Abstract
The floral homeotic C function gene AGAMOUS (AG) plays crucial roles in Arabidopsis development by specifying stamen and carpel identity, repressing A-class genes, as well as regulating floral meristem determination. Although the function of AG homologs from other core eudicots appears highly conserved, the role of AG orthologs in the design of floral architecture in basal angiosperm remains unknown. We isolated and identified an AG ortholog from Magnolia wufengensis, a woody basal angiosperm belonging to the Magnoliaceae. Sequence and phylogenetic analyses revealed that it is a clade member of the euAG lineage, and hence, the gene is referred to as MAwuAG (M. wu fengensis AGAMOUS). Moreover, two highly conserved motifs specific to C proteins, AG motifs I and II, are found in the C-terminal regions of the MAwuAG protein, but the N-terminal extensions that usually appear in euAG lineage members from eudicots were not found in MAwuAG. The cDNA has the first in-frame ATG immediately preceding the MADS domain. A semi-quantitative PCR analysis showed that the expression of MAwuAG was restricted to reproductive organs of stamens and carpels. The transgenic Arabidopsis containing 35S::MAwuAG displayed extremely early flowering, bigger stamens and carpels, and homeotic conversion of petals into staminoid organs, but ectopic expression of MAwuAG in the first whorls failed to convert the sepals into carpeloid structures that are usually observed in the overexpression transgenic Arabidopsis of AG orthologs from other core eudicots. In addition, the phenotype of the transgenic 35S::MAwuAG Arabidopsis revealed that the abscission of the outer three floral whorls (sepals, petals, and stamens) was inhibited.
Similar content being viewed by others
References
Bowman JL, Smyth DR, Meyerowitz EM (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112:1–20
Chanderbalia AS, Albertc VA, Leebens-Mackd J, Altmane NS, Soltis DE, Soltis PS (2009) Transcriptional signatures of ancient floral developmental genetics in avocado (Persea americana; Lauraceae). Proc Natl Acad Sci USA 106:8929–8934
Chang SJ, Puryear J, Cainey J (1993) A simple and efficient method for RNA isolating from pine trees. Plant Mol Biol Rep 11:113–116
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant J16:735–743
Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37
Davies B, Cartolano M, Schwarz-Sommer Z (2006) Flower development: the Antirrhinum perspective. Adv Bot Res 44:279–320
De Oliveira RR, Chalfun-Junior A, Paiva LV, Andrade AC (2010) In silico and quantitative analyses of MADS-box genes in Coffea arabica. Plant Mol Biol Rep 28:460–472
Dellaporta SL, Wood J, Hicks JB (1983) A plant minipreparation: version II. Plant Mol Biol Rep 1:19–20
Du N, Pijut PM (2010) Isolation and characterization of an AGAMOUS homolog from Fraxinus pennsylvanica. Plant Mol Biol Rep 28:344–351
Endress PK, James A, Doyle JA (2009) Reconstructing the ancestral angiosperm flower and its initial specializations. Am J Bot 96(1):22–66
Hou J, Gao Z, Zhang Z, Chen S, Ando T, Zhang J, Wang X (2011) Isolation and characterization of an AGAMOUS homologue PmAG from the Japanese apricot (Prunus mume Sieb. et Zucc.). Plant Mol Biol Rep 29:473–480
Hsu HF, Hsieh WP, Chen MK, Chang YY, Yang CH (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(6):1029–1045
Irish VF (2010) The flowering of Arabidopsis flower development. The Plant J 61:1014–1028
Kim S, Koh J, Yoo MJ, Kong H, Hu Y, Ma H, Soltis PS, Soltis DE (2005) Expression of floral MADS-box genes in basal angiosperms: implications for the evolution of floral regulators. The Plant J 43:724–744
Kitahara K, Hibino Y, Aida R, Matsumoto S (2004) Ectopic expression of the rose AGAMOUS-like MADS-box genes ‘MASAKO C1 and D1’ cause similar homeotic transformation of sepal and petal in Arabidopsis and sepal in Torenia. Plant Sci 166:1245–1252
Kramer EM, Jaramlllo MA, Di Stillo VS (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
Krizek BA, Fletcher JC (2005) Molecular mechanisms of flower development: an armchair guide. Nat Rev Genet 6:688–698
Liu X, Anderson JM, Pijut PM (2010) Cloning and characterization of Prunus serotina AGAMOUS, a putative flower homeotic gene. Plant Mol Biol Rep 28:193–203
Lv S, Du X, Lu W, Chong K, Meng Z (2007) Two AGAMOUS-like 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
Ma LY, Wang LR, He SC, Liu X, Wang XQ (2006a) A new species of Magnolia (Magnoliaceae) from Hubei, China. Bull Bot Res (China) 26(1):4–7
Ma LY, Wang LR, He SC, Liu X, Wang XQ (2006b) A new variety of Magnolia (Magnoliaceae) from Hubei, China. Bull Bot Res (China) 26(5):516–519
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
Mizukami Y, Ma H (1992) Ectopic expression of the floral homeotic gene AGAMOUS in transgenic Arabidopsis plants alters floral organ identity. Cell 71:119–131
Murashige T, Skoog F (1962) A revised media for rapid growth and bioassay with tobacco cultures. Physiol Plant 15:473–497
Pan IL, McQuinn R, Giovannoni JJ, Irish VF (2010) Functional diversification of AGAMOUS lineage genes in regulating tomato flower and fruit development. J Exp Bot 61:1795–1806
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
Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767
Song J, Ma W, Tang Y, Chen Z, Liao J (2010) Isolation and characterization of three MADS-box genes from Alpinia hainanensis (Zingiberaceae). Plant Mol Biol Rep 28:264–276
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Bio Evo 24(8):1596–1599
Teeri TH, Kotilainen M, Uimari A, Ruokolainen S, Ng YP, Malm U, Pollanen E, Broholm S, Laitinen R, Elomaa P, Albert VA (2006) Floral developmental genetics of Gerbera (Asteraceae). Adv Bot Res 44:323–351
Theissen G (2001) Development of floral organ identity: stories from the MADS house. Curr Opin Plant Biol 4:75–85
Weigel D, Meyerowitz EM (1994) The ABCs of floral homeotic genes. Cell 78:203–209
Whipple CJ, Schmidt RJ (2006) Genetics of grass flower development. Adv Bot Res 44:385–424
Wu X, Shi J, Xi M, Luo Z, Hu X (2010) A B functional gene cloned from lily encodes an ortholog of Arabidopsis PISTILLATA (PI). Plant Mol Biol Rep 28:684–691
Yamaguchi T, Hirano HY (2006) Function and diversification of MADS-box genes in rice. TSW Dev Embryol 1:99–108
Yang Y, Singer SD, Liu Z (2011) Petunia AGAMOUS enhancer-derived chimeric promoters specify a carpel-, stamen-, and petal-specific expression pattern sufficient for engineering male and female sterility in tobacco. Plant Mol Biol Rep 29:162–170
Yellina AL, Orashakova S, Lange S, Erdmann R, Leebens-Mack J, Becker A (2010) Floral homeotic C function genes repress specific B function genes in the carpel whorl of the basal eudicot California poppy (Eschscholzia californica). EvoDevo 1:13
Zahn LM, Feng BM, Ma H (2006) Beyond the ABC-model: regulation of floral homeotic genes. Adv Bot Res 44:164–196
Zhang XM, Wang Y, Lv XM, Li H, Sun P, Lu H, Li FL (2009) NtCP56, a new cysteine protease in Nicotiana tabacum L., involved in pollen grain development. J Exp Bot 60:1569–1577
Acknowledgments
This work was supported by the National Nature Science Foundation of China (grant no. 31170625), the Special Foundation of the China Postdoctoral Science Foundation (grant no. 200801048), and the China Postdoctoral Science Foundation (grant no. 20070410038).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wu, W., Chen, F., Jing, D. et al. Isolation and Characterization of an AGAMOUS-Like Gene from Magnolia wufengensis (Magnoliaceae). Plant Mol Biol Rep 30, 690–698 (2012). https://doi.org/10.1007/s11105-011-0385-3
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11105-011-0385-3