Skip to main content
Log in

Exon skipping of AGAMOUS homolog PrseAG in developing double flowers of Prunus lannesiana (Rosaceae)

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Two transcript isoforms of AGAMOUS homologs, from single and double flower Prunus lannesiana, respectively, showed different functions.

Abstract

The Arabidopsis floral homeotic C function gene AGAMOUS (AG) confers stamen and carpel identity. Loss of AG function results in homeotic conversions of stamens into petals and formation of double flowers. In order to present a molecular dissection of a double-flower cultivar in Prunus lannesiana (Rosaceae), we isolated and identified a single-copy gene, AG homolog from two genetically cognate P. lannesiana bearing single and double flowers, respectively. Sequence analysis revealed that the AG homolog, prseag-1, from double flowers showed a 170-bp exon skipping as compared to PrseAG (Prunus serrulata AGAMOUS) from the single flowers. Genomic DNA sequence revealed that abnormal splicing resulted in mutant prseag-1 protein with the C-terminal AG motifs I and II deletions. In addition, protein sequence alignment and phylogenetic analyses revealed that the PrseAG was grouped into the euAG lineage. A semi-quantitative PCR analysis showed that the expression of PrseAG was restricted to reproductive organs of stamens and carpels in single flowers of P. lannesiana ‘speciosa’, while the prseag-1 mRNA was highly transcribed throughout the petals, stamens, and carpels in double flowers from ‘Albo-rosea’. The transgenic Arabidopsis containing 35S::PrseAG displayed extremely early flowering, bigger stamens and carpels and homeotic conversion of petals into staminoid organs, but ectopic expression of prseag-1 could not mimic the phenotypic ectopic expression of PrseAG in Arabidopsis. In general, this study provides evidences to show that double flower ‘Albo-rosea’ is a putative C functional ag mutant in P. lannesiana.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

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

    PubMed  CAS  Google Scholar 

  • Bowman JL, Drews GN, Meyerowitz EM (1991b) Expression of the Arabidopsis floral homeotic gene agamous is restricted to specific cell types late in flower development. Plant Cell 3:749–758

    PubMed  CAS  Google Scholar 

  • Brewbader JL, Kwack BH (1963) The essential role of calcium ion in pollen tube germination and pollen tube growth. Am J Bot 50:859–865

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Dellaporta SL, Wood J, Hicks JB (1983) A plant minipreparation: version II. Plant Mol Biol Rep 1:19–20

    Article  CAS  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Drews GN, Bowman JL, Meyerowitz EM (1991) Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell 65:991–1002

    Article  PubMed  CAS  Google Scholar 

  • Egea-Cortlnes M, Saedler H, Sommer H (1999) Ternary complex formation between the MADS-box proteins SQUAMOSA, DEFICIENS and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus. The EMBO J 18:5370–5379

    Article  Google Scholar 

  • Galimba KD, Tolkin TR, Sullivan AM, Melzer R, Theißen G, Di Stilio VS (2012) Loss of deeply conserved C-class floral homeotic gene function and C- and E-class protein interaction in a double-flowered ranunculid mutant. Proc Natl Acad Sci U S A 109(34):E2267–2275

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hu S (1993) Experimental methods in plant embryology (I) determination of pollen viability. Chin Bull Bot 10:60–62 (in Chinese)

    Google Scholar 

  • Johanse DA (1940) Plant microtechnique. McGraw-Hill Book Company, New York, pp 27–94

    Google Scholar 

  • Kaufmann K, Melzer R, Thelssen G (2005) MIKC-type MADS-domain proteins: structural modularity, protein interactions and network evolution in land plants. Genes 347:183–198

    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′ cause similar homeotic transformation of sepal and petal in Arabidopsis and sepal in Torenia. Plant Sci 166:1245–1252

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Krizek BA, Fletcher JC (2005) Molecular mechanisms of flower development: an armchair guide. Nat Rev Genet 6:688–698

    Article  PubMed  CAS  Google Scholar 

  • Krizek BA, Meyerowitz EM (1996) Mapping the protein regions responsible for the functional specificities of the Arabidopsis MADS domain organ-identity proteins. Proc Natl Acad Sci U S A 93:4063–4070

    Article  PubMed  CAS  Google Scholar 

  • Lamb RS, Irish VF (2003) Functional divergence within the APETALA3/PISTILLATA floral homeotic gene lineages. Proc Natl Acad Sci U S A 100: 6558–6563

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Lv S, Du X, Lu W, Chong K, Meng Z (2007a) 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

    Article  Google Scholar 

  • Lv S, Du X, Lu W, Chong K, Meng Z (2007b) 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revied media for rapid growth and bioassay with tobacco cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Pelaz S, Ditta GS, Baumann E, Wisman E, Yanofsky MF (2000) B and C foral organ identity functions require SEPALLATA MADS-box genes. Nature 405:200–203

    Article  PubMed  CAS  Google Scholar 

  • Riechmann JL, Krizek BA, Meyerowitz EM (1996) Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. Proc Natl Acad Sci U S A 93:4793–4798

    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 

  • Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767

    PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Bio Evol 24(8):1596–1599

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Tzeng TY, Liu HC, Yang CH (2004) The C-terminal sequence of LMADS1 is essential for the formation of homodimers for B function proteins. J Biol Chem 279:10747–11075

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Whipple CJ, Schmidt RJ (2006) Genetics of grass flower development. Adv Bot Res 44:385–424

    Article  CAS  Google Scholar 

  • Yang Y, Thomas J (2004) Defining subdomains of the K domain important for protein–protein interactions of plant MADS proteins. Plant Mol Biol 55:45–59

    Article  PubMed  CAS  Google Scholar 

  • Zahn LM, Feng BM, Ma H (2006) Beyond the ABC-model: regulation of floral homeotic genes. Adv Bot Res 44:164–196

    Google Scholar 

  • Zhang P, Tan HT, Pwee KH, Kumar PP (2004) Conservation of class C function of floral organ development during 300 million years of evolution from gymnosperms to angiosperms. Plant J 37(4):566–577

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by National Nature Science Foundation of China (Grants 31170574).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hai Lu.

Additional information

Communicated by K. Kamo.

Z. Liu and D. Zhang contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, Z., Zhang, D., Liu, D. et al. Exon skipping of AGAMOUS homolog PrseAG in developing double flowers of Prunus lannesiana (Rosaceae). Plant Cell Rep 32, 227–237 (2013). https://doi.org/10.1007/s00299-012-1357-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-012-1357-2

Keywords

Navigation