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Chapman · Jiancheng Chang · David Weisman · Rick V Theor Appl Genet DOI 10.1007/s00122-007-0605-2 ORIGINAL PAPER Universal markers for comparative mapping and phylogenetic analysis in the Asteraceae (Compositae) Mark A. Chapman · JianCheng Chang · David Weisman · Rick V. Kesseli · John M. Burke Received: 3 April 2007 / Accepted: 30 June 2007 © Springer-Verlag 2007 Abstract The development of universal markers that can sequenced a subset of ten loci from a panel of cultivated be assayed across taxa, but which are polymorphic within saZower individuals. All 10 loci proved to be single-locus, taxa, can facilitate both comparative map-based studies and and nine of the 10 loci were polymorphic with an average phylogenetic analyses. Here we describe the development of 12.8 SNPs per kb. Taken together, these loci will provide of such markers for use in the Asteraceae, which includes an initial backbone for comparative genetic analyses within the crops lettuce, sunXower, and saZower as well as dozens the Asteraceae. Moreover, our results indicate that these of locally important crop and weed species. Using align- loci are phylogenetically informative, and hence can be ments of a conserved orthologous set (COS) of ESTs from used to resolve evolutionary relationships between taxa lettuce and sunXower and genomic sequences of Arabidop- within the family as well as within species. sis, we designed a suite of primer pairs that are conserved across species, but which are predicted to Xank introns. We then tested 192 such primer pairs in 8 species from across Introduction the family. Of these, 163 produced an amplicon in at least 1 taxon, and 125 ampliWed in at least half of the taxa sur- The Weld of comparative genomics relies upon the identiW- veyed. Thirty-nine ampliWed in all 8 species. Comparisons cation of orthologous genes and genomic regions between amongst sequences within the lettuce and sunXower EST the species of interest. Mapping of these orthologous databases indicate that the vast majority of these loci will regions in diVerent species provides insight into the extent be polymorphic. As a direct test of the utility of these mark- of synteny, and can facilitate the map-based cloning of ers outside the lettuce and sunXower subfamilies, we genes of interest (Gale and Devos 1998b; Paterson et al. 2000). Comparative genetic maps have been produced for a number of plant species; the majority of these are for crops Communicated by M. Xu. with extensive linkage maps often containing thousands of mapped loci. Thus far, the largest eVorts have focused on Mark A. Chapman and JianCheng Chang have contributed equally to the Solanaceae (Bonierbale et al. 1988; Livingstone et al. this work. 1999; Doganlar et al. 2002), Brassicaceae (Kowalski et al. Electronic supplementary material The online version of this 1994; Lagercrantz and Lydiate 1996; Lagercrantz et al. article (doi:10.1007/s00122-007-0605-2) contains supplementary 1996; Lagercrantz 1998; Lan and Paterson 2000), Fabaceae material, which is available to authorized users. (Choi et al. 2006; Kalo et al. 2004), Rosaceae (Dirlewanger et al. 2004), and Poaceae (Lin et al. 1995; Paterson et al. M. A. Chapman (&) · J. M. Burke Department of Plant Biology, Miller Plant Sciences Building, 1995; Maroof et al. 1996; Gale and Devos 1998a; Ming University of Georgia, Athens, GA 30602, USA et al. 1998; Wu et al. 2003; Bowers et al. 2005). Recent e-mail: [email protected] studies have revealed the potential of extending these anal- yses to comparisons of taxa from diVerent families; how- J. Chang · D. Weisman · R. V. Kesseli Department of Biology, University of Massachusetts, ever, such studies are generally restricted to localized Boston, 100 Morrissey Blvd, Boston, MA 02125, USA regions and/or microsyntenic analyses based on the full 123 Theor Appl Genet genome sequence of Arabidopsis thaliana (e.g., Grant et al. introgressive hybridization (e.g., Soltis and KuzoV 1995; 2000; Ku et al. 2001; Lee et al. 2001; Bowers et al. 2003; Okuyama et al. 2005). Finally, the lack of recombination in Dominguez et al. 2003; Timms et al. 2006). the chloroplast genome means that a phylogenetic investi- Early comparative mapping projects relied on hybridiza- gation based on multiple cpDNA sequences is little more tion-based assays of probes from one species against the than an analysis of one ‘super-locus’. The use of multiple, genome of another (Tanksley et al. 1992; Prince et al. 1993; unlinked nuclear loci, on the other hand, results in a Van Deynze et al. 1998; Fulton et al. 2002). Using this genome-wide phylogenetic signal that is more likely to reX- strategy, the pairing gene Ph from wheat and Xowering ect true species relationships (Small et al. 2004). time genes in Brassica were isolated based on the known In contrast to a cpDNA-based approach, phylogenetic genomic locations in other species (Foote et al. 1997; studies using nuclear DNA sequences have traditionally Osborn et al. 1997; Axelsson et al. 2001; Kole et al. 2001; been hampered by the lack of sequence information avail- GriYths et al. 2006). More recently, PCR-based markers able for the design of universal primers and diYculties dis- have been developed for comparative mapping in a range of tinguishing between orthologous and paralogous sequences species (Fourmann et al. 2002; Choi et al. 2006; Feltus (Soltis and Soltis 1998; Small et al. 2004). Consequently, et al. 2006; Fredslund et al. 2006; Wu et al. 2006). Ideally, nuclear DNA phylogenies have relied heavily on the such markers should utilize primers that anneal to highly sequence of the two internal transcribed spacers (ITS) of conserved regions of genes (e.g., exons) such that the same the nuclear ribosomal DNA (Alvarez and Wendel 2003), primers can be used in a range of related species. In addi- with only a handful of other nuclear genes/gene families tion, these primers should Xank a variable region of the having been used for phylogenetic inference, although the genome (e.g., introns) such that polymorphism can be list is continually growing (e.g., Strand et al. 1997; detected within species, allowing the loci to be mapped. reviewed in Small et al. 2004). Beyond their utility for comparative genomic analyses, Previous studies have shown that anchoring primers in readily-transferable nuclear DNA markers could also be of conserved orthologs can provide markers for comparative great value for assessing phylogenetic relationships (Doyle mapping in birds, mammals, and insects (Lyons et al. 1997; and Gaut 2000; Small et al. 2004). For phylogenetic recon- Smith et al. 2000; Chambers et al. 2003) and these same struction, DNA sequencing is the most widely chosen tech- markers are suitable for phylogenetic investigations (e.g., nique. Universal markers for phylogenetics should be Roca et al. 2001; Gaines et al. 2005). The recent availabil- designed with similar goals as those for comparative map- ity of the whole genome sequence of Arabidopsis and large ping: the primers must anneal to highly conserved gene expressed sequence tag (EST) databases for a growing regions; however, depending on the scale of the phyloge- number of plant species have provided the potential to align netic analysis, the internal portion of the amplicon should DNA sequences from multiple species, and to identify a be more variable. Currently the majority of universal conserved orthologous set (COS) of low or single-copy primer pairs available that amplify across families of Xow- genes (Fulton et al. 2002) that could be useful for compara- ering plants are speciWc to the chloroplast genome tive mapping studies and phylogenetic analyses. Wu et al. (reviewed in Small et al. 2004). (2006) expanded on this concept to identify COS loci from While comparing chloroplast DNA (cpDNA) gene six species of the euasterids, and homology was suYcient sequences is useful at higher taxonomic scales (Chase et al. within the euasterid I clade (tomato, potato, pepper and 1993; Kim and Jansen 1995), these genes do not usually coVee) to allow primer design for ampliWcation across spe- provide suYcient resolution for the analysis of more cies within this clade. closely related taxa; hence, intergenic chloroplast regions To date, there are no such universal nuclear markers or introns are used (e.g., Taberlet et al. 1991; Hamilton available for use in the Asteraceae (Compositae). This is 1999) because of their higher rate of nucleotide substitution despite the family comprising one-tenth of all Xowering (Gielly and Taberlet 1994). There are, however, problems plants, and including a number of major and minor crops associated with the sole use of organellar markers to such as lettuce, sunXower, saZower, globe artichoke, and resolve phylogenies. For example, the rate of cpDNA chicory, as well as numerous ecologically-important taxa sequence evolution is approximately one fourth that of including many weedy and invasive species (Funk et al. nuclear DNA (Wolfe et al. 1987), and thus even intergenic 2005; Kesseli and Michelmore 1997). To remedy this situa- sequences may not provide suYcient resolution between tion, we aligned ESTs deWned as COS loci from two phylo- closely related species. Further, because cpDNA is unipa- genetically distant members of the family, sunXower rentally inherited in the majority of species, it cannot (Helianthus annuus L.) and lettuce (Lactuca sativa L.), resolve relationships in taxa that have evolved via hybrid- with coding sequences from Arabidopsis. Primers were ization or allopolyploidy. It is also possible for chloroplast designed to anneal to highly conserved exon regions and to haplotypes to be transferred from one taxon to another via Xank putative introns based on their known positions in 123 Theor Appl Genet Arabidopsis. These primer pairs should be suitable for Carduoideae (Carthamus tinctorius L. and Centaurea mac- comparative mapping in crops such as sunXower, lettuce, ulosa Lam.) and Cichorioideae (Lactuca sativa L. and and saZower or globe artichoke, which represent the three Cichorium intybus L.) were chosen, plus four members of major subfamilies of the Asteraceae, as well as in phyloge- the largest subfamily, the Asteroideae (Senecio squalidus netic investigations at lower taxonomic levels.
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