Plant Molecular Biology

, Volume 74, Issue 1–2, pp 129–142 | Cite as

PtSVP, an SVP homolog from trifoliate orange (Poncirus trifoliata L. Raf.), shows seasonal periodicity of meristem determination and affects flower development in transgenic Arabidopsis and tobacco plants

Article

Abstract

A MADS-box gene was isolated using the suppressive subtractive hybridization library between early-flowering mutant and wild-type trifoliate orange (Poncirus trifoliata L. Raf.). This gene is highly homologous with Arabidopsis SHORT VEGETATIVE PHASE (SVP). Based on real-time PCR and in situ hybridization during bud differentiation, PtSVP was expressed intensively in dormant tissue and vegetative meristems. PtSVP transcripts were detected in apical meristems before floral transition, then down-regulated during the transition. PtSVP expression was higher in differentiated (flower primordium) than in undifferentiated cells (apical meristems). The PtSVP expression pattern during apical meristem determination suggested that its function is not to depress flower initiation but to maintain meristem development. Transcription of PtSVP in Arabidopsis svp-41 showed partially rescued SVP function. Ectopic overexpression of PtSVP in wild-type Arabidopsis induced late flowering similar to the phenotypes induced by other SVP/StMADS-11-like genes, but transformants produced additional trichomes and floral defects, such as flower-like structures instead of carpels. Ectopic expression of PtSVP in tobacco also caused additional florets. Overexpression of PtSVP in tobacco inhibited early transition of the coflorescence and prolonged coflorescence development, thus causing additional florets at the later stage. A yeast two-hybrid assay indicated that PtSVP significantly interacted with PtAP1, a homolog of Arabidopsis APETALA1 (AP1). These findings suggest that citrus SVP homolog genes are involved in flowering time regulation and may influence inflorescence meristem identity in some conditions or genetic backgrounds. SVP homologs might have evolved among plant species, but the protein functions are conserved between Arabidopsis and citrus.

Keywords

Floral transition Meristem determination SVP/StMADS-11-like gene Trifoliate orange 

Abbreviations

FT

FLOWERING LOCUS T

GFP

Green fluorescent protein

ORF

Open reading frame

SOC1

SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1

SP

Stamen primordium

SVP

SHORT VEGETATIVE PHASE

WUS

WUSCHEL

Notes

Acknowledgments

We thank P. Huijser for providing the svp-41 seeds used in this study (Max-Planck-Institut für Züchtungsforschung, Molekulare Pflanzengenetik, Cologne, Germany). We are also grateful to Prof. Li-Zhong Xiong and Prof. Han-Hui Kuang for their helpful discussions and help in revising the manuscript. This work was supported by grants from the National Natural Science Foundation of China (grant no.30671434, 30921002, 30971973) and the 863 Project of China (grant no. 2007AA10Z188).

Supplementary material

11103_2010_9660_MOESM1_ESM.doc (2.9 mb)
Supplementary material 1 (DOC 3005 kb)

References

  1. Blázquez MA (2000) Flower development pathways. J Cell Sci 113:3547–3548PubMedGoogle Scholar
  2. Blázquez MA (2005) The right time and place for making flowers. Science 309:1024–1025CrossRefPubMedGoogle Scholar
  3. Brill EM, Watson JM (2004) Ectopic expression of a Eucalyptus grandis SVP orthologue alters the flowering time of Arabidopsis thaliana. Funct Plant Biol 31:217–224CrossRefGoogle Scholar
  4. Cervera M, Navarro L, Peña L (2009) Gene stacking in 1-year-cycling APETALA1 citrus plants for a rapid evaluation of transgenic traits in reproductive tissues. J Biotechnol 140:278–282CrossRefPubMedGoogle Scholar
  5. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefPubMedGoogle Scholar
  6. Davenport TL (1990) Citrus flowering. Hort Rev 12:349–407Google Scholar
  7. DeFolter S, Immink RGH, Kieffer M, Parenicova L, Henz SR, Weigel D, Busscher M, Kooiker M, Colombo L, Kater MM, Davies B, Angenent GC (2005) Comprehensive interaction map of the Arabidopsis MADS box transcription factors. Plant Cell 17:1424–1433CrossRefGoogle Scholar
  8. Dornelas MC, Camargo RLB, Figueiredo LHM, Takita MA (2007) A genetic framework for flowering-time pathways in Citrus spp. Genet Mol Biol 30:769–779Google Scholar
  9. Endo T, Shimada T, Fujii H, Kobayashi Y, Araki T, Omura M (2005) Ectopic expression of an FT homolog from Citrus confers an early flowering phenotype on trifoliate orange (Poncirus trifoliata L. Raf.). Transgenic Res 14:703–712CrossRefPubMedGoogle Scholar
  10. Fujiwara S, Oda A, Kamada H, Coupland G, Mizoguchi T (2005) Circadian clock components in Arabidopsis. II. LHY/CCA1 regulates the floral integrator gene SOC1 in both GI-dependent and -independent pathways. Plant Biotech 22:319–325Google Scholar
  11. Gregis V, Sessa A, Colombo L, Kater MM (2006) AGL24, SHORT VEGETATIVE PHASE, and APETALA1 redundantly control AGAMOUS during early stages of flower development in Arabidopsis. Plant Cell 18:1373–1382CrossRefPubMedGoogle Scholar
  12. Gregis V, Sessa A, Colombo L, Kater MM (2008) AGAMOUS-LIKE24 and SHORT VEGETATIVE PHASE determine floral meristem identity in Arabidopsis. Plant J 56:891–902CrossRefPubMedGoogle Scholar
  13. Hartmann U, Hohmann S, Nettesheim K, Wisman E, Saedler H, Huijser P (2000) Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. Plant J 21:351–360CrossRefPubMedGoogle Scholar
  14. Jeon JS, Lee S, Jung KH, Jun SH, Kim C, An G (2000) Tissue-preferential expression of a rice α-tubulin gene, OsTubA1, mediated by the first intron. Plant Physiol 123:1005–1014CrossRefPubMedGoogle Scholar
  15. Jeong YM, Mun JH, Lee I, Woo JC, Hong CB, Kim SG (2006) Distinct roles of the first introns on the expression of Arabidopsis profilin gene family members. Plant Physiol 140:196–209CrossRefPubMedGoogle Scholar
  16. Jimenez S, Lawton-Rauh AL, Reighard GL, Abbott AG, Bielenberg DG (2009) Phylogenetic analysis and molecular evolution of the dormancy associated MADS-box genes from peach. BMC Plant Biol 9:81CrossRefPubMedGoogle Scholar
  17. Kikuchi M, Miki T, Kumagai T, Fukuda T, Kamiyama R, Miyasaka N, Hirosawa S (2000) Identification of negative regulatory regions within the first exon and intron of the BCL6 gene. Oncogene 19:4941–4945CrossRefPubMedGoogle Scholar
  18. Kinkema M, Fan W, Dong X (2000) Nuclear localization of NPR1 is required for activation of PR gene expression. Plant Cell 12:2339–2350CrossRefPubMedGoogle Scholar
  19. Koornneef M, Alonso-Blanco C, Peeters AJM, Soppe W (1998) Genetic control of flowering time in Arabidopsis. Annu Rev Plant Physiol 49:345–370CrossRefGoogle Scholar
  20. Laux T (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122:87–96PubMedGoogle Scholar
  21. Lee JH, Park SH, Lee JS, Ahn JH (2007a) A conserved role of SHORT VEGETATIVE PHASE (SVP) in controlling flowering time of Brassica plants. BBA 1769:455–461PubMedGoogle Scholar
  22. Lee JH, Yoo SJ, Park SH, Hwang I, Lee JS, Ahn JH (2007b) Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. Gene Dev 21:397–402CrossRefPubMedGoogle Scholar
  23. Li D, Liu C, Shen L, Wu Y, Chen H, Robertson M, Helliwell CA, Ito T, Meyerowitz E, Yu H (2008) A repressor complex governs the integration of flowering signals in Arabidopsis. Dev Cell 15:110–120CrossRefPubMedGoogle Scholar
  24. Liang SQ, Zhu WX, Xiang WT (1999) Precocious trifoliate orange (Poncirus trifoliata L. Raf.) biology characteristic and its stock experiment. Zhe Jiang Citrus 16:2–4 (In Chinese)Google Scholar
  25. Liu C, Zhou J, Bracha-Drori K, Yalovsky S, Ito T, Yu H (2007) Specification of Arabidopsis floral meristem identity by repression of flowering time genes. Development 134:1901–1910CrossRefPubMedGoogle Scholar
  26. Martín-Trillo M, Martínez-Zapater JM (2002) Growing up fast: manipulating the generation time of trees. Curr Opin Biotech 13:151–155CrossRefPubMedGoogle Scholar
  27. Masiero S, Li MA, Will I, Hartmann U, Saedler H, Huijser P, Schwarz-Sommer Z, Sommer H (2004) INCOMPOSITA: a MADS-box gene controlling prophyll development and floral meristem identity in Antirrhinum. Development 131:5981–5990CrossRefPubMedGoogle Scholar
  28. Mazzitelli L, Hancock RD, Haupt S, Walker PG, Pont SDA, McNicol J, Cardle L, Morris J, Viola R, Brennan R (2007) Co-ordinated gene expression during phases of dormancy release in raspberry (Rubus idaeus L.) buds. J Exp Bot 58:1035–1045CrossRefPubMedGoogle Scholar
  29. Meilan R (1997) Floral induction in woody angiosperms. New For 14:179–202Google Scholar
  30. Pelaz S, Gustafson-Brown C, Kohalmi SE, Crosby WL, Yanofsky MF (2001) APETALA1 and SEPALLATA3 interact to promote flower development. Plant J 26:385–394CrossRefPubMedGoogle Scholar
  31. Pillitteri LJ, Lovatt CJ, Wang LL (2004) Isolation and characterization of LEAFY and APETALA1 homologues from Citrus sinensis L. Osbeck ‘Washington’. J Am Soc Hort Sci 129:846–856Google Scholar
  32. Prakash AP, Kumar PP (2002) PkMADS1 is a novel MADS box gene regulating adventitious shoot induction and vegetative shoot development in Paulownia kawakamii. Plant J 29:141–151CrossRefPubMedGoogle Scholar
  33. Salehi H, Ransom CB, Oraby HF, Seddighi Z, Sticklen MB (2005) Delay in flowering and increase in biomass of transgenic tobacco expressing the Arabidopsis floral repressor gene FLOWERING LOCUS C. J Plant Physiol 162:711–717CrossRefPubMedGoogle Scholar
  34. Schmitz G, Tillmann E, Carriero F, Fiore C, Cellini F, Theres K (2002) The tomato Blind gene encodes a MYB transcription factor that controls the formation of lateral meristems. Proc Natl Acad Sci USA 99:1064–1069CrossRefPubMedGoogle Scholar
  35. Sentoku N, Kato H, Kitano H, Imai R (2005) OsMADS22, an STMADS11-like MADS-box gene of rice, is expressed in non-vegetative tissues and its ectopic expression induces spikelet meristem indeterminacy. Mol Genet Genom 273:1–9CrossRefGoogle Scholar
  36. Tan FC, Swain SM (2007) Functional characterization of AP3, SOC1 and WUS homologues from citrus (Citrus sinensis). Physiol Plant 131:481–495CrossRefPubMedGoogle Scholar
  37. Telfer A, Bollman KM, Poethig RS (1997) Phase change and the regulation of trichome distribution in Arabidopsis thaliana. Development 124:645–654PubMedGoogle Scholar
  38. Trevaskis B, Tadege M, Hemming MN, Peacock WJ, Dennis ES, Sheldon C (2007) Short vegetative phase-like MADS-box genes inhibit floral meristem identity in barley. Plant Physiol 143:225–235CrossRefPubMedGoogle Scholar
  39. Wilkie JD, Sedgley M, Olesen T (2008) Regulation of floral initiation in horticultural trees. J Exp Bot 59:3215CrossRefPubMedGoogle Scholar
  40. Yang X, Kalluri UC, Jawdy S, Gunter LE, Yin T, Tschaplinski TJ, Weston DJ, Ranjan P, Tuskan GA (2008) The F-Box gene family is expanded in herbaceous annual plants relative to woody perennial plants. Plant Physiol 148:1189–1200CrossRefPubMedGoogle Scholar
  41. Yao JL, Zhou Y, Hu CG (2007) Apomixis in Eulaliopsis binata: characterization of reproductive mode and endosperm development. Sex Plant Reprod 20:151–158CrossRefGoogle Scholar
  42. Yu H, Ito T, Wellmer F, Meyerowitz EM (2004) Repression of AGAMOUS-LIKE 24 is a crucial step in promoting flower development. Nat Genet 36:157–161CrossRefPubMedGoogle Scholar
  43. Zhang JZ, Li ZM, Liu L, Mei L, Yao JL, Hu CG (2008) Identification of early-flower-related ESTs in an early-flowering mutant of trifoliate orange (Poncirus trifoliata L. Raf.) by suppression subtractive hybridization and macroarray analysis. Tree Physiol 28:1449–1457PubMedGoogle Scholar
  44. Zhang JZ, Li ZM, Yao JL, Hu CG (2009) Identification of flowering-related genes between early flowering trifoliate orange mutant and wild-type trifoliate orange (Poncirus trifoliata L. Raf.) by suppression subtraction hybridization (SSH) and macroarray. Gene 430:95–104CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Key Laboratory of Horticultural Plant Biology (Ministry of Education), College of Horticulture and Forestry ScienceHuazhong Agricultural UniversityWuhanChina
  2. 2.Institute of Bast Fiber CropsChinese Academy of Agricultural SciencesChangshaChina
  3. 3.National Key Laboratory of Crop Genetic ImprovementHuazhong Agricultural UniversityWuhanChina
  4. 4.College of Life Science and TechnologyHuazhong Agricultural UniversityWuhanChina

Personalised recommendations