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EST database for early flower development in California poppy (Eschscholzia californica Cham., Papaveraceae) tags over 6000 genes from a basal eudicot

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Abstract

The Floral Genome Project (FGP) selected California poppy (Eschscholzia californica Cham. ssp. Californica) to help identify new florally-expressed genes related to floral diversity in basal eudicots. A large, non-normalized cDNA library was constructed from premeiotic and meiotic floral buds and sequenced to generate a database of 9079 high quality Expressed Sequence Tags (ESTs). These sequences clustered into 5713 unigenes, including 1414 contigs and 4299 singletons. Homologs of genes regulating many aspects of flower development were identified, including those for organ identity and development, cell and tissue differentiation, cell cycle control, and secondary metabolism. Over 5% of the transcriptome consisted of homologs to known floral gene families. Most are the first representatives of their respective gene families in basal eudicots and their conservation suggests they are important for floral development and/or function. App. 10% of the transcripts encoded transcription factors and other regulatory genes, including nine genes from the seven major lineages of the important MADS-box family of developmental regulators. Homologs of alkaloid pathway genes were also recovered, providing opportunities to explore adaptive evolution in secondary products. Furthermore, comparison of the poppy ESTs with the Arabidopsis genome provided support for putative Arabidopsis genes that previously lacked annotation. Finally, over 1800 unique sequences had no observable homology in the public databases. The California poppy EST database and library will help bridge our understanding of flower initiation and development among higher eudicot and monocot model plants and provide new opportunities for comparative analysis of gene families across angiosperm species.

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Abbreviations

ABI:

Applied Biosystems

AG :

AGAMOUS gene

AGL :

AGAMOUS-like gene

AP :

APETALA gene

DEF :

DEFICIENS gene

DEPC:

diethylpyrocarbonate

EF-1-α:

Elongation Factor 1-alpha gene

ESca :

Eschscholzia californica

EST:

Expressed Sequence Tag

FIM :

FIMBRIATA gene

FLO :

FLORICAULA gene

GO:

Gene Ontology Consortium

GLO :

GLOBOSA gene

Ks:

rate of synonymous substitutions

LFY :

LEAFY gene

Mbp:

Million base pairs

MYA:

Million years ago

MYB :

myeloblastosis-like gene

NCBI:

National Center for Biotechnology Information

PCR:

polymerase chain reaction

PGN:

Plant Genome Network

PI :

PISTILLATA gene

PLE :

PLENA gene

rRNA:

ribosomal RNA

RACE:

Rapid Amplification of cDNA Ends

RCA:

Rolling Circle Amplification

RuBisCO :

ribulose-1;5-bisphosphate carboxylase; ssp., species

TAIR:

The Arabidopsis Information Resource web site

References

  • Albert VA, Soltis DE, Carlson JE, Farmerie WG, Wall PK, Ilut DC, Mueller LA, Landherr LL, Hu Y, Buzgo M, Kim S, Yoo M-J, Frohlich MW, Perl-Treves R, Schlarbaum S, Bliss B, Tanksley S, Oppenheimer DG, Soltis PS, Ma H, dePamphilis CW, Leebens-Mack JH (2005) Floral gene resources from basal angiosperms for comparative genomics research. BMC Plant Biol 5:5

    Article  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  PubMed  CAS  Google Scholar 

  • Angenent GC, Franken J, Busscher M, Colombo L, van Tunen AJ (1993) Petal and stamen formation in petunia is regulated by the homeotic gene fpg1. Plant J 4:101–112

    Article  PubMed  CAS  Google Scholar 

  • Angenent GC, Franken J, Busscher M, Weiss D, van Tunen AJ (1994) Co-suppression of the petunia homeotic gene fbp2 affects the identity of the generative meristem. Plant J 5:33–44

    Article  PubMed  CAS  Google Scholar 

  • Becker A, Saedler H, Theissen G (2003) Distinct MADS-box gene expression patterns in the reproductive cones of the gymnosperm Gnetum gnemon. Dev Genes Evol 213:567–572

    Article  PubMed  CAS  Google Scholar 

  • Becker S, Gleissbergy S, Smyth DR (2005) Floral and vegetative morphogenesis in California poppy (Eschscholzia californica Cham.). Int J Plant Sci 166:537–555

    Article  CAS  Google Scholar 

  • Bennett MD, Smith JB (1976) Nuclear DNA amounts in angiosperms. Phil Trans Royal Soc London B 274:227–274

    CAS  Google Scholar 

  • Bennett MD, Bhandol P, Leitch IJ (2000) Nuclear DNA amounts in angiosperms and their modern uses—807 new estimates. Annals Bot 86:859–909

    Article  CAS  Google Scholar 

  • Bennetzen JL, Coleman C, Liu R, Ma J, Ramakrishna W (2004) Consistent over-estimation of gene number in complex plant genomes. Curr Opion Plant Biol 7:732–736

    Article  CAS  Google Scholar 

  • Blanc G, Wolfe KH (2004) Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16:1667–1678

    Article  PubMed  CAS  Google Scholar 

  • Bradley D, Carpenter R, Sommer H, Hartley N, Coen E (1993) Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the PLENA locus of Antirrhinum. Cell 72:85–95

    Article  PubMed  CAS  Google Scholar 

  • Busch A, Gleissberg S (2003) EcFLO, a FLORICAULA-like gene from Eschscholzia californica is expressed during organogenesis at the vegetative shoot apex. Planta 217:841–848

    Google Scholar 

  • Castillo-Davis CI. (2005) The evolution of noncoding DNA: how much junk, how much func? Trends Genet 21:533–536

    Article  PubMed  CAS  Google Scholar 

  • Clark C (1993) Papaveraceae (poppy family). In: Hickman JC (ed) The jepson manual, University of California Press, Berkeley, CA

    Google Scholar 

  • Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37

    Article  PubMed  CAS  Google Scholar 

  • Coen ES, Romero JM, Doyle S, Elliott R, Murphy G, Carpenter R (1990) Floricaula—a homeotic gene required for flower development in Antirrhinum majus. Cell 63:1311–1322

    Article  PubMed  CAS  Google Scholar 

  • Cook SA (1962) Genetic system, variation, and adaptation in Eschscholzia californica. Evolution 16:278–299

    Google Scholar 

  • Decker G, Wanner G, Zenk MH, Lottspeich F (2000) Characterization of proteins in latex of the opium poppy (Papaver somniferum) using two-dimensional gel electrophoresis and microsequencing. Electrophoresis 21:3500–3516

    Article  PubMed  CAS  Google Scholar 

  • Ditta G, Pinyopich A, Robles P, Pelaz S, Yanofsky MF (2004) The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Curr Biol 14:1935–1940

    Article  PubMed  CAS  Google Scholar 

  • Endress PK (2004) Structure and relationships of basal relictual angiosperms. Aus Syst Bot 17:343–366

    Article  Google Scholar 

  • Flanagan CA, Ma H (1994) Spatially and temporally regulated expression of the MADs-Box gene AGL2 in wild-type and mutant Arabidopsis flowers. Plant Mol Biol 26:581–595

    Article  PubMed  CAS  Google Scholar 

  • Frick S, Kramell R, Schmidt J, Fist AJ, Kutchan TM (2005) Comparative qualitative and quantitative determination of alkaloids in narcotic and condiment Papaver somniferum cultivars. J Nat Prod 68:666–673

    Article  PubMed  CAS  Google Scholar 

  • Goldberg RB, Beals TP, Sanders PM (1993) Anther development: basic principles and practical applications. Plant Cell 5:1217–1229

    Article  PubMed  CAS  Google Scholar 

  • Goto K, Meyerowitz EM (1994) Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev 8:1548–1560

    PubMed  CAS  Google Scholar 

  • Groot EP, Sinha N, Gleissberg S (2005) Expression patterns of STM-like KNOX and Histone H4 genes in shoot development of the dissected-leaved basal eudicot plants Chelidonium majus and Eschscholzia californica (Papaveraceae). Plant Mol Biol 58:317–331

    Article  PubMed  CAS  Google Scholar 

  • Huang H, Tudor M, Weiss CA, Hu Y, Ma H (1995) The Arabidopsis MADs-Box gene AGL3 is widely expressed and encodes a sequence-specific DNA-binding protein. Plant Mol Biol 28:549–567

    Article  PubMed  CAS  Google Scholar 

  • Iseli C, Jongeneel CV, Bucher P (1999) ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. Proc Int Conf Intell Syst Mol Biol 1999:138–148

  • Kramer EM, Irish VF (1999) Evolution of genetic mechanisms controlling petal development. Nature 399:144–148

    Article  PubMed  CAS  Google Scholar 

  • Koch MA, Haubold B, Mitchell-Olds T (2000) Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol Biol Evol 17:1483–1498.

    Google Scholar 

  • Kutchan TM (1995) Alkaloid biosynthesis-the basis for metabolic engineering of medicinal plants. Plant Cell 7:1059–1070

    Article  PubMed  CAS  Google Scholar 

  • Lee J, Pedersen H (2001) Stable genetic transformation of Eschscholzia californica expressing synthetic green fluorescent proteins. Biotechnol Prog 17:247–251

    Article  PubMed  CAS  Google Scholar 

  • Lincoln C, Long J, Meyerowitz E (2002) http//www.its.caltech.edu/plantlab/protocols/insitu.htm, accessed August 27, 2004

  • Ma H (1994) The unfolding drama of flower development: recent results from genetic and molecular analyses. Genes Dev 8:745–756

    PubMed  CAS  Google Scholar 

  • Ma H (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 56:393–434

    Article  PubMed  CAS  Google Scholar 

  • Ma H (2006) A molecular portrait of Arabidopsis meiosis. In: The Arabidopsis Book. Somerville CR, Meyerowitz EM, Dangl J, Stitt M (eds), American Society of Plant Biologists, Rockville, MD, doi/10.1199/tab.0009, http://www.aspb.org/publications/arabidopsis/

  • Ma H, dePamphilis C (2000) The ABCs of floral evolution. Cell 101:5–8

    Article  PubMed  CAS  Google Scholar 

  • McInerney JO (1998) GCUA: general codon usage analysis. Bioinformatics 14:372–373

    Google Scholar 

  • Mandel MA, Yanofsky MF (1998) The Arabidopsis AGL9 MADS box gene is expressed in young flower primordial. Sex Plant Reprod 11:22–28

    Article  CAS  Google Scholar 

  • Memelink J (2004) Putting the opium in poppy to sleep. Nature Biotech 22:1526–1527

    Article  CAS  Google Scholar 

  • Nakamura Y, Gojobori T, Ikemura T (2000) Codon usage tabulated from international DNA sequence databases: status for the year 2000. Nucleic Acids Res 28:292

    Google Scholar 

  • Nanda KK, Sharma R (1976) Effects of gibberellic acid and cyclic 39,59-adenosine monophosphate on the flowering of Eschscholtzia californica Cham, a qualitative long day plant. Plant Cell Physiol 17:1093–1095

    Google Scholar 

  • Park S-U, Facchini PJ (2000a) Agrobacterium rhizogenes-mediated transformation of opium poppy, Papaver somniferum L., and California poppy, Eschscholzia californica Cham., root cultures. J Exp Bot 51:1005–1016

    Article  CAS  Google Scholar 

  • Park S-U, Facchini PJ (2000b) Agrobacterium-mediated genetic transformation of California poppy, Eschscholzia californica Cham., via somatic embryogenesis. Plant Cell Rep 19:1006–1012

    Article  CAS  Google Scholar 

  • Park S-U, Min, Yu M, Facchini PJ (2002) Antisense RNA-mediated suppression of benzophenanthridine alkaloid biosynthesis in transgenic cell cultures of California poppy. Plant Physiol 128:696–706

    Article  PubMed  CAS  Google Scholar 

  • Pelaz S, Ditta GS, Baumann E, Wisman E, Yanofsky MF (2000) B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405:200–203

    Article  PubMed  CAS  Google Scholar 

  • Sato F (2005) RNAi and functional genomics. Plant Biotech 22:431–442

    CAS  Google Scholar 

  • Sato F, Hashimoto T, Hachiya A, Tamura K, Choi K-B, Morishige T, Fujimoto H, Yamada Y (2001) Metabolic engineering of plant alkaloid biosynthesis. Proc Natl Acad Sci USA 98:367–372

    Article  PubMed  CAS  Google Scholar 

  • Savidge B, Rounsley SD, Yanofsky MF (1995) Temporal relationship between the transcription of two Arabidopsis MADS box genes and the floral organ identity genes. Plant Cell 7:721–733

    Article  PubMed  CAS  Google Scholar 

  • Schneider H, Schuettpelz E, Pryer KM, Cranfill R, Magallon S, Lupia R (2004) Ferns diversified in the shadow of angiosperms. Nature 428:553–557

    Article  PubMed  CAS  Google Scholar 

  • Schwarz-Sommer Z, Huijser P, Nacken W, Saedler H, Sommer H (1990) Genetic control of flower development in Antirrhinum majus. Science 250:931–936

    CAS  Google Scholar 

  • Simon R, Carpenter R, Doyle S, Coen E (1994) Fimbriata controls flower development by mediating between meristem and organ identity genes. Cell 78:99–107

    Article  PubMed  CAS  Google Scholar 

  • Smith TF, Waterman MS (1981) Identification of common molecular subsequences. J Mol Biol 147:195–197

    Article  PubMed  CAS  Google Scholar 

  • Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767

    Article  PubMed  CAS  Google Scholar 

  • Soltis D, Soltis P, Albert V, Oppenheimer D, Frohlich MW, dePamphilis CW, Ma H, Theissen G (2002) Missing links: the genetic architecture of flower and floral diversification. Trends Plant Sci 7:22–31

    Article  PubMed  CAS  Google Scholar 

  • Soltis PS, Soltis DE, Kim S, Chanderbali A, Buzgo M (2006) Modifications of the ABC model based on analyses of basal angiosperms. In: Soltis DE, Soltis PS, Leebens-Mack JH (eds) Developmental genetics of the flower. Advances in botanical research series. Elsevier Limited, London. In press

    Google Scholar 

  • Soltis PS, Soltis DE, Zanis MJ, Kim S (2000) Basal lineages of angiosperms: Relationships and implications for floral evolution. Int J Plant Sci 161:S97–S107

    Google Scholar 

  • Sommer H, Beltran J-P, Huijser P, Pape H, Lonnig W-E, Saedler H, Schwarz-Sommer Z (1990) Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus: the protein shows homology to transcription factors. EMBO J 9:605–613

    PubMed  CAS  Google Scholar 

  • Thomas SG, Franklin-Tong VE (2004) Self-incompatibility triggers programmed cell death in Papaver pollen. Nature 429:305–309

    Article  PubMed  CAS  Google Scholar 

  • Trémousaygue D, Garnier L, Bardet C, Dabos P, Hervé C, Lescure B (2003) Internal telomeric repeats and ‘TCP domain’ protein-binding sites co-operate to regulate gene expression in Arabidopsis thaliana cycling cells. Plant J 33:957–966

    Article  PubMed  Google Scholar 

  • Tremousaygue D, Manevski A, Bardet C, Lescure N, Lescure B (1999) Plant interstitial telomere motifs participate in the control of gene expression in root meristems. Plant J 20:553–562

    Article  PubMed  CAS  Google Scholar 

  • Tröbner W, Ramirez L, Motte P, Hue I, Huijser P, Lönnig W-E, Saedler H, Sommer H, Schwarz-Sommer Z (1992) GLOBOSA: a homeotic gene which interacts with DEFICIENS in the control of Antirrhinum floral organogenesis. EMBO J 11:4693–4704

    PubMed  Google Scholar 

  • Wakelin AM, Lister CE, Conner AJ (2003) Inheritance and biochemistry of pollen pigmentation in California poppy (Eschscholzia californica Cham.). Int J Plant Sci 164:867–875

    Article  CAS  Google Scholar 

  • Weigel D, Meyerowitz EM (1994) The ABCs of floral homeotic genes. Cell 78:203–209

    Article  PubMed  CAS  Google Scholar 

  • Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM (1992) LEAFY controls floral meristem identity in Arabidopsis. Cell 69:843–859

    Article  PubMed  CAS  Google Scholar 

  • Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13:555–556

    PubMed  CAS  Google Scholar 

  • Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM (1990) The protein encoded by the Arabidopsis homeotic gene AGAMOUS resembles transcription factors. Nature 346:35–43

    Article  PubMed  CAS  Google Scholar 

  • Zahn LM, Kong H, Leebens-Mack JH, Kim S, Soltis PS, Landherr LL, Soltis DE, 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

    Article  CAS  Google Scholar 

  • Zahn LM, Leebens-Mack J, Arrington JM, Hu Y, Landherr L, dePamphilis CW, Becker A, Theissen G, Ma H (2006) Conservation and divergence in the AGAMOUS subfamily of MADS-Box genes: evidence of independent sub- and neofunctionalization events. Evol Dev 8:30–45

    Article  PubMed  CAS  Google Scholar 

  • 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 Hered 96:225–240

    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

    Google Scholar 

  • 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. Academic Press, Sheffield, pp 89–142

    Google Scholar 

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Acknowledgements

We thank Michael Kosco and Yoshita Oza for assistance with preparations for the in situ hybridization experiments and A. Omeis for plant growth and care. 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. We also thank William Farmerie for his suggestions on sequencing procedures. The Floral Genome Project was supported by a grant to C. dePamphilis and co-PIs from the NSF Plant Genome Research Program (DBI-0115684), A. Becker was supported by a fellowship from the German Research Foundation (DFG, BE 2547/2-1) and the PGN database hosted by Cornell University was supported by NSF grants DBI-9872617 and DBI-0115684.

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Author notes

  1. Jennifer M. Arrington

    Present address: Department of Biology, Randolph-Macon Woman’s College, Lynchburg, VA, 24503, USA

  2. James H. Leebens-Mack

    Present address: Department of Plant Biology, University of Georgia, Plant Sciences Building, Athens, GA, 30602-7271, USA

Authors and Affiliations

  1. The School of Forest Resources and Huck Institutes for Life Sciences, Pennsylvania State University, 323 Forest Resources Building, University Park, PA, 16802, USA

    John E. Carlson

  2. Department of Biology, The Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA, 16802, USA

    James H. Leebens-Mack, P. Kerr Wall, Laura M. Zahn, Lena L. Landherr, Yi Hu, Jennifer M. Arrington, Stephanie Choirean, Hong Ma & Claude W. dePamphilis

  3. Department of Plant Breeding, Cornell University, Ithaca, NY, 14853, USA

    Lukas A. Mueller, Daniel C. Ilut & Steven D. Tanksley

  4. Evolutionary Developmental Genetics Group, University of Bremen, 28359, Bremen, Germany

    Annette Becker

  5. Oxford Centre for Ecology and Hydrology, Mansfield Road, Oxford, OX1 3SR, UK

    Dawn Field

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  1. John E. Carlson
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Correspondence to John E. Carlson.

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Carlson, J.E., Leebens-Mack, J.H., Wall, P.K. et al. EST database for early flower development in California poppy (Eschscholzia californica Cham., Papaveraceae) tags over 6000 genes from a basal eudicot. Plant Mol Biol 62, 351–369 (2006). https://doi.org/10.1007/s11103-006-9025-y

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