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Tree Genetics & Genomes

, Volume 4, Issue 3, pp 419–433 | Cite as

An EST database for Liriodendron tulipifera L. floral buds: the first EST resource for functional and comparative genomics in Liriodendron

  • Haiying Liang
  • John E. Carlson
  • James H. Leebens-Mack
  • P. Kerr Wall
  • Lukas A. Mueller
  • Matyas Buzgo
  • Lena L. Landherr
  • Yi Hu
  • D. Scott DiLoreto
  • Daniel C. Ilut
  • Dawn Field
  • Steven D. Tanksley
  • Hong Ma
  • Claude W. dePamphilis
Original Paper

Abstract

Liriodendron tulipifera L. was selected by the Floral Genome Project for identification of new genes related to floral diversity in basal angiosperms. A large, non-normalized cDNA library was constructed from premeiotic and meiotic floral buds and sequenced to generate a database of 9,531 high-quality expressed sequence tags. These sequences clustered into 6,520 unigenes, of which 5,251 were singletons, and 1,269 were in contigs. Homologs of genes regulating many aspects of flower development were identified, including those for organ identity and development, cell and tissue differentiation, and cell-cycle control. Almost 5% of the transcriptome consisted of homologs to known floral gene families. Homologs of most of the genes involved in cell-wall construction were also recovered. This provides a new opportunity for comparative studies in lignin biosynthesis, a trait of key importance in the evolution of land plants and in the utilization of fiber from economically important tree species, such as Liriodendron. Also of note is that 1,089 unigenes did not match any sequence in the public databases, including the complete genomes of Arabidopsis, rice, and Populus. Some of these novel genes might be unique in basal angiosperm species and, when better characterized, may be informative for understanding the origins of diverged gene families. Thus, the Liriodendron expressed sequence tag database and library will help bridge our understanding of the mechanisms of flower initiation and development that are shared among basal angiosperms, eudicots, and monocots, and provide new opportunities for comparative analysis of gene families across angiosperm species.

Keywords

EST database Flower development Liriodendron tulipifera Magnoliaceae Basal angiosperm 

Abbreviations

ABI

Applied Biosystems

AP

APETALA gene

bp

base pairs

DEPC

diethylpyrocarbonate

EF-1

Elongation Factor 1-alpha gene

EST

expressed sequence tag

GO

Gene Ontology Consortium

Ks

rate of synonymous substitutions

MYB

myeloblastosis-like gene

PCR

polymerase chain reaction

RCA

rolling-circle amplification

Notes

Acknowledgements

We thank David Oppenheimer and his lab for guidance on the in situ hybridization experiments. We thank the tree-improvement field crew at the University of Tennessee at Knoxville for collecting, freezing, and shipping the tissue samples used for RNA extraction. We thank Sheila Plock for assistance with manipulations and curation of the cDNA library, and Marlin Druckenmiller in the Schatz Center for Tree Molecular Genetics at Penn State for assistance in high throughput sequencing. The Floral Genome Project was supported by a grant to C. dePamphilis and co-PIs from the NSF Plant Genome Research Program (DBI-0115684). Dr. Liang was supported by a post-doctoral fellowship from The Schatz Center for Tree Molecular Genetics.

Supplementary material

11295_2007_120_MOESM1_ESM.doc (5.6 mb)
Table S1 The annotations for the strongest BLASTx alignments from GenBank to the 4468 Ltu01 unigenes for matches with similarity (e) values <1e-5) (DOC 5.57 Mb)

References

  1. Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Ann Rev Plant Biol 54:519–549CrossRefGoogle Scholar
  2. Buzgo M, Liang H, Schlarbaum SE, DiLoreto DS, Carlson J, Soltis PS, Soltis DE (2006) Floral development in Liriodendron tulipifera L. (Magnoliaceae) and other basal angoisperms. In: Botany 2006, California State University, Chico, CA, USA, July 28–August 3, 2006; Presentation 617Google Scholar
  3. Cai Z, Penaflor C, Kuehl JV, Leebens-Mack J, Carlson JE, dePamphilis CW, Boore JL, Jansen RK (2006) Complete plastid genome sequences of Drimys, Liriodendron, and Piper: implications for the phylogenetic relationships of magnoliids. BMC Evol Biol 6:77PubMedCrossRefGoogle Scholar
  4. Cans C, Passer BJ, Shalak V, Nancy-Portebois V, Crible V, Amzallag N, Allanic D, Tufino R, Argentini M, Moras D, Fiucci G, Goud B, Mirande M, Amson R, Telerman A (2003) Translationally controlled tumor protein acts as a guanine nucleotide dissociation inhibitor on the translation elongation factor eEF1A. Proc Natl Acad Sci U S A 100:13892–13897PubMedCrossRefGoogle Scholar
  5. Carlson JE, Leebens-Mack JH, Wall PK, Zahn LM, Mueller LA, Landherr LL, Hu Y, Ilut DC, Arrington JM, Choirean S, Becker A, Field D, Tanksley SD, Ma H, dePamphilis CW (2006) EST database for early flower development in California poppy (Eschscholzia californica Cham., Papaveraceae) tags over 6,000 genes from a basal eudicot. Plant Mol Biol 62:351–369PubMedCrossRefGoogle Scholar
  6. Cui L, Wall PK, Leebens-Mack JH, Lindsay BG, Soltis DE, Doyle JJ, Soltis PS, Carlson JE, Arumuganathan K, Barakat A, Albert VA, Ma H, dePamphilis CW (2006) Widespread genome duplications throughout the history of flowering plants. Genome Res 16:738–749PubMedCrossRefGoogle Scholar
  7. Drews GN, Bowman JL, Meyerowitz EM (1991) Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell 65:991−1002PubMedCrossRefGoogle Scholar
  8. Endress PK, Igersheim A (2000) Gynoecium structure and evolution in basal angiosperms. Intl J Plant Sci 161:S211–S223CrossRefGoogle Scholar
  9. Glasser WG, Kaar WE, Jain RK, Sealey JE (2000) Isolation options for non-cellulosic heteropolysaccharides (HetPS). Cellulose 7:299–317CrossRefGoogle Scholar
  10. Hayward TK, Hamilton J, Tholudur A, Mc Millan JD (2000) Improvements in titer, productivity, and yield using solka-floc for cellulase production. Appl Biochem and Biotech 84–86:859–874CrossRefGoogle Scholar
  11. Hunt D (1998) Magnolias and their allies. International Dendrology Society & Magnolia Society, EnglandGoogle Scholar
  12. Jackson DP (1991) In situ hybridization in plants. In: Bowles DJ, Gurr SJ, McPhereson M (eds) Molecular Plant Pathology: A Practical Approach. Oxford University Press, Oxford, pp 163–174Google Scholar
  13. Jansen RK, Cai Z, Raubeson LA, Daniell H, dePamphilis CW, Leebens-Mack J, Müller KF, Guisinger-Bellian M, Haberle RC, Hansen AK, Chumley TW, Lee S-B, Peery R, McNeal J, Kuehl JV, Boore JL (2007) Analysis of 81 genes from 64 chloroplast genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc Natl Acad Sci USA (in press)Google Scholar
  14. Kim HJ, Hyun Y, Park JY, Park MJ, Park MK, Kim MD, Kim HJ, Lee MH, Moon J, Lee I, Kim J (2004) A genetic link between cold responses and flowering time through FVE in Arabidopsis thaliana. Nat Genet 36:167–171PubMedCrossRefGoogle Scholar
  15. Kim KH, Tucker MP, Keller FA, Aden A, Nguyen QA (2001) Continuous countercurrent extraction of hemicellulose from pretreated wood residues. Appl Biochem Biotechnol 91/93:253–268CrossRefGoogle Scholar
  16. Kong H, Landherr LL, Frohlich MW, Leebens-Mack J, Ma H, dePamphilis CW (2007) Patterns of gene duplication in the plant SKP1 gene family in angiosperms: evidence for multiple mechanisms of rapid gene birth. Plant J 50:873–885PubMedCrossRefGoogle Scholar
  17. Liang H, Fang EG, Tomkins JP, Luo M, Kudrna D, Arumuganathan K, Zhao S, Schlarbaum SE, Banks JA, dePamphilis CW, Mandoli DF, Wing RA, Carlson JE (2007) Development of a BAC library resource for yellow poplar (Liriodendron tulipifera) and the identification of genomic regions associated with flower development and lignin biosynthesis. Tree Genet Genomes 3:215–225CrossRefGoogle Scholar
  18. Lynn K, Fernandez A, Aida M, Sedbrook J, Tasaka M, Masson P, Barton MK (1999) The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis development and has overlapping functions with the ARGONAUTE1 gene. Development 126:469–481PubMedGoogle Scholar
  19. Kim SB, Lee YY (2002) Diffusion of sulfuric acid within lignocellulosic biomass particles and its impact on dilute-acid pretreatment. Bioresour Technol 83:165–71PubMedCrossRefGoogle Scholar
  20. Ma H (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Bio 56:393–434CrossRefGoogle Scholar
  21. Merkle SA (2006) Engineering forest trees with heavy metal resistance genes. Silvae Genet 55:263–268Google Scholar
  22. Nagle NJ, Elander RT, Newman MM, Rohrback BT, Ruiz RO, Torget RW (2002) Efficacy of a hot washing process for pretreated yellow poplar to enhance bioethanol production. Biotechnol Prog 18:734–738PubMedCrossRefGoogle Scholar
  23. Nakamura Y, Gojobori T, Ikemura T (2000) Codon usage tabulated from international DNA sequence databases: status for the year 2000. Nucl Acids Res 28:292PubMedCrossRefGoogle Scholar
  24. Newman KL, Fernandez AG, Barton MK (2002) Regulation of Axis Determinacy by the Arabidopsis PINHEAD. Gene Plant Cell 14:3029–3042CrossRefGoogle Scholar
  25. Parks CR, Wendel JF (1990) Molecular divergence between Asian and North American species of Liriodendron (Magnoliaceae) with implications for interpretation of fossil floras. Am J Bot 77:1243–1256CrossRefGoogle Scholar
  26. Ronse de Craene L, Soltis DE, Soltis PS (2003) Evolution of floral structures in basal angiosperms. Intl J Plant Sci 164:S329–363CrossRefGoogle Scholar
  27. Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–67PubMedCrossRefGoogle Scholar
  28. Soltis DE, Soltis PS, Chase MW, Mort ME, Albach DC, Zanis M, Savolainen V, Hahn WH, Hoot SB, Fay MF, Axtell M, Swensen SM, Prince LM, Kress WJ, Nixon KC, Farris JS (2000) Angiosperm phylogeny inferred from a combined data set of 18S rDNA, rbcL and atpB sequences. Bot J Linn Soc 133:381–461Google Scholar
  29. Soltis DE, Soltis PS, Albert VA, Oppenheimer DG, dePamphilis CW, Ma H, Frohlich MW, Theissen G (2002) Missing links: the genetic architecture of flower and floral diversification. Trends Plant Sci 7:22–31PubMedCrossRefGoogle Scholar
  30. Soltis DE, Soltis PS, Chase MW, Endress P (2005) Phylogeny, evolution, and classification of flowering plants. Sinauer Associates, Sunderland, MAGoogle Scholar
  31. Somerville C, Somerville S (1999) Plant functional genomics. Science 285:380–383PubMedCrossRefGoogle Scholar
  32. Vavelidis M, Melfos V, Boboti-Tsitlakidis I (1997) A new occurrence of placer gold in the Marathousa area (central Macedonia, N. Greece). In: Papunen H (ed) Mineral deposits: research and exploration, where do they meet? Proceedings of the Fourth Biennial SGA Meeting, Turku, Finland, 11–13 August, 1997. A.A. Balkema, Rotterdam, pp 339–342Google Scholar
  33. Wall PK, Leebens-Mack JH, Muller K, Field D, Altman NS, dePamphilis CW (2007) PlantTribes: A gene and gene family resource for comparative genomics in plants. Nucl Acids Res (in press)Google Scholar
  34. Wang J-PZ, Lindsay BG, Leebens-Mack J, Cui L, Wall K, Miller WC, dePamphilis CW (2004) EST clustering error evaluation and correction. Bioinformatics 20:2973–2984PubMedCrossRefGoogle Scholar
  35. Wen J (1999) Evolution of eastern Asian and eastern North American disjunct distributions in flowering plants. Annu Rev Ecol Syst 30:421–455CrossRefGoogle Scholar
  36. Wilde HD, Meagher RB, Merkle SA (1992) Expression of foreign genes in transgenic yellow-poplar plants. Plant Physiol 98:114–120PubMedCrossRefGoogle Scholar
  37. Xu M, Ruddall P (2006) Comparative floral anatomy and ontogeny in Magnoliaceae. Plant Syst Evol 258:1–15CrossRefGoogle Scholar
  38. Xu M, Li H, Zhang B (2006) Fifteen polymorphic simple sequence repeat markers from expressed sequence tags of Liriodendron tulipifera. Mol Ecol Notes 6:728–730CrossRefGoogle Scholar
  39. Yoo MJ, Albert VA, Soltis PS, Soltis DE (2006) Phylogenetic diversification of glycogen synthase kinase 3/SHAGGY-like kinase genes in plants. BMC Plant Biol 6:3PubMedCrossRefGoogle Scholar
  40. Zahn LM, Kong H, Leebens-Mack JH, Kim S, Soltis PS, Landherr LL, Soltis D, dePamphilis CW, Ma H (2005a) The evolution of the SEPALLATA subfamily of MADS-box genes: a pre-angiosperm origin with multiple duplications throughout angiosperm history. Genetics 169:2209–2223PubMedCrossRefGoogle Scholar
  41. Zahn LM, Leebens-Mack J, dePamphilis CW, Ma H, Theissen G (2005b) To B or Not to B a flower: the role of DEFICIENS and GLOBOSA orthologs in the evolution of the angiosperms. J Heredity 96:225–240CrossRefGoogle Scholar
  42. Zahn LM, Feng B, Fu MH (2006) Beyond the ABC model: Regulation of floral homeotic genes. In: Soltis DE, Soltis PS, Leebens-Mack JH (eds) Developmental Genetics of the Flower, Advances in Botanical Research. vol. 44. Elsevier, London, pp 163–207Google Scholar
  43. Zhang X, Dyachok J, Krishnakumar S, Smith LG, Oppenheimer DG (2005) IRREGULAR TRICHOME BRANCH1 in Arabidopsis encodes a plant homolog of the actin-related protein2/3 complex activator Scar/WAVE that regulates actin and microtubule organization. Plant Cell 17:2314–2326PubMedCrossRefGoogle Scholar
  44. Zhao D, Yu Q, Chen C, Ma H (2001) Genetic control of reproductive meristems. In: McManus MT, Veit B (eds) Meristematic Tissues in Plant Growth and Development. Sheffield Academic Press, pp 89–142Google Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Haiying Liang
    • 1
    • 6
  • John E. Carlson
    • 1
  • James H. Leebens-Mack
    • 2
    • 7
  • P. Kerr Wall
    • 2
  • Lukas A. Mueller
    • 3
  • Matyas Buzgo
    • 4
    • 8
  • Lena L. Landherr
    • 2
  • Yi Hu
    • 2
  • D. Scott DiLoreto
    • 1
  • Daniel C. Ilut
    • 3
  • Dawn Field
    • 5
  • Steven D. Tanksley
    • 3
  • Hong Ma
    • 2
  • Claude W. dePamphilis
    • 2
  1. 1.School of Forest Resources, the Huck Institutes of the Life SciencesPennsylvania State UniversityUniversity ParkUSA
  2. 2.Department of Biology, the Huck Institutes of the Life SciencesPennsylvania State UniversityUniversity ParkUSA
  3. 3.Department of Plant BreedingCornell UniversityIthacaUSA
  4. 4.Department of BotanyUniversity of FloridaGainesvilleUSA
  5. 5.Oxford Centre for Ecology and HydrologyOxfordUK
  6. 6.Department of Genetics and BiochemistryClemson UniversityClemsonUSA
  7. 7.Department of Plant BiologyUniversity of GeorgiaAthensUSA
  8. 8.Department of BiologyUniversity of Louisiana in ShreveportShreveportUSA

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