Functional analysis of an APETALA1-like MADS box gene from Eustoma grandiflorum in regulating floral transition and formation

  • Tien-Hsin Chuang
  • Kun-Hung Li
  • Pei-Fang Li
  • Chang-Hsien Yang
Original Article
  • 17 Downloads

Abstract

An Eustoma grandiflorum APETALA1 (EgAP1) gene showing high homology to the SQUA subfamily of MADS-box genes was isolated and characterized. EgAP1, containing a conserved euAP1 motif at the C-terminus, showed high sequence identity to Antirrhinum majus SQUAMOSA in the SQUA subfamily. EgAP1 mRNA was detected in the leaf and expressed significantly higher in young flower buds than in mature flower buds. In flowers, EgAP1 mRNA was strongly detected in sepal, weakly detected in petal and was absent in stamen and carpel. Transgenic Arabidopsis plants ectopically expressing EgAP1 flowered early and produced terminal flowers. In addition, the conversion of petals into stamen-like structures was also observed in 35S::EgAP1 flowers. 35S::EgAP1 was able to complement the ap1 flower defects by restoring the defect for sepal formation and significantly increasing second whorl petal production in Arabidopsis ap1 mutant plants. These results revealed that EgAP1 is the APETALA1 homolog in E. grandiflorum and that the function of EgAP1 is involved in floral induction and flower formation.

Keywords

APETALA1 Arabidopsis thaliana Eustoma grandiflorum Floral induction MADS box genes SQUAMOSA 

Notes

Acknowledgements

This work was supported by grants to C-H Y from the National Science Council, Taiwan, ROC, Grant nos. NSC98-2622-B-005-001–CC2 and NSC99-2622-B-005-001-CC2. This work was also supported in part by the Ministry of Education, Taiwan, R.O.C. under the ATU plan.

References

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefPubMedGoogle Scholar
  2. Angenent GC, Busscher M, Franken J, Mol JNM, van Tunen AJ (1992) Differential expression of two MADS box genes in wild-type and mutant petunia flowers. Plant Cell 4:983–993CrossRefPubMedPubMedCentralGoogle Scholar
  3. Angenent GC, Franken J, Busscher M, Weiss D, van Tunen AJ (1994) Co-suppression of the petunia homeotic gene fbp2 affects the identity of the generative meristem. Plant J 5:33–44CrossRefPubMedGoogle Scholar
  4. Azeez A, Miskolczi P, Tylewicz S, Bhalerao RP (2014) A tree ortholog of APETALA1 mMediates photoperiodic control of seasonal growth. Curr Biol 24:717–724CrossRefPubMedGoogle Scholar
  5. Berbel A, Navarro C, Ferrandiz C, Canas LA, Madueno F, Beltran JP (2001) Analysis of PEAM4, the pea AP1 functional homologue, supports a model for AP1-like genes controlling both floral meristem and floral organ identity in different plant species. Plant J 25:441–451CrossRefPubMedGoogle Scholar
  6. Bowman JL, Alvarez J, Weigel D, Meyerowitz EM (1993) Control of flower development in Arabidopsis thaliana by APETALA1 and interacting genes. Development 119:721–743Google Scholar
  7. Chang YY, Chiu YF, Wu JW, Yang CH (2009) Four orchid (Oncidium Gower Ramsey) AP1/AGL9-like MADS box genes show novel expression patterns and cause different effects on floral transition and formation in Arabidopsis thaliana. Plant Cell Physiol 50:1425–1438CrossRefPubMedGoogle Scholar
  8. Chen MK, Lin IC, Yang CH (2008) Functional analysis of three lily (Lilium longiflorum) APETALA1-like MADS box genes in regulating floral transition and formation. Plant Cell Physiol 49:704–717CrossRefPubMedGoogle Scholar
  9. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefPubMedGoogle Scholar
  10. Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37CrossRefPubMedGoogle Scholar
  11. Ferrandiz C, Gu Q, Martienssen R, Yanofsky MF (2000) Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development 127:725–734PubMedGoogle Scholar
  12. Fornara F, Parˇenicova L, Falasca G, Pelucchi N, Masiero S, Ciannamea S, Lopez-Dee Z, Altamura MM, Colombo L, Kater MM (2004) Functional characterization of OsMADS18, a member of the AP1/SQUA subfamily of MADS box genes. Plant Physiol 135:2207–2219CrossRefPubMedPubMedCentralGoogle Scholar
  13. Gustafson-Brown C, Savidge B, Yanofsky MF (1994) Regulation of the Arabidopsis floral homeotic gene. APETALA1 Cell 76:131–143CrossRefPubMedGoogle Scholar
  14. Hou CJ, Yang CH (2009) Functional analysis of FT and TFL1 orthologs from orchid (Oncidium Gower Ramsey) that regulate the vegetative to reproductive transition. Plant Cell Physiol 50:1544–1557CrossRefPubMedGoogle Scholar
  15. Hou CJ, Yang CH (2016) Comparative analysis of the pteridophyte Adiantum MFT ortholog reveals the specificity of combined FT/MFT C and N terminal interaction with FD for the regulation of the downstream gene AP1.. Plant Mol Biol 91:563–579CrossRefPubMedGoogle Scholar
  16. Hsu HF, Huang CH, Chou LH, Yang CH (2003) Ectopic expression of an orchid (Oncidium Gower Ramsey) AGL6-like gene promotes flowering by activating flowering time genes in Arabidopsis thaliana. Plant Cell Physiol 44:783–794CrossRefPubMedGoogle Scholar
  17. Huang H, Wang S, Jiang J, Liu G, Li H, Chen S, Xu H (2014) Overexpression of BpAP1 induces early flowering and produces dwarfism in Betula platyphylla × Betula pendula. Physiol Plant 151:495–506CrossRefPubMedGoogle Scholar
  18. Huijser P, Klein J, Lonnig W, 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 11:1239–1249PubMedPubMedCentralGoogle Scholar
  19. Ichimura K, Korenaga M (1998) Improvement of vase life and petal color expression in several cultivars of cut Eustoma flowers using sucrose with 8-hydroxy-quinoline sulfate. Bull Natl Res Inst Veg Ornam Plants Tea 13:31–39Google Scholar
  20. Ishimori M, Kawabata S (2014) Conservation and diversification of floral homeotic MADS-box genes in Eustoma grandiflorum. J Jpn Soc Hort Sci 83:172–180CrossRefGoogle Scholar
  21. Jack T (2001) Plant development going MADS. Plant Mol Biol 46:515–520CrossRefPubMedGoogle Scholar
  22. Jang S, An K, Lee S, An G (2002) Characterization of tobacco MADS-box genes involved in floral initiation. Plant Cell Physiol 43:230–238CrossRefPubMedGoogle Scholar
  23. Jeon JS, Lee S, Jung KH, Yang WS, Yi GH, Oh BG, An G (2000) Production of transgenic rice plants showing reduced heading date and plant height by ectopic expression of rice MADS-box genes. Mol Breed 6:581–592CrossRefGoogle Scholar
  24. Kater MM, Dreni L, Colombo L (2006) Functional conservation of MADS-box factors controlling floral organ identity in rice and Arabidopsis. J Exp Bot 57:3433–3444CrossRefPubMedGoogle Scholar
  25. Kempin SA, Savidge B, Yanofsky MF (1995) Molecular basis of the cauliflower phenotype in Arabidopsis. Science 267:522–525CrossRefPubMedGoogle Scholar
  26. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120CrossRefPubMedGoogle Scholar
  27. Kyozuka J, Harcourt R, Peacock WJ, Dennis ES (1997) Eucalyptus has functional equivalents of the Arabidopsis AP1 gene. Plant Mol Biol 35:573–584CrossRefPubMedGoogle Scholar
  28. Kyozuka J, Kobayashi T, Morita M, Shimamoto K (2000) Spatially and temporally regulated expression of rice MADS box genes with similarity to Arabidopsis class A, B and C genes. Plant Cell Physiol 41:710–718CrossRefPubMedGoogle Scholar
  29. Li KH, Chung TH, Hou CJ, Yang CH (2015) Functional analysis of the FT homolog from Eustoma grandiflorum reveals its role in regulating A and C functional MADS box genes to control floral transition and flower formation. Plant Mol Biol Rep 33:770–782CrossRefGoogle Scholar
  30. Liljegren SJ, Gustafson-Brown C, Pinyopich A, Ditta GS, Yanofsky MF (1999) Interactions among APETALA1, LEAFY, and TERMINAL FLOWER1 specify meristem fate. Plant Cell 11:1007–1018CrossRefPubMedPubMedCentralGoogle Scholar
  31. Litt A, Irish VF (2003) Duplication and diversification in the APETALA1/FRUITFULL floral homeotic gene lineage: implications for the evolution of floral development. Genetics 165:821–833PubMedPubMedCentralGoogle Scholar
  32. Liu Y, Kong J, Li T, Wang Y, Wang A, Han Z (2013a) Isolation and characterization of an APETALA1-like gene from pear (Pyrus pyrifolia). Plant Mol Biol Rep 31:1031–1039CrossRefGoogle Scholar
  33. Liu Y, Song H, Liu Z, Hu G, Lin S (2013b) Molecular characterization of loquat EjAP1 gene in relation to flowering. Plant Growth Regul 70:287–296CrossRefGoogle Scholar
  34. Mandel MA, Yanofsky MF (1995) A gene triggering flower formation in Arabidopsis. Nature 377:522–524CrossRefPubMedGoogle Scholar
  35. Mandel MA, Yanofsky MF (1998) The Arabidopsis AGL9 MADS box gene is expressed in young flower primordia. Sex Plant Reprod 11:22–28CrossRefGoogle Scholar
  36. Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360:273–277CrossRefPubMedGoogle Scholar
  37. Masiero S, Imbriano C, Ravasio F, Favaro R, Pelucchi N, Gorla MS, Mantovani R, Colombo L, Kater MM (2002) Ternary complex formation between MADS-box transcription factors and the histone fold protein NF-YB. J Biol Chem 277:26429–26435CrossRefPubMedGoogle Scholar
  38. Mino M, Oka M, Tasaka Y, Iwabuchi M (2003) Thermoinduction of genes encoding the enzymes of gibberellin biosynthesis and a putative negative regulator of gibberellin signal transduction in Eustoma grandiflorum. Plant Cell Rep 22:159–165CrossRefPubMedGoogle Scholar
  39. Miyazaki S, Sugawara H, Ikeo K, Gojobori T, Tateno Y (2004) DDBJ in the stream of various biological data. Nucleic Acids Res 32:D31-D34CrossRefPubMedCentralGoogle Scholar
  40. Mouradov A, Glassick TV, Hamdorf BA, Murphy LC, Marla SS, Yang Y, Teasdale RD (1998) Family of MADS-box genes expressed early in male and female reproductive structure of monterey pine. Plant Physiol 117:55–61CrossRefPubMedPubMedCentralGoogle Scholar
  41. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–479CrossRefGoogle Scholar
  42. Ohkawa K, Kano A, Kanematsu K, Korenaga M (1991) Effects of air temperature and time on rosette formation in seedlings of Eustoma grandiflorum. (Raf.). Shinn Sci Hortic 48:171–176CrossRefGoogle Scholar
  43. Ohkawa K, Korenaga M, Yoshizumi T (1993) Influence of temperature prior to seed ripening and at germination on rosette formation and bolting of Eustoma grandiflorum. Sci Hortic 53:225–230CrossRefGoogle Scholar
  44. Ohkawa K, Yoshizumi T, Korenaga M, Kanematsu K (1994) Reversal of heat-induced rosetting in Eustoma grandiflorum with low temperatures. Hortscience 29:165–166Google Scholar
  45. Peng YJ, Shih CF, Yang JY, Tan CM, Hsu WH, Huang YP, Liao PC, Yang CH (2013) A RING-Type E3 ligase controls anther dehiscence by activating the jasmonate biosynthetic pathway gene DEFECTIVE IN ANTHER DEHISCENCE1 in Arabidopsis. Plant J 74:310–327CrossRefPubMedGoogle Scholar
  46. Pnueli L, Hareven D, Broday L, Hurwitz C, Lifschitz E (1994) The TM5 MADS box gene mediates organ differentiation in the three inner whorls of tomato flowers. Plant Cell 6:175–186CrossRefPubMedPubMedCentralGoogle Scholar
  47. Purugganan MD, Rounsley SD, Schmidt RJ, Yanofsky MF (1995) Molecular evolution of flower development: diversification of the plant MADS-box regulatory gene family. Genetics 140:345–356PubMedPubMedCentralGoogle Scholar
  48. Rounsley SD, Ditta GS, Yanofsky MF (1995) Diverse roles for MADS box genes in Arabidopsis development. Plant Cell 7:1259–1269CrossRefPubMedPubMedCentralGoogle Scholar
  49. Schultz EA, Haughn GW (1993) Genetic analysis of the floral initiation process (FLIP) in Arabidopsis. Development 119:745–765Google Scholar
  50. Sun LM, Zhang JZ, Mei L, Hu CH (2014a) Molecular cloning, promoter analysis and functional characterizationof APETALA1-like gene from precocious trifoliate orange (Poncirus trifoliata L. Raf.). Sci Hortic 178:95–105CrossRefGoogle Scholar
  51. Sun Y, Fan Z, Li X. Li J, Yin H (2014b) The APETALA1 and FRUITFUL homologs in Camellia japonica and their roles in double flower domestication. Mol Breed 33:821–834CrossRefGoogle Scholar
  52. Sung SK, Yu GH, An G (1999) Characterization of MdMADS2, a member of the SQUAMOSA subfamily of genes, in apple. Plant Physiol 120:969–978CrossRefPubMedPubMedCentralGoogle Scholar
  53. Tang M, Tao YB, Xu ZF (2016) Ectopic expression of Jatropha curcas APETALA1 (JcAP1) caused early flowering in Arabidopsis, but not in Jatropha. PeerJ 4:e1969.  https://doi.org/10.7717/peerj.1969 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Theißen G (2001) Development of floral organ identity: stories from the MADS house. Curr Opin Plant Biol 4:75–85CrossRefPubMedGoogle Scholar
  55. Theißen G, Saedler H (1995) MADS-box genes in ontogeny and phylogeny of plants: Haeckel’s ‘biogenetic law’ revisited. Curr Opin Genet Dev 5:628–639CrossRefPubMedGoogle Scholar
  56. Theißen G, Saedler H (2001) Floral quartets. Nature 409:469–471CrossRefPubMedGoogle Scholar
  57. Theißen G, Becker A, Di Rosa A, Kanno A, Kim JT, Münster T, Winter KU, Saedler H (2000) A short history of MADS-box genes in plants. Plant Mol Biol 42:115–149CrossRefPubMedGoogle Scholar
  58. Thompson JD, Higgins DG, Gibson TJ (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefPubMedPubMedCentralGoogle Scholar
  59. 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 mutations. Nucleic Acids Res 31:4401–4409CrossRefPubMedPubMedCentralGoogle Scholar
  60. Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309:1056–1059CrossRefPubMedGoogle Scholar
  61. Yamamoto A, Fujita K, Takabe T (2010) Ectopic expression of DnaK chaperone from a halotolerant cyanobacterium Aphanothece halophytica induced the bolting without cold treatment in Eustoma grandiflorum. Plant Biotechnol 27:489–493CrossRefGoogle Scholar
  62. Yu H, Goh CJ (2000) Identification and characterization of three orchid MADS-box genes of the AP1/AGL9 subfamily during floral transition. Plant Physiol 123:1325–1336CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Korean Society for Plant Biotechnology and Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  • Tien-Hsin Chuang
    • 1
  • Kun-Hung Li
    • 1
  • Pei-Fang Li
    • 1
  • Chang-Hsien Yang
    • 1
    • 2
  1. 1.Institute of BiotechnologyNational Chung Hsing UniversityTaichungTaiwan, ROC
  2. 2.Agricultural Biotechnology CenterNational Chung Hsing UniversityTaichungTaiwan, ROC

Personalised recommendations