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.
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Abbreviations
- ABI:
-
Applied Biosystems
- AP :
-
APETALA gene
- bp:
-
base pairs
- DEPC:
-
diethylpyrocarbonate
- EF-1-α:
-
Elongation Factor 1-alpha gene
- EST:
-
expressed sequence tag
- GO:
-
Gene Ontology Consortium
- K s :
-
rate of synonymous substitutions
- MYB :
-
myeloblastosis-like gene
- PCR:
-
polymerase chain reaction
- RCA:
-
rolling-circle amplification
References
Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Ann Rev Plant Biol 54:519–549
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 617
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 6:77
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 100:13892–13897
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 62:351–369
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 16:738–749
Drews GN, Bowman JL, Meyerowitz EM (1991) Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell 65:991−1002
Endress PK, Igersheim A (2000) Gynoecium structure and evolution in basal angiosperms. Intl J Plant Sci 161:S211–S223
Glasser WG, Kaar WE, Jain RK, Sealey JE (2000) Isolation options for non-cellulosic heteropolysaccharides (HetPS). Cellulose 7:299–317
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 84–86:859–874
Hunt D (1998) Magnolias and their allies. International Dendrology Society & Magnolia Society, England
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 163–174
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)
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 36:167–171
Kim KH, Tucker MP, Keller FA, Aden A, Nguyen QA (2001) Continuous countercurrent extraction of hemicellulose from pretreated wood residues. Appl Biochem Biotechnol 91/93:253–268
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 50:873–885
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 3:215–225
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 126:469–481
Kim SB, Lee YY (2002) Diffusion of sulfuric acid within lignocellulosic biomass particles and its impact on dilute-acid pretreatment. Bioresour Technol 83:165–71
Ma H (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Bio 56:393–434
Merkle SA (2006) Engineering forest trees with heavy metal resistance genes. Silvae Genet 55:263–268
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 18:734–738
Nakamura Y, Gojobori T, Ikemura T (2000) Codon usage tabulated from international DNA sequence databases: status for the year 2000. Nucl Acids Res 28:292
Newman KL, Fernandez AG, Barton MK (2002) Regulation of Axis Determinacy by the Arabidopsis PINHEAD. Gene Plant Cell 14:3029–3042
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 77:1243–1256
Ronse de Craene L, Soltis DE, Soltis PS (2003) Evolution of floral structures in basal angiosperms. Intl J Plant Sci 164:S329–363
Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–67
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 133:381–461
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 7:22–31
Soltis DE, Soltis PS, Chase MW, Endress P (2005) Phylogeny, evolution, and classification of flowering plants. Sinauer Associates, Sunderland, MA
Somerville C, Somerville S (1999) Plant functional genomics. Science 285:380–383
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 339–342
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)
Wang J-PZ, Lindsay BG, Leebens-Mack J, Cui L, Wall K, Miller WC, dePamphilis CW (2004) EST clustering error evaluation and correction. Bioinformatics 20:2973–2984
Wen J (1999) Evolution of eastern Asian and eastern North American disjunct distributions in flowering plants. Annu Rev Ecol Syst 30:421–455
Wilde HD, Meagher RB, Merkle SA (1992) Expression of foreign genes in transgenic yellow-poplar plants. Plant Physiol 98:114–120
Xu M, Ruddall P (2006) Comparative floral anatomy and ontogeny in Magnoliaceae. Plant Syst Evol 258:1–15
Xu M, Li H, Zhang B (2006) Fifteen polymorphic simple sequence repeat markers from expressed sequence tags of Liriodendron tulipifera. Mol Ecol Notes 6:728–730
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 6:3
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 169:2209–2223
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 96:225–240
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 163–207
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 17:2314–2326
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 89–142
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.
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Communicated by A.E. Jeffery Dean
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Table S1Table S2Table S3
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)
The annotations for the strongest BLASTn alignments from GenBank to the 963 Ltu01 unigenes for matches with similarity (e) values <1e-5) (DOC 5.57 Mb)
Additional cell wall synthesis genes identified in Ltu01 (DOC 5.57 Mb)
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Liang, H., Carlson, J.E., Leebens-Mack, J.H. et al. An EST database for Liriodendron tulipifera L. floral buds: the first EST resource for functional and comparative genomics in Liriodendron . Tree Genetics & Genomes 4, 419–433 (2008). https://doi.org/10.1007/s11295-007-0120-2
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DOI: https://doi.org/10.1007/s11295-007-0120-2