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Systematics |
2Biosystematics Group, Wageningen University, Generaal Foulkesweg 37, 6703 BL Wageningen, The Netherlands
Received for publication November 28, 2000. Accepted for publication March 9, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: AFLPs • Asteraceae • Compositae • Lactuca • Lactuceae • lettuce • molecular phylogeny • phenetic relationships
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The taxonomic status of this species, the boundaries among L. sativa and close relatives, and the boundaries of the genus Lactuca L. s.l. (sensu lato) (Lactuceae, Asteraceae) itself have been the subject of controversy among taxonomists for many decades. One of the most widely used classifications today is that of Feráková (1977)
, comprising the European species of Lactuca. She subdivides the genus into four sections: Lactuca, Mulgedium (Cass.) C.B. Clarke, Lactucopsis (Schultz-Bip. ex Vis. et Panc.) Rouy., and Phaenixopus (Cass.) Benth. Section Lactuca is subdivided into the subsections Lactuca and Cyanicae DC. The subsection Lactuca comprises L. sativa, L. serriola L., L. altaica Fisch. et C.A. Mey., L. saligna L., L. virosa L., and L. livida Boiss. et Reut. Lactuca livida is closely related to L. virosa (Velasco Negueruela, 1981
). The species L. sativa, L. serriola, and L. altaica are closely related and probably conspecific (see Koopman et al., 1998
, for a discussion). The lesser known southwest Asian species L. aculeata Boiss. & Kotschy ex Boiss., L. scarioloides Boiss., L. azerbaijanica Rech., L. georgica Grossh., and the South-African species L. dregeana DC. are also closely related to L. sativa/serriola/altaica (Zohary, 1991
). These species could all be classified in Feráková's subsection Lactuca if her classification were to be extended to include non-European species. The species of subsect. Lactuca comprise the readily accessible part of the lettuce gene pool and form potentially valuable gene sources for lettuce breeding (Zohary, 1991
). Lactuca serriola, L. saligna, L. virosa, and to a lesser extent L. altaica are already commonly used as lettuce genitors. The Lactuca species outside subsect. Lactuca, as well as species from genera closely related to Lactuca, are interesting candidates for broadening the lettuce gene pool (Koopman et al., 1998
).
In a previous study, Koopman et al. (1998)
used ITS-1 (internal transcribed spacer-1) sequences to examine the relationships of species within or close to the lettuce gene pool. The study enabled straightforward conclusions on the generic and infrageneric boundaries of Lactuca, but was inconclusive as to the relationships among closely related species, e.g., within subsect. Lactuca. Koopman et al. (1998)
concluded that additional information from a more variable marker was needed to resolve these relationships. A study by Hill et al. (1996)
demonstrated that AFLPs (Vos et al., 1995
) are variable markers useful for studying relationships among closely related species of Lactuca. Therefore, in the present study we used AFLP markers to further elucidate the relationships among Lactuca species and species from related genera. Our study had four foci: (1) the distinction between L. sativa and L. serriola, (2) the distinction between L. serriola and the serriola-like species L. dregeana, L. altaica, and L. aculeata, (3) the position of L. saligna and L. virosa relative to these serriola-like species, and (4) the detection of clusters/clades of closely related species outside subsect. Lactuca.
Data were analyzed both phenetically and cladistically, and the validity of cladistic analysis of AFLP data was discussed. A subset of data was used to compare various combinations of similarity coefficients and clustering methods for phenetic analyses.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), representing 20 species of Lactuca and related genera. The species are listed in Table 1 according to the subtribal classification of Bremer (1994)
and the generic and specific classification of Feráková (1977)
and Iwatsuki et al. (1995)
. The choice of species, the major generic concepts in Lactuca and related genera, and the delimitation of Lactuca were discussed in Koopman et al. (1998)
. Details on the accessions were given in Koopman et al. (1998)
and on the website of the Centre for Genetic Resources, The Netherlands (CGN) at http://www.plant.wageningen-ur.nl/CGN. Each accession was represented by two plants. Voucher specimens of the plant material in rosette, bolting, and flowering stages were deposited at the Herbarium Vadense (WAG), supplemented with photographs of the plants in all three stages and with pappus preparations and fruit samples. All plants were grown under standard greenhouse conditions.
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AFLP analysis
The AFLP procedure was performed according to Van Eck et al. (1995)
with minor modifications. In the restriction/ligation reaction 
250 ng of genomic DNA was digested for 1 h at 37°C using 2.5 U (units) EcoRI, 2.5 U MseI, and 8 µL 5x restriction-ligation buffer (5x RL buffer) in a total volume of 40 µL. Restriction/ligation was continued for another 3 h after addition of 10 µL of ligation mixture (containing 5 pmol EcoRI adapter, 50 pmol MseI adapter, 1.0 µL 10 mmol/L ATP, 2.0 µL 5x RL buffer, and 1.0 U T4 DNA ligase). The subsequent selection of biotinylated restriction fragments with streptavidin-coated Dynabeads was replaced by a tenfold dilution of the restriction/ligation mixture with distilled water.
Preselective amplification was performed using the primers E01 (EcoRI + A) and M02 (MseI + C). The resulting product was diluted 50-fold with T0.1E buffer (10 mmol/L Tris pH 8.0, 0.1 mmol/L EDTA). The final restriction fragment amplification was performed using primers with three selective nucleotides. The EcoRI primer in this reaction was labeled with 33P. A pilot study was conducted to test ten primer combinations: E33/M59, E35/M48, E35/M49, E35/M59, E35/M60, E38/M54, E44/M48, E44/M49, E45/M48, and E45/M49. The test data set contained four plants of L. sativa, two plants of L. saligna, and one plant from each of the other species in Table 1. The AFLP fragments for this experiment were separated on a 0.35-mm sequence system (Gibco BRL/Life Technologies, Rockville, Maryland, USA) and visualized on Kodak X-OMAT LS Scientific Imaging Film (Eastman Kodak, Rochester, New York, USA). Selection of primer combinations was based on the number of bands per lane, the number of bands that were constant among the species, and the absence of very fat bands or smears. Primer combinations E35/M48 (EcoRI + ACA/MseI + CAC) and E35/M49 (EcoRI + ACA/MseI + CAG) were selected to generate the final data set. The AFLP procedure for E35/M48 was performed as above. For E35/M49, final restriction fragment amplification and separation and visualization of the AFLP fragments was performed according to Arens et al. (1998)
. Lactuca sativa ‘Norden’ served as size standard on each gel. A reference gel with fragment lengths of ‘Norden’ was kindly provided by Keygene N.V. (Wageningen, The Netherlands).
Data analysis
AFLP fragments were scored as present/absent. Fragment scoring and lane matching were performed automatically on digital images of the autoradiograms, using Phoretix 1D advanced Version 4.00 (Phoretix International, Newcastle upon Tyne, UK). All but the faintest bands were scored, where necessary scores and matches were corrected manually. Fragments scored ranged from 112 to 453 nucleotides for E35/M48 and from 111 to 502 nucleotides for E35/M49. Data from both primer combinations were combined in one data set. The data set was analyzed in two steps.
Firstly, a data subset was constructed comprising L. sativa and its closest relatives, L. serriola, L. dregeana, L. altaica, and L. aculeata. In the following these will be referred to as the "serriola-like species." The subset was used to compare various similarity coefficients and clustering methods and to study the relationships among the serriola-like species in detail. Clustering methods and similarity coefficients were tested using the procedures SIMQUAL, SAHN, and TREE from the program NTSYSpc version 2.02k (Applied Biostatistics, Setauket, New York, USA). The "TM" option was set to "FIND" to enable detection of all possible trees. The clustering methods UPGMA, WPGMA, Complete-link, and Single-link were applied in all possible combinations with the similarity coefficients Dice, Jaccard, and Simple matching. Clustering methods and similarity coefficients are described in Rohlf (1993)
. Cophenetic correlation coefficients (r) were calculated and compared for each of the combinations using the procedures COPH and MXCOMP from NTSYSpc 2.02k. These coefficients indicate the correlation between a similarity matrix and the phenetic tree resulting from it after a cluster analysis, and thus are a measure for the goodness of fit of the cluster analysis to the similarity matrix.
Species relationships among the serriola-like species were studied using a principal coordinates analysis (PCO). Jaccard's similarity coefficient and the procedures DCENTER, EIGEN, and MXPLOT from NTSYSpc 2.02k were used to perform the PCO.
Secondly, analyses were performed on the entire data set, containing all accessions from Table 1. This data set was used to compare phenetic and cladistic analysis of the AFLP data and to detect well-supported species clusters/clades within Lactuca s.l. The cluster analysis was performed with TREECON 1.2 (Van de Peer and De Wachter, 1994
), which enabled bootstrapping of the resulting phenogram. Nei and Li's (1979)
dissimilarity coefficient and UPGMA clustering were used; bootstrap values were calculated in 1000 replications. Cladistic analyses and determination of phylogenetic signal in the data set were performed using PAUP version 4.0a (Swofford, 1999
). Parsimony settings were: ACCTRAN and "collapse of zero length branches" (max). Phylogenetic signal was determined from the tree-length distribution of 100 000 trees, using the g1-statistic (Hillis and Huelsenbeck, 1992
). The lettuce data set contained >25 taxa and >500 variable characters, and therefore the critical value of –0.08 was used. A g1-statistic lower than this critical value indicates the presence of significant phylogenetic signal in the corresponding data set (Hillis and Huelsenbeck, 1992
).
The cladistic analyses started as a jackknife analysis using 10 000 replicates of a fast heuristic search, nominal deletion of 37% of the characters, and "Jac" resampling. A 50% majority rule consensus tree was calculated based on the jackknife analysis and used as a constraint tree for a heuristic search. The heuristic search comprised 10 000 random-addition sequences and tree bisection-reconnection (TBR) branch swapping with "multrees" switched off. A second search was performed using four cycles of successive weighting. The strict consensus of the heuristic search above was used as a starting point. Characters were reweighted by the maximum value of the rescaled consistency indices, and the searches were conducted with 100 random-addition sequences, tree-bisection-reconnection (TBR) branch swapping, and "multrees" on. Jackknife values for the resulting tree were calculated as above.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Table 2 shows the cophenetic correlation coefficients from analyses of the data subset containing L. sativa and its closest relatives, L. serriola, L. dregeana, L. altaica, and L. aculeata (the serriola-like species). UPGMA clustering yielded the highest cophenetic correlation in all cases, Single-link the lowest. The ranking of WPGMA and Complete-link was less consistent (see Table 2). Among the similarity coefficients, Jaccard consistently yielded the highest cophenetic correlations, followed by Dice and Simple matching. Since a similar ranking of similarity coefficients and clustering methods was found by Mace, Lester, and Gebhardt (1999) and Mace, Gebhardt, and Lester (1999) for Solanum and Datura/Brugmansia, it possibly applies to all AFLP data sets. The combination of Jaccard similarity with UPGMA clustering yielded the highest cophenetic correlation and is therefore considered most suitable for determining phenetic species relationships in Lactuca s.l. The combination of UPGMA with the Dice or Nei and Li (equaling 1-Dice) coefficient is also suitable for our data set, since trees based on these coefficients were identical to those based on Jaccard's coefficient. Identical topologies for the Jaccard and Dice coefficients were also found by Milbourne et al. (1997)
for AFLP data from cultivated potato.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, showing a large L. sativa/L. serriola cluster with L. serriola accessions branching off basally to a large subcluster containing all L. sativa accessions and one L. serriola accession. This L. serriola is a "landrace type," intermediate between L. sativa and L. serriola. The L. sativa/L. serriola cluster is clearly separated from L. saligna, L. virosa, L. indica, and L. perennis.
The L. serriola and L. sativa oilseed accessions in the present study fell within L. sativa. This is consistent with the results of Frietema de Vries, Van der Meijden, and Brandenburg (1994)
and Frietema de Vries (1996)
. In their principal components analysis of morphological data, the L. sativa and L. serriola accessions fall in two partly overlapping groups. According to the text, the oilseed accessions are included in the L. sativa cluster, although an accompanying figure depicts them as intermediate between L. sativa and L. serriola (Frietema de Vries, Van der Meijden, and Brandenburg, 1994
; Frietema de Vries, 1996
).
Given the lack of distinction between L. sativa and L. serriola in the present study, the position of the L. serriola oilseeds within L. sativa in the study of Frietema de Vries, Van der Meijden, and Brandenburg (1994)
and Frietema de Vries (1996)
, the presence of a L. serriola "landrace type" within L. sativa in the study of Hill et al. (1996)
, and the close similarity of L. sativa and L. serriola in other characters (discussed in Koopman et al., 1998
), we support the conclusion of Frietema de Vries, Van der Meijden, and Brandenburg (1994)
and Frietema de Vries (1996)
that L. sativa and L. serriola are conspecific. However, we do not support the distinction of L. sativa subsp. sativa and L. sativa subsp. serriola, as proposed by Frietema de Vries (1996)
. In our opinion, the species are too similar even to maintain them as subspecies. Therefore, we consider the earliest name, L. sativa, the correct name for both L. serriola and L. sativa.
Position of L. dregeana, L. altaica, and L. aculeata relative to L. serriola
Lactuca dregeana accessions fell within the mixed L. sativa/L. serriola cluster/clade in all our analyses. Most accessions within this cluster/clade show a mixture of L. serriola and L. sativa characteristics. For example, L. sativa accession CGN 5999 has an especially rigid, nearly woody stem, and spines on the midribs beneath, characteristics usually associated with L. serriola. On the other hand, L. serriola accessions CGN 5803 and CGN 4674 show spineless lower midribs, somewhat fleshy leaves, and involucres that are not completely reflexed when the fruits are ripe. These characteristics are usually associated with L. sativa. The L. dregeana accessions show a similar combination of characteristics. They resemble L. sativa in their somewhat fleshy leaves and involucres that are not completely reflexed when the achenes are ripe. On the other hand, they show L. serriola characteristics such as a rigid, spiny stem, spiny lower midribs, and dark brown, spotted achenes.
The combination of morphological characteristics and the position of L. dregeana in the mixed sativa/serriola cluster/clade in our AFLP analyses suggest that L. dregeana escaped from cultivation. The fact that L. dregeana is endemic to South Africa could mean that it originated from the primitive lettuce cultivars introduced there by European settlers in the 17th century. Lettuce seed production in the Cape was reported as early as 1652–1654 (Karsten, 1951
) and could easily have led to escapes to the wild by wind dispersal of achenes from cultivars with loose involucres. After taking into account the morphology of L. dregeana, its position in the AFLP analyses, and its possible origin in cultivated lettuce, L. dregeana probably does not deserve a species status, but it should be regarded conspecific with L. sativa/L. serriola.
The L. altaica accessions in the present study fell within a group of L. serriola accessions, corroborating previous ITS-1 results and the conclusion that L. altaica is probably conspecific with L. serriola (Koopman et al., 1998
). However, this conclusion is based on only two L. altaica accessions. Recently, additional wild material of L. altaica and its relatives L. serriola and L. saligna was collected in Uzbekistan (Van Soest, 1997
). A study on this material is currently being carried out to further elucidate the relationships and taxonomic status of L. altaica.
The accessions of L. aculeata form a clearly distinct group among the serriola-like species, with a 100% jackknife and bootstrap support. The position of L. aculeata separate from, yet closely related to, the other serriola-like species is well supported by our earlier ITS-1 study (Koopman et al., 1998
). This distinct position of L. aculeata within the serriola-like species makes it an ideal outgroup for studies into L. sativa, L. serriola, and their closest relatives.
All serriola-like species together, i.e., including L. aculeata, form a homogeneous group of closely related species within subsect. Lactuca. This is indicated by the 100% jackknife and bootstrap support for this group in the present AFLP analysis (Fig. 2a,b), the 95% bootstrap support in a previous ITS-1 analysis, and the fact that all serriola-like species are fully interfertile (Koopman et al., 1998
).
Position of L. saligna and L. virosa within subsect. Lactuca
The results of previous studies on plant morphology (De Vries and Van Raamsdonk, 1994
), crossability (Thompson, Whitaker, and Kosar, 1941
; Lindqvist, 1960
; De Vries, 1990
), SDS (sodium dodecyl sulphate) electrophoresis patterns of seed proteins (De Vries, 1996
), isozyme analysis of foliar esterases (Roux, Chengjiu, and Roux, 1985
), karyotype (Lindqvist, 1960
; Koopman and De Jong, 1996
), chromosome banding pattern (Koopman, De Jong, and De Vries, 1993
), DNA content (Koopman and De Jong, 1996
; Koopman, 2000
), nuclear RFLPs (restriction fragment length polymorphisms) (Kesseli, Ochoa, and Michelmore, 1991
), mtDNA RFLPs (Vermeulen et al., 1994
), nuclear AFLPs (Hill et al., 1996
), and ITS-1 sequences (Koopman et al., 1998
) showed different possibilities for the position of L. saligna and L. virosa relative to the serriola-like species, as was discussed in Koopman et al. (1998)
.
The present results indicate that L. virosa is more closely related to the serriola-like species than is L. saligna. However, the position of L. saligna and L. virosa relative to the serriola-like species is not very reliable, as is indicated by the low bootstrap and jackknife supports on the branches separating L. saligna and L. virosa. The results are not consistent with the AFLP analysis of Hill et al. (1996)
, indicating that L. saligna is the closest relative of the serriola-like species and that L. perennis is even more closely related to the serriola-like species than is L. virosa. However, Hill et al. (1996)
do not indicate support values for the relationships. Given the different positions of L. saligna and L. virosa in the study of Hill et al. (1996)
and in the present study, and the lack of branch support for these positions, we conclude that the available AFLP data are inconclusive as to the position of L. virosa and L. saligna relative to the serriola-like species. This is also true for the position of L. perennis.
In the present study, L. virosa accessions CGN 15679 and 15680 form a separate clade with a 100% bootstrap support. The anomalous position of these accessions may indicate that they are a distinct infraspecific taxon within L. virosa. The distinct position of CGN 15679 and CGN 15680 is also reflected by the fact that their DNA content is 1.16 times that of the other L. virosa accessions (Koopman, 2000
).
Species clusters/clades outside subsect. Lactuca
In a previous study using ITS-1 sequences, four clades of species were detected outside subsect. Lactuca: (1) L. tatarica/L. sibirica/L. viminea, (2) L. perennis/C. plumieri, (3) L. tenerrima/S. tuberosus, (4) M. muralis/C. alpina. Only one of these clades could be partially confirmed by our AFLP results. In all phenetic and cladistic analyses, the only well-supported cluster/clade outside subsect. Lactuca was one with L. tatarica, L. sibirica, and L. quercina. The relationship between L. tatarica and L. sibirica is consistent with the ITS-1 results and with the classification of Feráková (1977)
. The close relationship of L. tatarica and L. sibirica with L. quercina is not. In the ITS-1 phylogeny, L. quercina has its own distinct branch, while L. tatarica and L. sibirica occupy the same clade. In the classification of Feráková (1977)
, L. quercina is classified in section Lactucopsis, while L. tatarica and L. sibirica together make up section Mulgedium. The close relationship between L. tatarica and L. sibirica was confirmed by our recent crossing experiments, reported here for the first time. We conducted reciprocal crosses between four L. tatarica accessions and four L. sibirica accessions, and these crosses yielded viable seeds for six out of eight combinations of accessions. The F1 plants were vigorous and fully fertile, indicating a close genetic relationship between L. tatarica and L. sibirica. The possible close relationship of L. tatarica/L. sibirica with L. quercina needs more verification. Species relationships involving L. viminea, L. indica, L. perennis, L. tenerrima, M. muralis, C. plumieri, C. alpina, S. tuberosus, P. purpurea, and C. intybus could not be assessed in the present study, because the AFLPs were too variable to determine reliable relationships of these species.
Methodological considerations
In the present study, the data were analyzed both phenetically and cladistically. The validity of such analyses is sometimes disputed, although this dispute was not reflected in literature until now. Critics recognize two main sources of error in the cladistic analysis of AFLP data. Firstly, the fact that AFLPs are anonymous markers is a source of error. Because AFLP fragments are identified by their length and not by their base composition, nonidentical fragments of equal length will mistakenly be scored as identical. Secondly, the fact that AFLPs are scored dominantly is a source of error. AFLPs are usually scored as dominant characters, i.e., with only the character states present (1), and absent (0). In reality, at least part of the bands may represent codominant markers that have three character states, namely 0/0, 1/0, and 1/1. Both sources of error introduce homoplasies in the data set, possibly leading to erroneous tree topologies in cladistic analyses. In our opinion, the impact of these homoplasies on the conclusions regarding species relationships will be minor.
When we compare phenetic and cladistic analysis of AFLP data, there are two possible situations. Firstly, the topologies of the phenogram and the cladogram may be identical. In this case, the homoplasies were too minor to influence the topology of the cladogram. Consequently, they will not affect conclusions on species relationships. Secondly, the topologies of the phenogram and the cladogram may be different. In this case, the homoplasies significantly affected the topology of branches in the cladogram. However, because the differences are caused by homoplasies, there will be internal conflict in the data defining these branches. In branch support analyses such as bootstrapping or jackknifing, the presence of such conflicting data gives rise to low support values. These poorly supported branches will be discarded as uninformative when conclusions on species relationships are drawn. Therefore, in this case, too, the homoplasies in the AFLP data will not affect the conclusions on species relationships. In both cases, cladistic analysis of AFLP data will give rise to reliable phylogenetic conclusions, notwithstanding the validity of the theoretical objections.
The first case is illustrated by a study of Kardolus, Van Eck, and Van den Berg (1998)
in which a cladogram and a phenogram of 16 wild Solanum species show highly similar topologies, even for moderately supported groups. In our lettuce study both cases are present: the well-supported parts of the phenogram and the cladogram show similar topologies, while the differences in the remaining parts of the trees are poorly supported.
Conclusions
AFLPs proved to be suitable molecular markers to study the relationships among closely related species of Lactuca s.l. In phenetic analyses of a data subset, the combination of Jaccard's similarity coefficient with UPGMA clustering resulted in the highest cophenetic value. The results of a principal coordinates analysis of the subset were comparable to those of the UPGMA analysis. A data set comprising all accessions was analyzed phenetically as well as cladistically, and the well-supported parts of the trees were comparable for both types of analyses. The AFLP results corroborated the conclusions from a previous ITS-1 sequence study (Koopman et al., 1998
) that the serriola-like species L. sativa, L. serriola, L. dregeana, and L. altaica cannot be reliably distinguished and are probably conspecific. Lactuca dregeana possibly escaped from cultivation. Lactuca aculeata is closely related to the other serriola-like species, but clearly different. The AFLP results were inconclusive as to the position of L. saligna and L. virosa relative to the serriola-like species, but the status of subsect. Lactuca (the serriola-like species together with L. saligna and L. virosa) as a recognizable group within Lactuca s.l. was supported in all analyses. In the previous ITS-1 study, a number of species clades outside subsect. Lactuca were identified. Among the relationships indicated by these clades, only the close relationship between L. tatarica and L. sibirica (together constituting Lactuca subsect. Mulgedium) was corroborated by the present AFLP results. The close relationship between these species was also corroborated by our crossability data.
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FOOTNOTES |
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3 Author for reprint requests (e-mail: wim.koopman{at}biosysnhn.dpw.wag-ur.nl)
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4 Current address: Keygene N.V., P.O. Box 216, 6700 AE Wageningen, The Netherlands.
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