Tree Genetics & Genomes

, Volume 6, Issue 3, pp 357–365 | Cite as

Analysis of expressed sequence tags from Ginkgo mature foliage in China

  • Yi-Qiang Wang
  • Ji-Kang Shen
  • Torkel Berglund
  • Anna B. Ohlsson
  • Xiao-Feng Tang
  • Zhai-Kui Zhou
  • Ruo-Yan Wu
  • Xiao-Hui Zhou
  • Jie-Nan Chen
Original Paper

Abstract

Ginkgo biloba L. is a tree native to China, which has large importance within medicine and horticulture. The extracts from Ginkgo mature leaves with rich flavonoids and terpenoids are commonly used for a variety of folk remedies. We constructed a cDNA library derived from mature leaves of Ginkgo, which consisted of 8.12 × 105 clones with the insert length of 500–2,000 bp. We performed an analysis of expressed sequence tags (ESTs) and obtained partial sequences from 2,039 clones, which represented 1,437 unigenes consisting of 249 contigs and 1,188 singletons. The 2,039 ESTs were submitted to GenBank (dbEST) at NCBI and were assigned GenBank accession numbers from GE647881 to GE649919. The 1,235 cDNA clones out of 2,039 (60.1%) were assigned putative functions, and the remaining 804 clones were not similar to any known gene sequences in the databases. The five largest categories of Ginkgo clones were: “energy” (19.4%), “disease/defense” (16%), “metabolism” (11.3%), “unclassified proteins” (12.5%), and "secondary metabolism" (9%). The highly expressed transcripts in the cDNA library were some genes related to photosynthesis, disease/defense, and flavonoid biosynthesis, including ribulose–bisphosphate carboxylase small-chain gene, pathogenesis-related protein gene, light-harvesting chlorophyll a/b binding protein of photosystem gene, catalase gene, and phenylcoumaran benzylic ether reductase gene et al. Many genes with ESTs similar to photosynthesis, secondary metabolism, and stress-response genes were characterized. The analysis of ESTs indicates that it is a useful approach for isolating Ginkgo genes homologous to known genes. Our results provide new information about mature leaf-specific transcripts of Ginkgo.

Keywords

Mature foliage cDNA library Expressed sequence tags Ginkgo 

Abbreviations

contigs

Contiguous consensus sequences

CTAB

Cetyl trimethyl ammonium bromide

ESTs

Expressed sequence tags

FunCat

Functional categories

References

  1. Allona I, Quinn M, Shoop E, Swope K, Cyr SS, Carlis J, Riedel J, Retzel E, Campbell MM, Sederoff R, Whetten RW (1998) Analysis of xylem formation in pine by cDNA sequencing. Proc Natl Acad Sci USA 95:9693–9698CrossRefPubMedGoogle Scholar
  2. Balz JP, Courtois D, Drieu J, Drieu K, Reynoird JP, Sohier C, Teng BP, Touché A, Pétiard V (1999) Production of ginkgolides and bilobalide by Ginkgo biloba plants and tissue cultures. Planta Med 65:620–626CrossRefPubMedGoogle Scholar
  3. Begley TP, Downs DM, Ealick SE, McLafferty FW, Campobasso N, Chiu HJ, Kinsland C, Reddick JJ, Xi J (1999) Thiamin biosynthesis in prokaryotes. Arch Microbiol 171:293–300CrossRefPubMedGoogle Scholar
  4. Bradbeer JW (1969) The activities of the photosynthetic carbon cycle enzymes of greening bean leaves. New Phytol 68:233–245CrossRefGoogle Scholar
  5. Brenner ED, Katari MS, Stevenson DW, Rudd SA, Douglas AW, Moss WN, Twigg RW, Runko SJ, Stellari GM, McCombie WR, Coruzzi GM (2005) EST analysis in Ginkgo biloba: an assessment of conserved developmental regulators and gymnosperm specific genes. BMC Genomics 6:143CrossRefPubMedGoogle Scholar
  6. Chang SJ, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Report 11:113–116CrossRefGoogle Scholar
  7. Cooke R, Raynal M, Laudie M, Grellet F, Delseny M, Morris P-C, Guerrier D, Giraudat J, Quigley F, Clabault G, Li YF, Mache R, Krivitzky M, Gy IJJ, Kreis M, Lecharny A, Parmentier Y, Marbach J, Fleck J, Clément B, Philipps G, Hervé C, Bardet C, Tremousaygue D, Lescure B, Lacomme C, Roby D, Jourjon MF, Chabrier P, Charpenteau JL, Desprez T, Amselem J, Chiapello H, Höfte H (1996) Further progress towards a catalogue of all Arabidopsis genes: analysis of a set of 5000 non-redundant ESTs. Plant J 9:101–124CrossRefPubMedGoogle Scholar
  8. Crafts-Brandner SJ, Salvucci ME (2000) Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. PNAS 97:13430–13435CrossRefPubMedGoogle Scholar
  9. Curtis-Prior P, Vere D, Fray P (1999) Therapeutic value of Ginkgo biloba in reducing symptoms of decline in mental function. J Pharm Pharmacol 51:535–541CrossRefPubMedGoogle Scholar
  10. DeFeudis FV (1998) Ginkgo biloba extract (EGb 761): from chemistryto clinic. Ullstein Med, WiesbadenGoogle Scholar
  11. Dixon RA, Steele CL (1999) Flavonoids and isoflavonoids-a gold mine for metabolic engineering. Trends Plant Sci 4:394–400CrossRefPubMedGoogle Scholar
  12. Ewing B, Hillier L, Wendl MC, Green P (1998) Base-calling of automated sequencer traces using Phred. I. Accuracy assessment. Genome Res 8:175–185PubMedGoogle Scholar
  13. Ferrer JL, Austin MB, Stewart C, Noel JP (2008) Structure and function of enzymes involved in the biosynthesis of phenylpropanoids. Plant physiol biochem 46:356–370CrossRefPubMedGoogle Scholar
  14. Gold PE, Cahill L, Wenk GL (2003) The lowdown on Ginkgo biloba. Sci Am 288:86–91CrossRefPubMedGoogle Scholar
  15. Hori T, Ridge RW, Tulecke W, Del Tredici P, Tremouillaux-Guiller J, Tobe H (1997) Ginkgo biloba—a global treasure. Springer, TokyoGoogle Scholar
  16. Huang XQ, Madan A (1999) CAP3: A DNA sequence assembly program. Genome Res 9:868–877CrossRefPubMedGoogle Scholar
  17. Kang SM, Min JY, Kim YD, Karigar CS, Kim SW, Goo GH, Choi MS (2009) Effect of abiotic elicitors on the accumulation of bilobalide and ginkgolides in Ginkgo biloba cell cultures. J Biotechnol 139:84–88CrossRefPubMedGoogle Scholar
  18. Kirst M, Johnson AF, Baucom C, Ulrich E, Hubbard K et al (2003) Apparent homology of expressed genes from wood-forming tissues of loblolly pine (Pinus taeda L.) with Arabidopsis thaliana. Proc Natl Acad Sci USA 100:7383–7388CrossRefPubMedGoogle Scholar
  19. Koiwa H, Bressan RA, Hasegawa PM (1997) Regulation of protease inhibitors and plant defense. Trends Plant Sci 2:379–384CrossRefGoogle Scholar
  20. Lawrence PK, Koundal KR (2002) Plant protease inhibitors in control of phytophagous insects. EJB Electron J Biotechnol 5:1–17Google Scholar
  21. Li XP, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395CrossRefPubMedGoogle Scholar
  22. Liu X, Deng Z, Gao S, Sun X, Tang K (2007) Molecular cloning and characterization of a glutathione S-transferase gene from Ginkgo biloba. DNA Seq 18:371–379CrossRefPubMedGoogle Scholar
  23. Masoudi-Nejad A, Tonomura K, Kawashima MY, Suzuki M, Itoh M, Kanehisa M, Endo GS (2006) EGassembler online bioinformatics service for large-scale processing, clustering and assembling ESTs and genomic DNA fragments. Nucleic Acids Res 34:459–462CrossRefGoogle Scholar
  24. Nadimpalli R, Yalpani N, Johal GS, Simmons CR (2000) Prohibitins, stomatins, and plant disease response genes compose a protein puperfamily that controls cell proliferation, ion channel regulation, and death. J. Biol. Chem 275:29579–29586CrossRefPubMedGoogle Scholar
  25. Ogihara Y, Mochida K, Nemoto Y, Murai K, Yamazaki Y, Shin IT (2003) Correlated clustering and virtual display of gene expression patterns in the wheat life cycle by large-scale statistical analyses of expressed sequence tags. Plant J 33:1001–1011CrossRefPubMedGoogle Scholar
  26. Papageorgiou GC, Murata N (1995) The unusually strong stabilizing effects of glycine betaine on the structure and function of the oxygen-evolving Photosystem II complex. Photosynth Res 44:243–252CrossRefGoogle Scholar
  27. Park YS, Kwak JM, Kwon OY, Kim YS, Lee DS, Cho MJ et al (1993) Generation of expressed sequence tags of random root cDNA clones of Brassica napus by single-run partial sequencing. Plant Physiol 103:359–370CrossRefPubMedGoogle Scholar
  28. Pavy N, Laroche J, Bousquet J, Mackay J (2005) Large-scale statistical analysis of secondary xylem ESTs in pine. Plant Mol Biol 57:203–224CrossRefPubMedGoogle Scholar
  29. Penning TM, Drury JE (2007) Human aldo–keto reductases: function, gene regulation, and single nucleotide polymorphisms. Arch Biochem Biophys 464:241–250CrossRefPubMedGoogle Scholar
  30. Pollack JR, Perou CM, Alizadeh AA, Eisen MB, Pergamenschikov A, Williams C, Jeffrey SS, Botstein D, Brown PO (1999) Genome-wide analysis of DNA copy-number changes using cDNA microarrays. Nat Genet 23:41–46CrossRefPubMedGoogle Scholar
  31. Ronning CM, Stegalkina SS, Ascenzi RA, Bougri O, Hart AL, Utterbach TR et al (2003) Comparative analyses of potato expressed sequence tag libraries. Plant Physiol 131:419–429CrossRefPubMedGoogle Scholar
  32. Rothwell GW, Holt B (1997) Fossils and phenology in the evolution of Ginkgo biloba. In: Hori T, Ridge RW, Tulecke W, Tredici PD, Trémouillaux-Guiller J, Tobe H (eds) Ginkgo biloba—a global treasure. Springer, Tokyo, pp 223–230Google Scholar
  33. Ruepp A, Zollner A, Maier D, Albermann K, Hani J, Mokrejs M, Tetko I, Güldener U, Mannhaupt G, Münsterkötter M, Mewes HW (2004) The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res 32:5539–5545CrossRefPubMedGoogle Scholar
  34. Shen B, Carneiro N, Torres-Jerez I, Stevenson B, McCreery T, Helentjaris T, Baysdorfer C, Almira E, Ferl RJ, Habben JE, Larkins B (1994) Partial sequencing and mapping of clones from two maize cDNA libraries. Plant Mol Biol 26:1085–1101CrossRefPubMedGoogle Scholar
  35. Shen G, Pang Y, Wu W, Deng Z, Zhao L, Cao Y, Sun X, Tang K (2006) Cloning and characterization of a flavanone 3-hydroxylase gene from Ginkgo biloba. Biosci Rep 26:19–29CrossRefPubMedGoogle Scholar
  36. Skribanek A, Solvmosi K, Hideg É, Böddi B (2008) Light and temperature regulation of greening in dark-grown Ginkgo. Physiol Plant 134:649–659CrossRefPubMedGoogle Scholar
  37. Sterky F, Regan S, Karlsson J, Hertzberg M, Rohde A, Holmberg A, Amini B, Balerao R, Larsson M, Villarroel R, Montagu MV, Sandberg G, Olssen O, Teeri TT, Boerjan W, Gustafsson P, Uhlén M, Sundberg B, Lundeberg J (1998) Gene discovery in the wood-forming tissues of poplar: analysis of 5,692 expressed sequence tags. Proc Natl Acad Sci USA 95:13330–13335CrossRefPubMedGoogle Scholar
  38. Sun YK, Li WK, Fitzloff JF, Breemen RB (2005) Liquid chromatography–electrospray tandem mass spectrometry of terpenoid lactones in Ginkgo biloba. J Mass Spectrom 40:373–379CrossRefPubMedGoogle Scholar
  39. Ujino-Ihara T, Yoshimura K, Ugawa Y, Yoshimaru H, Nagasaka K, Tsumura Y (2000) Expression analysis of ESTs derived from the inner bark of Cryptomeria japonica. Plant Mol Biol 43:451–457CrossRefPubMedGoogle Scholar
  40. Ujino-Ihara T, Kanamori H, Yamane H, Taguchi Y, Namiki N, Mukai Y, Yoshimura K, Tsumura Y (2005) Comparative analysis of expressed sequence tags of conifers and angiosperms reveals sequences specifically conserved in conifers. Plant Mol Biol 59:895–907CrossRefPubMedGoogle Scholar
  41. Wang GX, Cao FL, Chen J (2006) Progress in researches on the pharmaceutical mechanism and clinical application of Ginkgo biloba extract on various kinds of diseases. Chin J Integr Med 12:234–239CrossRefPubMedGoogle Scholar
  42. Whitney SM, Andrews TJ (2001) The gene for the ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) small subunit relocated to the plastid genome of tobacco directs the synthesis of small subunits that assemble into Rubisco. Plant Cell 13:193–205CrossRefPubMedGoogle Scholar
  43. Xing SY, Wu DJ, Xing LF, You XL, Zhang YP, Sun X, Liu YQ (2002) Quantitative genetic analysis and multiple trait selection of pharmaceutical composition on Ginkgo biloba L. leaves. Yi Chuan Xue Bao 29:928–935PubMedGoogle Scholar
  44. Yamamoto K, Sasaki T (1997) Large-scale EST sequencing in rice. Plant Mol Biol 35:135–144CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Yi-Qiang Wang
    • 1
  • Ji-Kang Shen
    • 1
  • Torkel Berglund
    • 2
  • Anna B. Ohlsson
    • 2
  • Xiao-Feng Tang
    • 3
  • Zhai-Kui Zhou
    • 4
  • Ruo-Yan Wu
    • 1
  • Xiao-Hui Zhou
    • 1
  • Jie-Nan Chen
    • 4
  1. 1.School of Life Science and BiotechnologyCentral South University of Forestry and TechnologyChangshaChina
  2. 2.School of BiotechnologyRoyal Institute of Technology (KTH)StockholmSweden
  3. 3.Key Laboratory of Non-timber Forest Breeding and Cultivation of National Forestry MinistryCentral South University of Forestry and TechnologyChangshaChina
  4. 4.Institute of Biological and Environmental Science and TechnologyCentral South University of Forestry and TechnologyChangshaChina

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