Skip to main content
SpringerLink
Log in

Cloning and Characterization of Three APETALA1/FRUITFULL-like Genes in Different Flower Types of Rosa × hybrida L.

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

To clarify the molecular mechanism of flower development in Rosa × hybrida L., three different APETALA1/FRUITFULL (AP1/FUL)-like MADS-box genes were isolated and their expression analyzed in normally developed flowers and in malformed flowers of a stable phenotype. AP1/FUL-like genes were designated as RhAP1-1, RhFUL, and RhAP1-2. Alignment of amino acid sequences showed 83% identity between RhAP1-1 and TrAP1 of Taihangia rupestris and 82% identity between RhFUL and TrFUL of T. rupestris. RhAP1-1 is 97% identical to RhAP1-2 and 58% identical to RhFUL. Expression of RhAP1-1 and RhAP1-2 in whorls 1 and 2 of rose flowers exclusively is in accordance with the expression pattern of class A genes in other plant species. In contrast, RhFUL showed a unique expression pattern and was expressed only in sepals. The roles of all putative A, B, and C class genes were examined in different flower organs of normally developed flowers and in malformed flowers that are similar to a classic C function mutant from Arabidopsis (with petals in whorl 3 and sepals in whorl 4). The expression pattern of the putative class B genes was similar in both normal and malformed flowers. However, the putative class A genes were upregulated and class C genes were downregulated in all flower organs of the mutant. These data suggest that suppression of the class C genes RhC1 and RhC2 leads to altered expression of RhAP1-1, RhFUL, and RhAP1-2 in whorls 3 and 4 that leads to the mutant flower phenotype.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Ahmadi N, Mibus H, Serek M (2009) Characterization of ethylene-induced organ abscission in F1 breeding lines of miniature roses (Rosa hybrida L.). J Plant Growth Regul 52(3):260–266

    CAS  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Angenent GC, Franken J, Busscher M, Colombo L, van Tunen AJ (1993) Petal and stamen formation in petunia is regulated by the homeotic gene fbp1. Plant J 4:101–112

    Article  PubMed  CAS  Google Scholar 

  • Angenent GC, Franken J, Busscher M, Van Dijken A, Van Went JL (1995) A novel class of MADS box genes is involved in ovule development in Petunia. Plant Cell 7:1569–1582

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303(5666):2022–2025

    Article  PubMed  CAS  Google Scholar 

  • Chmelnitsky I, Khayat E, Zieslin N (2003) Involvement of RAG, a rose homologue of AGAMOUS, in phyllody development of Rosa hybrida cv. Motrea. Plant Growth Regul 39:63–66

    Article  CAS  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  PubMed  CAS  Google Scholar 

  • Ditta G, Pinyopich A, Robles P, Pelaza S, Yanofsky MF (2004) The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Curr Biol 14(21):1935–1940

    Article  PubMed  CAS  Google Scholar 

  • Elo A, Lemmetyinen J, Turunen ML, Tikka L, Sopanen T (2001) Three MADS-box genes similar to APETALA1 and FRUITFULL from silver birch (Betula pendula). Physiol Plant 112:95–103

    Article  PubMed  CAS  Google Scholar 

  • Elo A, Lemmetyinen J, Novak A, Keinonen K, Porali I, Hassinen M, Sopanen T (2007) BpMADS4 has a central role in the inflorescence initiation in silver birch (Betula pendula, Roth). Physiol Plant 131:149–158

    Article  PubMed  CAS  Google Scholar 

  • Ferrario S, Immink RG, Angenent GC (2004) Conservation and diversity in flower land. Curr Opin Plant Biol 7(1):84–91

    Article  PubMed  Google Scholar 

  • Ganelevin R, Zieslin N (2002) Contribution of sepals and gibberellin treatments to growth and development of rose (Rosa hybrida) flowers. Plant Growth Regul 37:255–261

    Article  CAS  Google Scholar 

  • Gu Q, Ferrandiz C, Yanofsky MF, Martienssen R (1998) The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development 125:1509–1517

    PubMed  CAS  Google Scholar 

  • Higgins DG (1994) CLUSTAL W: multiple alignments of DNA and protein sequences. Methods Mol Biol 25:307–318

    PubMed  CAS  Google Scholar 

  • Huijser P, 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

    PubMed  CAS  Google Scholar 

  • Jack T (2004) Molecular and genetic mechanisms of floral control. Pant Cell 16:1–17

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kempin SA, Savidge B, Yanofsky MF (1995) Molecular basis of the cauliflower phenotype in Arabidopsis. Science 267(5197):522–525

    Article  PubMed  CAS  Google Scholar 

  • Kitahara K, Matsumoto S (2000) Rose MADS-box genes ‘MASAKO C 1 and D 1’ homologous to class C floral identity genes. Plant Sci 151:121–134

    Article  PubMed  CAS  Google Scholar 

  • Kitahara K, Hirai S, Fukui H, Matsumoto S (2001) Rose MADS-box genes ‘MASAKO BP and B 3’ homologous to class B floral identity genes. Plant Sci 161:549–557

    Article  CAS  Google Scholar 

  • Kitahara K, Hibino Y, Aida R, 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

    Article  CAS  Google Scholar 

  • Litt A, Irish VF (2003) Duplication and diversification in the APETALA1/FRUITFUL floral homeotic gene lineage: implications for the evolution of floral development. Genetics 165:821–833

    PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Lu 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. J Evol Dev 9(1):92–104

    Article  CAS  Google Scholar 

  • Ma H, Yanpfsky MF, Meyerowitz EM (1991) AGLI-AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Genes Dev 5:484–495

    Article  PubMed  CAS  Google Scholar 

  • Mandel MA, Yanofsky MF (1995) The Arabidopsis AGL8 MADS-box gene is expressed in inflorescence meristems and is negatively regulated by APETALAI. Plant Cell 7:1763–1771

    Article  PubMed  CAS  Google Scholar 

  • Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF (1992) Molecular characterization of Arabidopsis floral homeotic gene APETELA1. Nature 360:273–277

    Article  PubMed  CAS  Google Scholar 

  • Matsumoto S, Kitahara K (2005) MADS-box genes in rose: expression analysis of AGAMOUS, PISTILLATA; APETALA3 and SEPALLATA homologue genes in the green rose. Acta Hortic 690:203–210

    CAS  Google Scholar 

  • Mor Y, Zieslin N (1992) Phyllody malformation in flowers of Rosa x hybrida cv. Motrea: effects of rootstocks, flower position, growth regulators and season. J Exp Bot 43(246):89–93

    Article  CAS  Google Scholar 

  • Müller BM, Saedler H, Zachgo S (2001) The MADS-box gene DEFH28 from Antirrhinum is involved in the regulation of floral meristem identity and fruit development. Plant J 28(2):169–179

    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  PubMed  CAS  Google Scholar 

  • Pelaz S, Gustafson-Brown C, Kohalmi SE, Crosby WL, Yanofsky MF (2001) APETALA1 and SEPALLATA3 interact to promote flower development. Plant J 26:385–394

    Article  PubMed  CAS  Google Scholar 

  • Pnueli L, Abdu-Abdeid M, Zamir D, Nacken W, Schwarz-Sommer Z, Lifschitz E (1991) The MADS box gene family in tomato: temporal expression during floral development, conserved secondary structures and homology with homeotic genes from Antirrhinum and Arabidopsis. Plant J 1:255–266

    Article  PubMed  CAS  Google Scholar 

  • Preston JC, Kellogg EA (2007) Conservation and divergence of APETALA1/FRUITFULL-like gene function in grasses: evidence from gene expression analyses. Plant J 52(1):69–81

    Article  PubMed  CAS  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386

    PubMed  CAS  Google Scholar 

  • Sather DN, Golenberg EM (2009) Duplication of AP1 within the Spinacia oleracea L. AP1/FUL clade is followed by rapid amino acid and regulatory evolution. Planta 229(3):507–521

    Article  PubMed  CAS  Google Scholar 

  • Schwarz-Sommer ZS, Huijser P, Nacken W, Saedeler H, Sommer H (1990) Genetic control of flower development by homeotic genes in Antirrhinum majus. Science 250:931–936

    Article  PubMed  CAS  Google Scholar 

  • Shore P, Sharrocks AD (1995) The MADS box family of transcription factors. Eur J Biochem 229:1–13

    Article  PubMed  CAS  Google Scholar 

  • Sriskandarajah S, Mibus H, Serek M (2007) Transgenic Campanula carpatica plants with reduced ethylene sensitivity. Plant Cell Rep 26:805–813

    Article  PubMed  CAS  Google Scholar 

  • Sung SK, Yu GH, An GH (1999) Characterization of MdMADS2, a member of the SQUAMOSA subfamily of genes, in apple. Plant Physiol 120:969–978

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Theissen G, Saedler H (1995) MADS-box genes in plant ontogeny and phylogeny: Haeckel’s ‘biogenetic law’ revisited. Curr Opin Genet Dev 5:628–639

    Article  PubMed  CAS  Google Scholar 

  • Theissen G, Saedler H (2001) Plant biology. Floral quartets. Nature 409:469–471

    Article  PubMed  CAS  Google Scholar 

  • Theissen G, Kim JT, Saedler H (1996) Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes. J Mol Evol 43:484–516

    Article  PubMed  CAS  Google Scholar 

  • Vandenbussche M, Theissen G, van de Peer Y, Gerats T (2003) Structural diversification and neo-functionalization during floral MADS-box gene evolution by C-terminal frameshift mutation. Nucleic Acids Res 31:4401–4409

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi A, Wu MF, Yang L, Yang L, Wu G, Poethig R, Wagner D (2009) The microRNA-regulated SBP-box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Dev Cell 17(2):268–278

    Article  PubMed  CAS  Google Scholar 

  • Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann K, Meyerowitz EM (1990) The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346:35–39

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Prof. Bjarne M. Stummann for critical reading of the manuscript and valuable comments, and Prof. Errol Hewett (Massey University, Palmerston North, New Zealand) for linguistic editing of the manuscript.

Author information

Authors and Affiliations

  1. Faculty of Natural Sciences, Institute for Ornamental and Woody Plant Science, Leibniz University of Hannover, Herrenhäuser Str. 2, 30419, Hannover, Germany

    Heiko Mibus, Dirk Heckl & Margrethe Serek

Authors
  1. Heiko Mibus
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dirk Heckl
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Margrethe Serek
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Heiko Mibus.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mibus, H., Heckl, D. & Serek, M. Cloning and Characterization of Three APETALA1/FRUITFULL-like Genes in Different Flower Types of Rosa × hybrida L.. J Plant Growth Regul 30, 272–285 (2011). https://doi.org/10.1007/s00344-010-9190-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-010-9190-8

Keywords

Search

Navigation