Skip to main content
Log in

Universal markers for comparative mapping and phylogenetic analysis in the Asteraceae (Compositae)

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

The development of universal markers that can be assayed across taxa, but which are polymorphic within taxa, can facilitate both comparative map-based studies and phylogenetic analyses. Here we describe the development of such markers for use in the Asteraceae, which includes the crops lettuce, sunflower, and safflower as well as dozens of locally important crop and weed species. Using alignments of a conserved orthologous set (COS) of ESTs from lettuce and sunflower and genomic sequences of Arabidopsis, we designed a suite of primer pairs that are conserved across species, but which are predicted to flank introns. We then tested 192 such primer pairs in 8 species from across the family. Of these, 163 produced an amplicon in at least 1 taxon, and 125 amplified in at least half of the taxa surveyed. Thirty-nine amplified in all 8 species. Comparisons amongst sequences within the lettuce and sunflower EST databases indicate that the vast majority of these loci will be polymorphic. As a direct test of the utility of these markers outside the lettuce and sunflower subfamilies, we sequenced a subset of ten loci from a panel of cultivated safflower individuals. All 10 loci proved to be single-locus, and nine of the 10 loci were polymorphic with an average of 12.8 SNPs per kb. Taken together, these loci will provide an initial backbone for comparative genetic analyses within the Asteraceae. Moreover, our results indicate that these loci are phylogenetically informative, and hence can be used to resolve evolutionary relationships between taxa within the family as well as within species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alvarez I, Wendel JF (2003) Ribosomal ITS sequences and plant phylogenetic inference. Mol Phylogenet Evol 29:417–434

    Article  PubMed  CAS  Google Scholar 

  • Axelsson T, Shavorskaya O, Lagercrantz U (2001) Multiple flowering time QTLs within several Brassica species could be the result of duplicated copies of one ancestral gene. Genome 44:856–864

    Article  CAS  Google Scholar 

  • Baldwin BG (1993) Molecular Phylogenetics of Calycadenia (Compositae) based on ITS sequences of nuclear ribosomal DNA—chromosomal and morphological evolution reexamined. Am J Bot 80:222–238

    Article  CAS  Google Scholar 

  • Bonierbale MW, Plaisted RL, Tanksley SD (1988) RFLP maps based on a common set of clones reveal modes of chromosomal evolution in potato and tomato. Genetics 120:1095–1103

    PubMed  Google Scholar 

  • Bowers JE, Abbey C, Anderson S, Chang C, Draye X, Hoppe AH, Jessup R, Lemke C, Lennington J, Li ZK, Lin YR, Liu SC, Luo LJ, Marler BS, Ming RG, Mitchell SE, Qiang D, Reischmann K, Schulze SR, Skinner DN, Wang YW, Kresovich S, Schertz KF, Paterson AH (2003) A high-density genetic recombination map of sequence-tagged sites for Sorghum, as a framework for comparative structural and evolutionary genomics of tropical grains and grasses. Genetics 165:367–386

    PubMed  CAS  Google Scholar 

  • Bowers JE, Arias MA, Asher R, Avise JA, Ball RT, Brewer GA, Buss RW, Chen AH, Edwards TM, Estill JC, Exum HE, Goff VH, Herrick KL, Steele CLJ, Karunakaran S, Lafayette GK, Lemke C, Marler BS, Masters SL, McMillan JM, Nelson LK, Newsome GA, Nwakanma CC, Odeh RN, Phelps CA, Rarick EA, Rogers CJ, Ryan SP, Slaughter KA, Soderlund CA, Tang HB, Wing RA, Paterson AH (2005) Comparative physical mapping links conservation of microsynteny to chromosome structure and recombination in grasses. Proc Natl Acad Sci USA 102:13206–13211

    Article  PubMed  CAS  Google Scholar 

  • Burke JM, Lai Z, Salmaso M, Nakazato T, Tang S, Heesacker A, Knapp SJ, Rieseberg LH (2004) Comparative mapping and rapid karyotypic evolution in the genus Helianthus. Genetics 167:449–457

    Article  PubMed  CAS  Google Scholar 

  • Chambers EW, Lovin DD, Severson DW (2003) Utility of comparative anchor-tagged sequences as physical anchors for comparative genome analysis among the Culicidae. Am J Trop Med Hyg 69:98–104

    PubMed  CAS  Google Scholar 

  • Chapman B, Chang J (2000) Biopython: python tools for computational biology. ACM SIGBIO Newsl 20:15–19

    Article  Google Scholar 

  • Chase MW, Soltis DE, Olmstead RG, Morgan D, Les DH, Mishler BD, Duvall MR, Price RA, Hills HG, Qiu YL, Kron KA, Rettig JH, Conti E, Palmer JD, Manhart JR, Sytsma KJ, Michaels HJ, Kress WJ, Karol KG, Clark WD, Hedren M, Gaut BS, Jansen RK, Kim KJ, Wimpee CF, Smith JF, Furnier GR, Strauss SH, Xiang QY, Plunkett GM, Soltis PS, Swensen SM, Williams SE, Gadek PA, Quinn CJ, Eguiarte LE, Golenberg E, Learn GH, Graham SW, Barrett SCH, Dayanandan S, Albert VA (1993) Phylogenetics of seed plants—an analysis of nucleotide sequences from the plastid gene RbcL. Ann Mo Bot Gard 80:528–580

    Article  Google Scholar 

  • Choi HK, Luckow MA, Doyle J, Cook DR (2006) Development of nuclear gene-derived molecular markers linked to legume genetic maps. Mol Genet Genomics 276:56–70

    Article  PubMed  CAS  Google Scholar 

  • Dirlewanger E, Graziano E, Joobeur T, Garriga-Caldere F, Cosson P, Howad W, Arus P (2004) Comparative mapping and marker-assisted selection in Rosaceae fruit crops. Proc Natl Acad Sci USA 101:9891–9896

    Article  PubMed  CAS  Google Scholar 

  • Doganlar S, Frary A, Daunay MC, Lester RN, Tanksley SD (2002) A comparative genetic linkage map of eggplant (Solanum melongena) and its implications for genome evolution in the Solanaceae. Genetics 161:1697–1711

    PubMed  CAS  Google Scholar 

  • Dominguez I, Graziano E, Gebhardt C, Barakat A, Berry S, Arus P, Delseny M, Barnes S (2003) Plant genome archaeology: evidence for conserved ancestral chromosome segments in dicotyledonous plant species. Plant Biotechnol J 1:91–99

    Article  PubMed  CAS  Google Scholar 

  • Doyle JJ, Gaut BS (2000) Evolution of genes and taxa: a primer. Plant Mol Biol 42:1–23

    Article  PubMed  CAS  Google Scholar 

  • Feltus FA, Singh HP, Lohithaswa HC, Schulze SR, Silva TD, Paterson AH (2006) A comparative genomics strategy for targeted discovery of single-nucleotide polymorphisms and conserved-noncoding sequences in orphan crops. Plant Physiol 140:1183–1191

    Article  PubMed  CAS  Google Scholar 

  • Foote T, Roberts M, Kurata N, Sasaki T, Moore G (1997) Detailed comparative mapping of cereal chromosome regions corresponding to the Ph1 locus in wheat. Genetics 147:801–807

    PubMed  CAS  Google Scholar 

  • Fourmann M, Barret P, Froger N, Baron C, Charlot F, Delourme R, Brunel D (2002) From Arabidopsis thaliana to Brassica napus: development of amplified consensus genetic markers (ACGM) for construction of a gene map. Theor Appl Genet 105:1196–1206

    Article  PubMed  CAS  Google Scholar 

  • Fredslund J, Schauser L, Madsen LH, Sandal N, Stougaard J (2005) PriFi: using a multiple alignment of related sequences to find primers for amplification of homologs. Nucleic Acids Res 33:W516–W520

    Article  PubMed  CAS  Google Scholar 

  • Fredslund J, Madsen LH, Hougaard BK, Nielsen AM, Bertioli D, Sandal N, Stougaard J, Schauser L (2006) A general pipeline for the development of anchor markers for comparative genomics in plants. BMC Genomics 7:207

    Article  PubMed  CAS  Google Scholar 

  • Fulton TM, Van der Hoeven R, Eannetta NT, Tanksley SD (2002) Identification, analysis, and utilization of conserved ortholog set markers for comparative genomics in higher plants. Plant Cell 14:1457–1467

    Article  PubMed  CAS  Google Scholar 

  • Funk VA, Bayer RJ, Keeley S, Chan R, Watson L, Gemeinholzer B, Schilling EE, Panero JL, Baldwin BG, Garcia-Jacas N, Susanna A, Jansen R (2005) Everywhere but Antarctica: using a supertree to understand the diversity and distribution of the Compositae. Biol Skr 55:343–374

    Google Scholar 

  • Gaines CA, Hare MP, Beck SE, Rosenbaum HC (2005) Nuclear markers confirm taxonomic status and relationships among highly endangered and closely related right whale species. Proc R Soc Lond B 272:533–542

    Article  CAS  Google Scholar 

  • Gale MD, Devos KM (1998a) Comparative genetics in grasses. Proc Natl Acad Sci USA 95:1971–1974

    Article  PubMed  CAS  Google Scholar 

  • Gale MD, Devos KM (1998b) Plant comparative genetics after ten years. Science 282:656–658

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Jacas N, Susanna A, Garnatje T, Vilatersana R (2001) Generic delimitation and phylogeny of the subtribe Centaureinae (Asteraceae): a combined nuclear and chloroplast DNA analysis. Ann Bot 87:503–515

    Article  CAS  Google Scholar 

  • Gielly L, Taberlet P (1994) The use of chloroplast DNA to resolve plant phylogenies - noncoding versus RbcL sequences. Mol Biol Evol 11:769–777

    PubMed  CAS  Google Scholar 

  • Grant D, Cregan P, Shoemaker RC (2000) Genome organization in dicots: genome duplication in Arabidopsis and synteny between soybean and Arabidopsis. Proc Natl Acad Sci USA 97:4168–4173

    Article  PubMed  CAS  Google Scholar 

  • Griffiths S, Sharp R, Foote TN, Bertin I, Wanous M, Reader S, Colas I, Moore G (2006) Molecular characterization of Ph1 as a major chromosome pairing locus in polyploid wheat. Nature 439:749–752

    Article  PubMed  CAS  Google Scholar 

  • Hamilton MB (1999) Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Mol Ecol 8:521–523

    PubMed  CAS  Google Scholar 

  • Kalo P, Seres A, Taylor SA, Jakab J, Kevei Z, Kereszt A, Endre G, Ellis THN, Kiss GB (2004) Comparative mapping between Medicago sativa and Pisum sativum. Mol Genet Genomics 272:235–246

    Article  PubMed  CAS  Google Scholar 

  • Kesseli R, Michelmore RM (1997) The Compositae: systematically fascinating but specifically neglected. In: Paterson AH (ed) Genome mapping of Plants. R.G. Landes Co., Georgetown, pp 179–191

    Google Scholar 

  • Kim KJ, Jansen RK (1995) NdhF sequence evolution and the major clades in the sunflower family. Proc Natl Acad Sci USA 92:10379–10383

    Article  PubMed  CAS  Google Scholar 

  • Kole C, Quijada P, Michaels SD, Amasino RM, Osborn TC (2001) Evidence for homology of flowering-time genes VFR2 from Brassica rapa and FLC from Arabidopsis thaliana. Theor Appl Genet 102:425–430

    Article  CAS  Google Scholar 

  • Kopp A, True JR (2002) Phylogeny of the oriental Drosophila melanogaster species group: a multilocus reconstruction. Syst Biol 51:786–805

    Article  PubMed  Google Scholar 

  • Kowalski SP, Lan TH, Feldmann KA, Paterson AH (1994) Comparative mapping of Arabidopsis thaliana and Brassica oleracea chromosomes reveals islands of conserved organization. Genetics 138:499–510

    PubMed  CAS  Google Scholar 

  • Ku HM, Vision T, Liu JP, Tanksley SD (2000) Comparing sequenced segments of the tomato and Arabidopsis genomes: large-scale duplication followed by selective gene loss creates a network of synteny. Proc Natl Acad Sci USA 97:9121–9126

    Article  PubMed  CAS  Google Scholar 

  • Ku HM, Liu JP, Doganlar S, Tanksley SD (2001) Exploitation of Arabidopsis-tomato synteny to construct a high-resolution map of the ovate-containing region in tomato chromosome 2. Genome 44:470–475

    Article  PubMed  CAS  Google Scholar 

  • Lagercrantz U (1998) Comparative mapping between Arabidopsis thaliana and Brassica nigra indicates that Brassica genomes have evolved through extensive genome replication accompanied by chromosome fusions and frequent rearrangements. Genetics 150:1217–1228

    PubMed  CAS  Google Scholar 

  • Lagercrantz U, Lydiate DJ (1996) Comparative genome mapping in Brassica. Genetics 144:1903–1910

    PubMed  CAS  Google Scholar 

  • Lagercrantz U, Putterill J, Coupland G, Lydiate D (1996) Comparative mapping in Arabidopsis and Brassica, fine scale genome collinearity and congruence of genes controlling flowering time. Plant J 9:13–20

    Article  PubMed  CAS  Google Scholar 

  • Lai Z, Livingstone K, Zou Y, Church SA, Knapp SJ, Andrews J, Rieseberg LH (2005) Identification and mapping of SNPs from ESTs in sunflower. Theor Appl Genet 111:1532–1544

    Article  PubMed  CAS  Google Scholar 

  • Lan T-H, Paterson AH (2000) Comparative mapping of quantiative trait loci sculpting the curd of Brassica oleracea. Genetics 155:1927–1954

    PubMed  CAS  Google Scholar 

  • Lee JM, Grant D, Vallejos CE, Shoemaker RC (2001) Genome organization in dicots. II. Arabidopsis as a ‘bridging species’ to resolve genome evolution events among legumes. Theor Appl Genet 103:765–773

    Article  CAS  Google Scholar 

  • Lin Y-R, Schertz KF, Paterson AH (1995) Comparative analysis of QTLs affecting plant height and maturity across the Poaceae, in reference to an interspecific sorghum mapping population. Genetics 141:391–411

    PubMed  CAS  Google Scholar 

  • Livingstone KD, Lackney VK, Blauth JR, van Wijk R, Jahn MK (1999) Genome mapping in Capsicum and the evolution of genome structure in the Solanaceae. Genetics 152:1183–1202

    PubMed  CAS  Google Scholar 

  • Lyons LA, Laughlin TF, Copeland NG, Jenkins NA, Womack JE, Obrien SJ (1997) Comparative anchor tagged sequences (CATS) for integrative mapping of mammalian genomes. Nat Genet 15:47–56

    Article  PubMed  CAS  Google Scholar 

  • Maroof MAS, Yang GP, Biyashev RM, Maughan PJ, Zhang Q (1996) Analysis of the barley and rice genomes by comparative RFLP linkage mapping. Theor Appl Genet 92:541–551

    Article  Google Scholar 

  • Ming R, Liu SC, Lin YR, da Silva J, Wilson W, Braga D, van Deynze A, Wenslaff TF, Wu KK, Moore PH, Burnquist W, Sorrells ME, Irvine JE, Paterson AH (1998) Detailed alignment of Saccharum and Sorghum chromosomes: comparative organization of closely related diploid and polyploid genomes. Genetics 150:1663–1682

    PubMed  CAS  Google Scholar 

  • Okuyama Y, Fujii N, Wakabayashi M, Kawakita A, Ito M, Watanabe M, Murakami N, Kato M (2005) Nonuniform concerted evolution and chloroplast capture: heterogeneity of observed introgression patterns in three molecular data partition phylogenies of Asian Mitella (Saxifragaceae). Mol Biol Evol 22:285–296

    Article  PubMed  CAS  Google Scholar 

  • Osborn TC, Kole C, Parkin IAP, Sharpe AG, Kuiper M, Lydiate DJ, Trick M (1997) Comparison of flowering time genes in Brassica rapa, B. napus and Arabidopsis thaliana. Genetics 146:1123–1129

    PubMed  CAS  Google Scholar 

  • Paterson AH, Lin Y-R, Li Z, Schertz KF, Doebley JF, Pinson SRM, Liu S-C, Stansel JW, Irvine JE (1995) Convergent domestication of cereal crops by independent mutations at corresponding genetic loci. Science 269:1714–1718

    Article  PubMed  CAS  Google Scholar 

  • Paterson AH, Bowers JE, Burow MD, Draye X, Elsik CG, Jiang CX, Katsar CS, Lan TH, Lin YR, Ming RG, Wright RJ (2000) Comparative genomics of plant chromosomes. Plant Cell 12:1523–1539

    Article  PubMed  CAS  Google Scholar 

  • Prince JP, Pochard E, Tanksley SD (1993) Construction of a molecular linkage map of pepper and a comparison of synteny with tomato. Genome 36:404–417

    Article  CAS  PubMed  Google Scholar 

  • Rieseberg LH, Van Fossen C, Desrochers AM (1995) Hybrid speciation accompanied by genomic reorganization in wild sunflowers. Nature 375:313–316

    Article  CAS  Google Scholar 

  • Roca AL, Georgiadis N, Pecon-Slattery J, O’Brien SJ (2001) Genetic evidence for two species of elephant in Africa. Science 293:1473–1477

    Article  PubMed  CAS  Google Scholar 

  • Rokas A, Carroll SB (2005) More genes or more taxa? The relative contribution of gene number and taxon number to phylogenetic accuracy. Mol Biol Evol 22:1337–1344

    Article  PubMed  CAS  Google Scholar 

  • Rokas A, Williams BL, King N, Carroll SB (2003) Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425:798–804

    Article  PubMed  CAS  Google Scholar 

  • Roy SW, Fedorov A, Gilbert W (2003) Large-scale comparison of intron positions in mammalian genes shows intron loss but no gain. Proc Natl Acad Sci USA 100:7158–7162

    Article  PubMed  CAS  Google Scholar 

  • Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Small RL, Cronn RC, Wendel JF (2004) Use of nuclear genes for phylogeny reconstruction in plants. Aust Syst Bot 17:145–170

    Article  CAS  Google Scholar 

  • Smith E, Shi L, Drummond P, Rodriguez L, Hamilton R, Powell E, Nahashon S, Ramlal S, Smith G, Foster J (2000) Development and characterization of expressed sequence tags for the turkey (Meleagris gallopavo) genome and comparative sequence analysis with other birds. Anim Genet 31:62–67

    Article  PubMed  CAS  Google Scholar 

  • Soltis DE, Kuzoff RK (1995) Discordance between nuclear and chloroplast phylogenies in the Heuchera group (Saxifragaceae). Evolution 49:727–742

    Article  Google Scholar 

  • Soltis DE, Soltis PS (1998) Choosing an approach and an appropriate gene for phylogenetic analysis. In: Soltis DE, Soltis PM, Doyle JJ (eds) Molecular systematics of plants. II. DNA sequencing. Kluwer Academic Publishers, Boston, pp 1–42

    Google Scholar 

  • Strand AE, Leebens-Mack J, Milligan BG (1997) Nuclear DNA-based markers for plant evolutionary biology. Mol Ecol 6:113–118

    Article  PubMed  CAS  Google Scholar 

  • Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of 3 noncoding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109

    Article  PubMed  CAS  Google Scholar 

  • Tanksley SD, Ganal MW, Prince JP, Devicente MC, Bonierbale MW, Broun P, Fulton TM, Giovannoni JJ, Grandillo S, Martin GB, Messeguer R, Miller JC, Miller L, Paterson AH, Pineda O, Roder MS, Wing RA, Wu W, Young ND (1992) High-density molecular linkage maps of the tomato and potato genomes. Genetics 132:1141–1160

    PubMed  CAS  Google Scholar 

  • Timms L, Jimenez R, Chase M, Lavelle D, McHale L, Kozik A, Lai Z, Heesacker A, Knapp S, Rieseberg L, Michelmore R, Kesseli R (2006) Analyses of synteny between Arabidopsis thaliana and species in the Asteraceae reveal a complex network of small syntenic segments and major chromosomal rearrangements. Genetics 173:2227–2235

    Article  PubMed  CAS  Google Scholar 

  • Van Deynze AE, Sorrells ME, Park WD, Ayres NM, Fu H, Cartinhour SW, Paul E, McCouch SR (1998) Anchor probes for comparative mapping of grass genera. Theor Appl Genet 97:356–369

    Article  Google Scholar 

  • Vilatersana R, Susanna A, Garcia-Jacas N, Garnatje T (2000) Generic delimitation and phylogeny of the Carduncellus-Carthamus complex (Asteraceae) based on ITS sequences. Plant Syst Evol 221:89–105

    Article  CAS  Google Scholar 

  • Wolfe KH, Li WH, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci USA 84:9054–9058

    Article  PubMed  CAS  Google Scholar 

  • Wu XL, Larson SR, Hu ZM, Palazzo AJ, Jones TA, Wang RRC, Jensen KB, Chatterton NJ (2003) Molecular genetic linkage maps for allotetraploid Leymus wildryes (Gramineae: Triticeae). Genome 46:627–646

    Article  PubMed  CAS  Google Scholar 

  • Wu FN, Mueller LA, Crouzillat D, Petiard V, Tanksley SD (2006) Combining bioinformatics and phylogenetics to identify large sets of single-copy orthologous genes (COSII) for comparative, evolutionary and systematic studies: A test case in the euasterid plant clade. Genetics 174:1407–1420

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

EST sequence data were obtained from the Compositae Genome Project website. This work was supported by grants from the National Science Foundation (DBI-0421630 to RVK and DBI-0332411 to JMB), the NSF Research Experience for Undergraduates Program (DBI-0354125 to UMass Boston) and the United States Department of Agriculture (03-35300-13104 to JMB). Comments from members of our lab groups improved an earlier version of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mark A. Chapman.

Additional information

Communicated by M. Xu.

Mark A. Chapman and JianCheng Chang have contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

122_2007_605_MOESM1_ESM.xls

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chapman, M.A., Chang, J., Weisman, D. et al. Universal markers for comparative mapping and phylogenetic analysis in the Asteraceae (Compositae). Theor Appl Genet 115, 747–755 (2007). https://doi.org/10.1007/s00122-007-0605-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-007-0605-2

Keywords

Navigation