Abstract
The trioecious papaya is a unique system to study the roles of flower organ identity genes of the ABC model in a multi-sex-type plant species. We have cloned two Agamous ( AG) subfamily genes, CpPLE and CpSTK, and one AP1 subfamily gene, CpFUL—a FRUITFUL homolog. CpPLE, CpSTK, and CpFUL are grouped into the PLE, D, and euFUL sublineages, respectively. Both CpPLE and CpSTK were expressed only in flowers, not in roots and leaves based on Northern and RT-PCR analyses. Specifically, CpPLE was detected only in the stamens and carpels of flowers of all three sex types, from a very early stage of flower development through full maturity. CpSTK expression was detected in female and hermaphrodite flowers, but completely absent in male flowers. This is the only gene found so far that shows sex-type-specific expression in papaya but this is likely to be an indirect effect of sex determination rather than a causative agent. CpFUL was expressed in leaves and all parts of the flowers except stamens. The genomic structures and expression patterns of CpPLE and CpSTK are consistent with their potential functions as C and D class genes, respectively. CpPLE belongs to the PLE lineage and is therefore an ortholog of SHP1/2 rather than AG. However, CpPLE is likely to perform ancestral functions in carpel and stamen identity, whereas SHP1/2 are involved in fruit development. These findings demonstrate that the evolution of gene function within the AG and PLE lineages has been quite dynamic, even over relatively short phylogenetic distances.
Similar content being viewed by others
References
Alvarez-Buylla ER, Pelaz S, Liljegren SJ, Gold SE, Burgeff C et al. (2000) An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proc Natl Acad Sci U S A 97:5328–5333
Becker A, Theißen G (2003) The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol Phy Evol 29:464–489
Bowers JE, Chapman BA, Rong J, Paterson AH (2003) Unraveling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422:433–438
Bowman JL, Smyth DR, Meyerowitz EM (1989) Genes directing flower development in Arabidopsis. Plant Cell 1:37–52
Causier B, Castillo R, Zhou JL, Ingram R, Xue YB, Schwarz-Sommer Z et al (2005) Evolution in action: following function in duplicated floral homeotic genes. Curr Biol 15:1508–1512
Chittenden LM, Schertz KF, Lin YR, Wing RA, Paterson AH (1994) A detailed RFLP map of Sorghum bicolor x S. propinquum, suitable for high-density mapping, suggests ancestral duplication of Sorghum chromosomes or chromosomal segments. Theor Appl Genet 87:925–933
Coen ES, Meyerowitz EM (1991) War of the whorls: genetic interactions controlling flower development. Nature 353:31–37
Crepet WL, Nixon KC, Gandolfo MA (2004) Fossil evidence and phylogeny: the age of major angiosperm clades based on mesofossil and macrofossil evidence from Cretaceous deposits. Am J Bot 91:1666–1682
Davies B, Motte P, Keck E, Saedler H, Sommer H, Schwarz-Sommer Z (1999) PLENA and FARINELLI: redundancy and regulatory interactions between two Antirrhinum MADS-box factors controlling flower development. EMBO J 18:4023–4034
Decraene LPR, Smets EF (1999) The floral development and anatomy of Carica papaya (Caricaceae). Can J Bot 77:582–598
Deyholos MK, Sieburth LE (2000) Separable whorl-specific expression and negative regulation by enhancer elements within the AGAMOUS second intron. Plant Cell 12:1799–1810
Di Stilio VS, Kramer EM, Baum DA (2004) Floral MADS box genes and the evolution of homeotic gender dimorphism in meadow rues (Thalictrum, Ranunculaceae). Plant J 41:755–766
Drews GN, Bowman JL, Meyerowitz EM (1991) Negative regulation of the Arabidopsis homeotic gene AGAMOUS by APETALA2 product. Cell 65:991–1002
Favaro R, Pinyopich A, Battaglia R, Kooiker M, Borghi L et al. (2003) MADS-box protein complexes control carpel and ovule development in Arabidopsis. Plant Cell 15:2603–2611
Gu Q, Ferrándiz C, Yanofsky MF, Martienssen R (1998) The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development 125:1509–1517
Hall JC, Sytsma KJ, Iltis HH (2002) Phylogeny of Capparaceae and Brassicaceae based on chloroplast sequence data. Am J Bot 89:1826–1842
Hall TC, Buchbinder BU, Pyne JW, Sun SM, Bliss FA (1978) Messenger RNA for G1 protein of French bean seeds: cell-free translation and product characterization. Proc Natl Acad Sci U S A 75:3196–3200
Hong RL, Hamaguchi L, Busch MA, Weigel D (2003) Regulatory elements of the floral homeotic gene AGAMOUS identified by phylogenetic footprinting and shadowing. Plant Cell 15:1296–1309
Kramer EM, Jaramillo MA, Di Stilio 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
Lenhard M, Bohnert A, Jürgens G, Laux T (2001) Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS. Cell 105:805–814
Lijegren SJ, Ditta GS, Eshed Y, Savidge B, Bowman JL et al (2000) SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404:766–770
Liu Z, Meyerowitz EM (1995) LEUNIG regulates AGAMOUS expression in Arabidopsis flowers. Development 121:975–991
Litt A, Irish VF (2003) Duplication and diversification of the APETALA1/FRUITFULL floral homeotic gene lineage: implications for the evolution of floral development. Genetics 165:821–833
Litt A (2007) An evaluation of A-function: evidence from the APETALA1 and APETALA2 gene lineages. Int J Plant Sci 168:73–91
Lohmann JU, Hong RL, Hobe M, Busch MA, Parcy F et al (2001) A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105:793–803
Ma H, Yanofsky MF, Meyerowitz EM (1991) AGL1-AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Genes Dev 5:484–495
Mayer KFX, Schoof H, Haecher A, Lenhard M, Jürgens G et al (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95:805–815
Ming R, Moore PH, Zee F, Abbey CA, Ma H et al (2001) Construction and characterization of a papaya BAC library as a foundation for molecular dissection of a tree-fruit genome. Theor Appl Genet 102:892–899
Moore RC, Grant SR, Purugganan MD (2005) Molecular population genetics of redundant floral-regulatory genes in Arabidopsis thaliana. Mol Biol Evol 22:91–103
Pinyopich A, Ditta GS, Savidge B, Lijegren SJ, Baumann E et al (2003) Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 424:85–88
Pfent C, Pobursky KJ, Sather DN, Golenberg EM (2005) Characterization of SpAPETALA3 and SpPISTILLATA, B class floral identity genes in Spinacia oleracea, and their relationship to sexual dimorphism. Dev Gen Evol 215:132–142
Renner SS, Ricklefs RE (1995) Dioecy and its correlates in the flowering plants. Am J Bot 82:596–606
Riechmann JL, Meyerowitz EM (1997) MADS domain proteins in plant development. J Biol Chem 378:1079–1101
Riechmann JL, Ito T, Meyerowitz EM (1999) Non-AUG initiation of AGAMOUS mRNA translation in Arabidopsis thaliana. Mol Cell Biol 19:8505–8512
Rounsley SD, Ditta GS, Yanofsky MF (1995) Diverse roles for MADS box genes in Arabidopsis development. Plant Cell 7:1259–1269
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
Sieburth LE, Meyerowitz EM (1997) Molecular dissection of the AGAMOUS control region shows that cis elements for spatial regulation are located intragenically. Plant Cell 9:355–365
Swofford DL (2002) PAUP*: phylogenetic analysis using parasimony (*and other methods), 4.0b10th edn. Sunderland, Massachusetts: Sinauer Associates
Tai TH, Tanksley SD (1990) A rapid and inexpensive method for isolation of total DNA from dehydrated plant tissue. Plant Mol Biol Rep 8:297–303
Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604
Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM (1992) LEAFY controls floral meristem identity in Arabidopsis. Cell 69:843–859
Weigel D, Meyerowitz EM (1993) Activation of floral homeotic genes in Arabidopsis. Science 261:1723–1726
Wikström N, Savolainen V, Chase MW (2001) Evolution of the angiosperm: calibrating the family tree. Proc R Soc Lond B 268:2211–2220
Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA et al (1990) The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346:35–39
Yu Q, Moore PH, Albert HH, Roader AHK, Ming R (2005) Cloning and characterization of a FLORICAULA/LEAFY ortholog, PFL, in polygamous papaya. Cell Res 15:576–584
Acknowledgments
We thank Marc Crepeau and Jim Carr for technical assistance, and Elliot Meyerowitz for providing the Arabidopsis AG cDNA clone. This work was supported by a USDA-ARS Cooperative Agreement (CA 58-3020-8-134) with the Hawaii Agriculture Research Center.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Xuemei Chen
Rights and permissions
About this article
Cite this article
Yu, Q., Steiger, D., Kramer, E.M. et al. Floral MADS-box Genes in Trioecious Papaya: Characterization of AG and AP1 Subfamily Genes Revealed a Sex-type-specific Gene. Tropical Plant Biol. 1, 97–107 (2008). https://doi.org/10.1007/s12042-007-9000-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12042-007-9000-z