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SuperSAGE combined with PCR walking allows global gene expression profiling of banana (Musa acuminata), a non-model organism

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Abstract

Super-serial analysis of gene expression (SuperSAGE) was used to characterize, for the first time, the global gene expression pattern in banana (Musa acuminata). A total of 10,196 tags were generated from leaf tissue, representing 5,292 expressed genes. Forty-nine tags of the top 100 most abundantly expressed transcripts were annotated by homology to cDNA or EST sequences. Typically for leaf tissue, analysis of the transcript profiles showed that the majority of the abundant transcripts are involved in energy production, mainly photosynthesis. However, the most abundant tag was derived from a type 3 metallothionein transcript, which accounted for nearly 3% of total transcripts analysed. Furthermore, the 26-bp long SuperSAGE tags were applied in 3′-rapid amplification of cDNA ends (3′RACE) for the identification of unknown tags. In combination with thermal asymmetric interlaced PCR (TAIL-PCR), this allowed the recovery of a full gene sequence of a novel NADPH:protochlorophyllide oxidoreductase, the key enzyme in chlorophyll biosynthesis. SuperSAGE in conjunction with 3′RACE and TAIL-PCR will be a powerful tool for transcriptomics of non-model, but otherwise important organisms.

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Abbreviations

MT:

metallothionein

RACE:

rapid amplification of cDNA ends

SAGE:

serial analysis of gene expression

TAIL-PCR:

thermal asymmetric interlaced PCR

References

  • Aert R, Sági L, Volckaert G (2004) Gene content and density in banana (Musa acuminata) as revealed by genomic sequencing of BAC clones. Theor Appl Genet 109:129–139

    PubMed  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 

  • Chakravarthy S, Tuori RP, D’Ascenzo MD, Fobert PR, Després C, Martin GB (2003) The tomato transcription factor Pti4 regulates defense-related gene expression via GCC box and non-GCC box cis elements. Plant Cell 15:3033–3050

    Article  PubMed  CAS  Google Scholar 

  • Chen JJ, Rowley JD, Wang SM (2000) Generation of longer cDNA fragments from serial analysis of gene expression tags for gene identification. Proc Natl Acad Sci USA 97:349–353

    Article  PubMed  ADS  CAS  Google Scholar 

  • Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182

    Article  PubMed  CAS  Google Scholar 

  • Eggermont K, Goderis I, Broekaert W (1996) High-throughput RNA extraction from samples based on homogenization by reciprocal shaking in the presence of sand and glass beads. Plant Mol Biol Rep 14:273–279

    Article  CAS  Google Scholar 

  • Ekman DR, Lorenz WW, Przybyla AE, Wolfe NL, Dean JFD (2003) SAGE analysis of transcriptome responses in Arabidopsis roots exposed to 2,4,6-trinitrotoluene. Plant Physiol 133:1397–1406

    Article  PubMed  CAS  Google Scholar 

  • Fizames C, Muños S, Cazettes C, Nacry P, Boucherez J, Gaymard F, Piquemal D, Delorme V, Commes T, Doumas P, Cooke R, Marti J, Sentenac H, Gojon A (2004) The Arabidopsis root transcriptome by serial analysis of gene expression. Gene identification using the genome sequence. Plant Physiol 134:67–80

    Article  PubMed  CAS  Google Scholar 

  • Gibbings JG, Cook BP, Dufault MR, Madden SL, Khuri S, Turnbull CJ, Dunwell M (2003) Global transcript analysis of rice leaf and seed using SAGE technology. Plant Biotechnol J 1:271–285

    Article  PubMed  CAS  Google Scholar 

  • Hashimoto SI, Suzuki Y, Kasai Y, Morohoshi K, Yamada T, Sese J, Morishita S, Sugano S, Matsushima K (2004) 5′end SAGE for the analysis of transcriptional start sites. Nat Biotechnol 22:1146–1149

    Article  PubMed  CAS  Google Scholar 

  • Jung S, Lee J, Lee D (2003) Use of SAGE technology to reveal changes in gene expression in Arabidopsis leaves undergoing cold stress. Plant Mol Biol 52:553–567

    Article  PubMed  CAS  Google Scholar 

  • Lee JY, Lee DH (2003) Use of serial analysis of gene expression technology to reveal changes in gene expression in Arabidopsis pollen undergoing cold stress. Plant Physiol 132:517–529

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Mitsukawa N, Oosumi T, Whittier RF (1995) Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J 8:457–463

    Article  PubMed  CAS  Google Scholar 

  • Lorenz WW, Dean JFD (2002) SAGE profiling and demonstration of differential gene expression along the axial developmental gradient of lignifying xylem in loblolly pine (Pinus taeda). Tree Physiol 22:301–310

    PubMed  CAS  Google Scholar 

  • Lysák M, Dolezelova M, Horry JP, Swennen R, Dolezel J (1999) Flow cytometric analysis of nuclear DNA content in Musa. Theor Appl Genet 98:1344–1350

    Google Scholar 

  • Matsumura H, Nirasawa S, Terauchi R (1999) Transcript profiling in rice (Oryza sativa L.) seedlings using serial analysis of gene expression (SAGE). Plant J 20:719–726

    Article  PubMed  CAS  Google Scholar 

  • Matsumura H, Nirasawa S, Kiba A, Urasaki N, Saitoh H, Ito M, Kawai-Yamada M, Uchimiya H, Terauchi R (2003a) Overexpression of Bax inhibitor suppresses the fungal elicitor-induced cell death in rice (Oryza sativa L.) cells. Plant J 33:425–434

    Article  PubMed  CAS  Google Scholar 

  • Matsumura H, Reich S, Ito A, Saitoh H, Kamoun S, Winter P, Kahl G, Reuter M, Krüger DH, Terauchi R (2003b) Gene expression analysis of plant host-pathogen interactions by SuperSAGE. Proc Natl Acad Sci USA 100:15718–15723

    Article  PubMed  ADS  CAS  Google Scholar 

  • Ng P, Wei C, Sung W, Chiu KP, Lipovich L, Ang CC, Gupta S, Shahab A, Ridwan A, Wong CH, Liu ET, Ruan Y (2005) Gene identification signature (GIS) analysis for transcriptome characterisation and genome annotation. Nat Methods 2:105–111

    Article  PubMed  CAS  Google Scholar 

  • Pauws E, Van Kampen AHC, Van de Graaf SAR, De Vijlder JJM, Ris-Stalpers C (2001) Heterogeneity in polyadenylation cleavage sites in mammalian mRNA sequences: implications for SAGE analysis. Nucleic Acids Res 29:1690–1694

    Article  PubMed  CAS  Google Scholar 

  • Raskin VI, Schwartz A (2002) The charge-transfer complex between protochlorophyllide and NADPH: an intermediate in protochlorophyllide photoreduction. Photosynth Res 74:181–186

    Article  PubMed  CAS  Google Scholar 

  • Robinson SJ, Cram DJ, Lewis CT, Parkin IAP (2004) Maximizing the efficacy of SAGE analysis identifies novel transcripts in Arabidopsis. Plant Physiol 136:3223–3233

    Article  PubMed  CAS  Google Scholar 

  • Ryo A, Kondoh N, Wakatsuki T, Hada A, Yamamoto N, Yamamoto M, Yamamoto N (2000) A modified serial analysis of gene expression that generates longer sequence tags by nonpalindromic cohesive linker ligation. Anal Biochem 277:160–162

    Article  PubMed  CAS  Google Scholar 

  • Saha S, Sparks AB, Rago C, Akmaev V, Wang CJ, Vogelstein B, Kinzler KW, Velculescu VE (2002) Using the transcriptome to annotate the genome. Nat Biotechnol 20:508–512

    Article  PubMed  CAS  Google Scholar 

  • Spano AJ, He Z, Michel H, Hunt DF, Timko MP (1992) Molecular cloning, nuclear gene structure, and developmental expression of NADPH:protochlorophyllide oxidoreductase in pea (Pisum sativum L.). Plant Mol Biol 18:967–972

    Article  PubMed  CAS  Google Scholar 

  • Van den Berg A, Van der Leij J, Poppema S (1999) Serial analysis of gene expression: rapid RT-PCR analysis of unknown SAGE tags. Nucleic Acids Res 27:17

    Article  Google Scholar 

  • Velculescu VE, Zhang L, Vogelstein B, Kinzler KW (1995) Serial analysis of gene expression. Science 270:484–487

    PubMed  ADS  CAS  Google Scholar 

  • Velculescu VE, Zhang L, Zhou W, Vogelstein J, Basrai MA, Bassett DE, Hieter P, Vogelstein B, Kinzler KW (1997) Characterization of the yeast transcriptome. Cell 88:243–251

    Article  PubMed  CAS  Google Scholar 

  • Wei CL, Ng P, Chiu KP, Wong CH, Ang CC, Lipovich L, Liu ET, Ruan Y (2004) 5′ Long serial analysis of gene expression (LongSAGE) and 3′ longSAGE for transcriptome characterization and genome annotation. Proc Natl Acad Sci USA 101:11701–11706

    Article  PubMed  ADS  CAS  Google Scholar 

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Acknowledgements

The authors are indebted to Dr. S. Reich and Dr. D. Krüger (Humboldt University, Berlin, Germany) for providing the EcoP15I endonuclease and Dr. K.W. Kinzler (Johns Hopkins University, Baltimore, USA) for making the SAGE2000 software available. We are also grateful to Ms. I. Van den houwe (INIBAP Transit Center, Katholieke Universiteit Leuven, Belgium) for providing the plant material. Many thanks are due to Mr. I. Op De Beeck, Mr. C.O. Dimkpa and Ms. E. Thiry for technical assistance. Access to the Syngenta Musa 3′ EST database, donated by Syngenta to the International Network for the Improvement of Banana and Plantain (INIBAP) for use within the framework of the Global Musa Genomics Consortium is acknowledged. The research conducted at the Katholieke Universiteit Leuven was supported via an agreement with INIBAP by a grant of the Belgian Directorate-General for Development Cooperation (DGDC).

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Authors and Affiliations

  1. Laboratory of Tropical Crop Improvement, Katholieke Universiteit Leuven, Kasteelpark Arenberg 13, 3001, Leuven, Belgium

    Bert Coemans, Serge Remy, Rony Swennen & László Sági

  2. Iwate Biotechnology Research Center, Narita 22-174-4, 024-0003, Kitakami, Iwate, Japan

    Hideo Matsumura & Ryohei Terauchi

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  1. Bert Coemans
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  2. Hideo Matsumura
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  3. Ryohei Terauchi
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  4. Serge Remy
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  5. Rony Swennen
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  6. László Sági
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Correspondence to Bert Coemans.

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Communicated by J. S. (Pat) Heslop-Harrison

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Coemans, B., Matsumura, H., Terauchi, R. et al. SuperSAGE combined with PCR walking allows global gene expression profiling of banana (Musa acuminata), a non-model organism. Theor Appl Genet 111, 1118–1126 (2005). https://doi.org/10.1007/s00122-005-0039-7

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