science Foundation (20090450891).

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Correspondence to Jing-Ping Liao.

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Song, JJ., Ma, W., Tang, YJ. et al. Isolation and Characterization of Three MADS-box Genes from Alpinia hainanensis (Zingiberaceae). Plant Mol Biol Rep 28, 264–276 (2010). https://doi.org/10.1007/s11105-009-0147-7

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