Skip to main content
SpringerLink
Log in

Next-generation transcriptome analysis in transgenic birch overexpressing and suppressing APETALA1 sheds lights in reproduction development and diterpenoid biosynthesis

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

Abstract

Key message

Overexpression of BpAP1 could cause early flowering in birch. BpAP1 affected the expression of many flowering-related unigenes and diterpenoid biosynthesis in transgenic birch, and BpPI was a putative target gene of BpAP1.

Abstract

APETALA1 (AP1) is an MADS-box transcription factor that is involved in the flowering process in plants and has been a focus of genetic studies examining flower development. Here, we carried out transcriptome analysis of birch (Betula platyphylla Suk.), including BpAP1 overexpression lines, BpAP1 suppression lines, and non-transgenic line (NT). Compared with NT, we detected 8302 and 7813 differentially expressed unigenes in 35S::BpAP1 and 35S::BpAP1RNAi transgenic lines, respectively. Overexpression and suppression of BpAP1 in birch affected diterpenoid biosynthesis and altered expression of many flowering-related unigenes. Moreover, combining information from the RNA-seq database and the birch genome, we predicted downstream target genes of BpAP1. Among the 166 putative target genes of BpAP1, there was a positive correlation between BpAP1 and BpPI. These results provide references for further examining the relationship between BpAP1 and its target genes, and reveal that BpAP1 functions as a transcription regulator in birch.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

Abbreviations

AP1 :

APETALA1

NT:

Non-transgenic line

FT :

FLOWERING LOCUS T

SOC1 :

SUPPRESSOR OF OVEREXPRESSION OF CO1

LFY :

LEAFY

PI :

PISTILLATA

ChIP:

Chromatin immunoprecipitation

GGDP:

Geranylgeranyl diphosphate

RNA-seq:

RNA sequencing

WPM:

Woody plant medium

Nr:

Non-redundant

KEGG:

Kyoto encyclopedia of genes and genomes

COG:

Clusters of orthologous groups

GO:

Gene ontology

RPKM:

Reads per kb per million reads

DEUs:

Differentially expressed unigenes

DETGs:

Differentially expressed target genes

References

  • Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi A, Ikeda Y, Ichinoki H, Notaguchi M, Goto K, Araki T (2005) FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309:1052–1056

    Article  CAS  PubMed  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 Central  CAS  PubMed  Google Scholar 

  • Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. Nat Genet 25(1):25–29

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Audic S, Claverie JM (1997) The significance of digital gene expression profiles. Genome Res 7:986–995

    CAS  PubMed  Google Scholar 

  • Cardon GH, Hohmann S, Nettesheim K, Saedler H, Huijser P (1997) Functional analysis of the Arabidopsisthaliana SBP-box gene SPL3: a novel gene involved in the floral transition. Plant J 12:367–377

    Article  CAS  PubMed  Google Scholar 

  • Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116

    Article  CAS  Google Scholar 

  • Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676

    Article  CAS  PubMed  Google Scholar 

  • de Hoon MJ, Imoto S, Nolan J, Miyano S (2004) Open source clustering software. Bioinformatics 20(9):1453–1454

    Article  PubMed  Google Scholar 

  • Dijkstra C, Adams E, Bhattacharya A, Page AF, Anthony P, Kourmpetli S, Power JB, Lowe KC, Thomas SG, Hedden P, Phillips AL, Davey MR (2008) Over-expression of a gibberellin 2-oxidase gene from Phaseoluscoccineus L. enhances gibberellin inactivation and induces dwarfism in Solanum species. Plant Cell Rep 27:463–470

    Article  CAS  PubMed  Google Scholar 

  • Esumi T, Tao R, Yonemori K (2007) Relationship between floral development and transcription levels of LEAFY and TERMINALFLOWER1 homologs in Japanese pear (Pyruspyrifolia Nakai) and quince (Cydoniao blonga Mill.). J Jpn Soc Hortic Sci 76:294–304

    Article  CAS  Google Scholar 

  • Garcia-Martinez JL, Lopez-Diaz I, Sanchez-Beltran MJ, Phillips AL, Ward DA, Gaskin P, Hedden P (1997) Isolation and transcript analysis of gibberellin 20-oxidase genes in pea and bean in relation to fruit development. Plant Mol Biol 33:1073–1084

    Article  CAS  PubMed  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng QD, Chen ZH, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hsu CY, Liu Y, Luthe DS, Yuceer C (2006) Poplar FT2 shortens the juvenile phase and promotes seasonal flowering. Plant Cell 18:1846–1861

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 151:495–506

    Article  CAS  PubMed  Google Scholar 

  • Huang J, Lu X, Yan H, Chen S, Zhang W, Huang R, Zheng Y (2012) Transcriptome characterization and sequencing-based identification of salt-responsive genes in Millettia pinnata, a semi-mangrove plant. DNA Res 19:195–207

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Huang J, Tang D, Shen Y, Qin B, Hong L, You A, Li M, Wang X, Yu H, Gu M, Cheng Z (2010) Activation of gibberellin 2-oxidase 6 decreases active gibberellin levels and creates a dominant semi-dwarf phenotype in rice (Oryzasativa L.). J Genet Genomics 37:23–36

    Article  CAS  PubMed  Google Scholar 

  • Irish VF, Sussex IM (1990) Function of the apetala-1 gene during Arabidopsis floral development. Plant Cell 2:741–753

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jack T (2004) Molecular and genetic mechanisms of floral control. Plant Cell 16(suppl 1):S1–S17

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jarvinen P, Lemmetyinen J, Savolainen O, Sopanen T (2003) DNA sequence variation in BpMADS2 gene in two populations of Betula pendula. Mol Ecol 12:369–384

    Article  CAS  PubMed  Google Scholar 

  • Kanehisa M, Goto S (2000) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kaufmann K, Wellmer F, Muino JM, Ferrier T, Wuest SE, Kumar V, Serrano-Mislata A, Madueno F, Krajewski P, Meyerowitz EM, Angenent GC, Riechmann JL (2010) Orchestration of floral initiation by APETALA1. Science 328:85–89

    Article  CAS  PubMed  Google Scholar 

  • Klein J, Saedler H, Huijser P (1996) A new family of DNA binding proteins includes putative transcriptional regulators of the Antirrhinum majus floral meristem identity gene SQUAMOSA. Mol Gen Genet 250:7–16

    CAS  PubMed  Google Scholar 

  • Lamb RS, Hill TA, Tan QKG, Irish VF (2002) Regulation of APETALA3 floral homeotic gene expression by meristem identity genes. Development 129:2079–2086

    CAS  PubMed  Google Scholar 

  • Lee JH, Yoo SJ, Park SH, Hwang I, Lee JS, Ahn JH (2007) Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. Gene Dev 21:397–402

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lemmetyinen J, Pennanen T, Lännenpää M, Sopanen T (2001) Prevention of flower formation in dicotyledons. Mol Breed 7:341–350

    Article  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  CAS  PubMed  Google Scholar 

  • Lloyd G, McCown B (1980) Commercially-feasible micropropagation of mountain laurel, Kalmia latifolia, by use of shoot-tip culture. Combined Proc Int Plant Prop Soc 30:421–427

    Google Scholar 

  • Marioni JC, Mason CE, Mane SM, Stephens M, Gilad Y (2008) RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res 18:1509–1517

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Michaels SD, Ditta G, Gustafson-Brown C, Pelaz S, Yanofsky M, Amasino RM (2008) AGL24 acts as a promoter of flowering in Arabidopsis and is positively regulated by vernalization. Plant J 33(5):867–874

    Article  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628

    Article  CAS  PubMed  Google Scholar 

  • Ng M, Yanofsky MF (2001) Activation of the Arabidopsis B class homeotic genes by APETALA1. Plant Cell 13(4):739–753

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Norusis M (2008) SPSS 16.0 statistical procedures companion. Prentice Hall Press

  • Olszewski N, Sun TP, Gubler F (2002) Gibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell 14(Suppl 1):S61–S80

    PubMed Central  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Pillitteri LJ, Lovatt CJ, Walling LL (2004) Isolation and characterization of a TERMINAL FLOWER homolog and its correlation with juvenility in citrus. Plant Physiol 135(3):1540–1551

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Poupin MJ, Federici F, Medina C, Matus JT, Timmermann T, Arce-Johnson P (2007) Isolation of the three grape sub-lineages of B-class MADS-box TM6, PISTILLATA and APETALA3 genes which are differentially expressed during flower and fruit development. Gene 404:10–24

    Article  CAS  PubMed  Google Scholar 

  • Riechmann JL, Wang M, Meyerowitz EM (1996) DNA-binding properties of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA and AGAMOUS. Nucleic Acids Res 24:3134–3141

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288:1613–1616

    Article  CAS  PubMed  Google Scholar 

  • Searle I, He YH, Turck F, Vincent C, Fornara F, Krober S, Amasino RA, Coupland G (2006) The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Gene Dev 20:898–912

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sessions A, Yanofsky MF, Weigel D (2000) Cell-cell signaling and movement by the floral transcription factors LEAFY and APETALA1. Science 289:779–782

    Article  CAS  PubMed  Google Scholar 

  • Sundstrom JF, Nakayama N, Glimelius K, Irish VF (2006) Direct regulation of the floral homeotic APETALA1 gene by APETALA3 and PISTILLATA in Arabidopsis. Plant J 46:593–600

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Team RC (2012) R: a language and environment for statistical computing

  • Thomas SG, Phillips AL, Hedden P (1999) Molecular cloning and functional expression of gibberellin 2-oxidases, multifunctional enzymes involved in gibberellin deactivation. Proc Natl Acad Sci USA 96:4698–4703

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350–4354

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Turck F, Fornara F, Coupland G (2008) Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu Rev Plant Biol 59:573–594

    Article  CAS  PubMed  Google Scholar 

  • Wagner D, Sablowski RW, Meyerowitz EM (1999) Transcriptional activation of APETALA1 by LEAFY. Science 285:582–584

    Article  CAS  PubMed  Google Scholar 

  • Wang JW, Czech B, Weigel D (2009a) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138:738–749

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Gerstein M, Snyder M (2009b) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wellmer F, Alves-Ferreira M, Dubois A, Riechmann JL, Meyerowitz EM (2006) Genome-wide analysis of gene expression during early Arabidopsis flower development. PLoS Genet 2:e117

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 309:1056–1059

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi S (2008) Gibberellin Metabolism and its Regulation. Annu Rev Plant Biol 59:225–251

    Article  CAS  PubMed  Google Scholar 

  • Yang H, Mo H, Fan D, Cao Y, Cui S, Ma L (2012) Overexpression of a histone H3K4 demethylase, JMJ15, accelerates flowering time in Arabidopsis. Plant Cell Rep 31(7):1297–1308

    Article  CAS  PubMed  Google Scholar 

  • Yu H, Xu Y, Tan EL, Kumar PP (2002) AGAMOUS-LIKE 24, a dosage-dependent mediator of the flowering signals. Proc Natl Acad Sci 99(25):16336–16341

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang JZ, Ai XY, Sun LM, Zhang DL, Guo WW, Deng XX, Hu CG (2011) Transcriptome profile analysis of flowering molecular processes of early flowering trifoliate orange mutant and the wild-type [Poncirus trifoliata (L.) Raf.] by massively parallel signature sequencing. BMC Genom 12:63

    Article  CAS  Google Scholar 

  • Zhang X, Feng B, Zhang Q, Zhang D, Altman N, Ma H (2005) Genome-wide expression profiling and identification of gene activities during early flower development in Arabidopsis. Plant Mol Biol 58:401–419

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Fundamental Research Funds for the Central Universities, 2572015BA02.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, 26 Hexing Road, Harbin, 150040, China

    Haijiao Huang, Su Chen, Huiyu Li & Jing Jiang

Authors
  1. Haijiao Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Su Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Huiyu Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jing Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jing Jiang.

Additional information

Communicated by Z.-Y. Wang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 153 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, H., Chen, S., Li, H. et al. Next-generation transcriptome analysis in transgenic birch overexpressing and suppressing APETALA1 sheds lights in reproduction development and diterpenoid biosynthesis. Plant Cell Rep 34, 1663–1680 (2015). https://doi.org/10.1007/s00299-015-1817-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-015-1817-6

Keywords

Search

Navigation