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II: the Origin of S Received 20 September 1991 Heredity 69 (1992) 112—121 Genetical Society of Great Britain Molecular systematics of the genus Seneclo L. II: The origin of S. vulgar/s L. STEPHEN A. HARRIS & RUTH INGRAM Department of Biology and Predilnical Medicine, Sir Harold Mitchell Building. University of St Andrews, St Andrews, Fife KY16 9TH, Scotland Theorigin of Senecio vulgaris L. and the relationship of its two subspecies, ssp. vulgaris and ssp. denticulatus (0. F. Muell.) P. D. Sell, are examined using nuclear ribosomal and chioroplast DNA analyses. No evidence was found to support either an allopolyploid or an autopolyploid origin of S. vulgaris, although it would appear that S. vernalis Waldst. & Kit, is not one of the progenitor taxa. Two results of particular interest were found: (i) the apparent identity of the chioroplast genomes of S. vulgaris ssp. vulgaris and S. squalidus L. and (ii) the divergence of the chloroplast genomes of ssp. vulgaris and Ainsdale ssp. denticulatus by at least eight site mutations. These results are discussed in the light of evidence derived from morphological, cytological and allozyme studies. Keywords:Asteraceae,molecular variation, Senecio vulgaris ssp. vulgaris, S. vulgaris ssp. denti- culatus. Introduction characteristically spathulate leaf shape (Allen, 1967; Kadereit, 1984b). Seneciovulgaris L., the common groundsel, is one of Within Senecio vulgaris ssp. vulgaris, two varieties the most widespread annual/ephemeral species in are recognized: var. vulgaris, the more frequent non- Britain. Taxonomically two subspecies are recognized, radiate variety and var. hibernicus, an inland radiate which differ ecologically. Senecio vulgaris ssp. vu/guns variety which has increased in frequency in recent is the common weedy groundsel associated with dis- years. Isozyme analysis indicates that the latter variety turbed sites, whilst ssp. denticulatus (0. F. Muell.) P. D. has originated through introgression from S. squalidus, Sell is rare in Britain, being confined to a few coastal following the introduction of £ squalidus in the seven- sites, where it grows on sand dunes (Lancashire and teenth century and its more recent spread and naturali- Channel Islands). This subspecies is a winter annual. zation (Abbott et al., 1991). Kadereit (1 984a) discusses the life-history and There are thus three intraspecific taxa recognized in germination pattern of ssp. denticulatus and states that Senecio vu/ga ris,all of which are tetraploid this subspecies becomes a montane element in the (2n=4x=40). Kadereit (1984b) suggested that S. Mediterranean. AlIen (1967) lists the coastal sites in vulganis ssp. denticulatus is an autopolyploid of fairly Europe where the subspecies occurs. Early records of recent origin with S. vernalis (2n =2x=20)as its ssp. denticulatus (Allen, 1967; Perring & Sell, 1968; parent. Kadereit also suggested that ssp. denticulatus is Crisp, 1972) from other coastal sites in the British Isles an ancestoral form of ssp. vulgaris through selection for (Devon, Cornwall, Cheshire and the Isle of Man) have an ephemeral life-history as an agricultural weed. An not been confirmed in recent years (Ashton, 1990). alternative suggestion, based on cytological studies of This may be due to extinction of the subspecies at these chromosome pairing in species—species hybrids was sites or the early confusion surrounding the nomen- put forward by Weir & Ingram (1980). They suggested clature of the intraspecific ranks of S. vulgaris (Allen, an allopolyploid origin for S. vulganis between S. 1967). squalidus, or a taxon related to it, and a second Morphologically, Senecio vulgaris ssp. denticulatus is unidentified taxon. These two suggestions need not be distinguished from ssp. vu/guns by the possession of mutually exclusive because there can be no clear short ray florets, a densely arachinoid indumentum and division between autopolyploidy and allopolyploidy, MOLECULAR SYSTEMATCS OF SENEC/O 113 and the nature of the control of chromosome pairing in of the taxa, except S. paludosus (Section Doria) have polyploids of this group is complex (Ingram & Noltie, been variously placed in either Section Jacobaea or 1987, 1989). Section Senecio (Chater & Walters, 1976; Alexander, Recently polyploid speciation has been analysed 1979). using molecular techniques. Both the nuclear and chioroplast genomes have been successfully used. The DNAextraction and molecular methods nuclear genome is inherited biparentally and tandemly arranged ribosomal sequences (rDNA) have proved DNAextraction and molecular methods are given in very useful (Jorgensen & Cluster, 1988). Ribosomal Harris & Ingram (1 991a). In the cpDNA analysis a total RNAgeneshave proved useful in confirming hybridity of 11 restriction enzymes were used; one tetranucleo- in Claytonia (Doyle & Doyle, 1988). Similar examples tide cutting enzyme (HaeIII), 10 hexanucleotide cutting are found in Tripsacum andersonii (Talbert eta!., 1990) enzymes (BamHl, BglII, EcoRl, EcoRV, HinDIII, and the Saxifragaceae (Doyle et al., 1985). In each case KpnI, PstI, Sad, XhoI) and one heptanucleotide the supposed hybrid had the additive rDNA patterns cutting enzyme (BstEII).Inthe rDNA survey only three of the two putative parents. enzymes were used (BamHI, EcoRI, EcoRV). The Angiosperm chioroplast genome (cpDNA) is a small circular molecule which is usually inherited Probecharacteristics uniparentally through the maternal parent (Palmer et a!., 1988; Harris & Ingram, 1991b). Chioroplast DNA ClonedLactuca sativa cpDNA fragments (Jansen & has been used to address questions of both allopoly- Palmer, 1987) were used either singly (Cl, C2, C4, C6, ploid and autopolyploid speciation, although allopoly- C7, C9, C15) or as a mixture (C5a—C5c; ploid speciation is the most studied of these two ClO—Ci 1—C12; C13-C14). These probes sampled modes. Studies of allopolyploid speciation using approximately 80 per cent of the Senecio chloroplast cpDNA markers have been made, for example, in genome. Papaver (Mb et a!., 1988), Senecio cambrensis (Harris A cloned nuclear ribosomal DNA repeat from & Ingram, 199 la), Tragopogon (Soltis & Soltis, 1989) Triticum aestivum 'Chinese Spring' was used to locate and Oryza (Daily & Second, 1990). Autopolyploid ribosomal sequences in the Senecio nuclear genome. speciation has been successfully studied in Heuchera The probe, pTA7 1, is a complete rDNA repeat of 9.1 grossularitfolia (Wolf et a!., 1990) and H. micranthera kb cloned into an EcoRI site of pUC19 (Gerlach & Bedbrook, 1979). In addition two iDNA clones from (Soltis eta!., 1989). The aims of the present investigation were: (i) to Taraxacum were used (King & Schaal, 1990). pTEE3 determine the possible origin of Senecio vulgaris s. 1. is a 3.9 kb EcoRl fragment which contains the coding using cpDNA and rDNA markers; and (ii) to analyse region of the rDNA repeat. pTEE5 is a 5.3 kb EcoRl the relationship between S. vulgaris ssp. vulgaris and fragment which contains the majority of the intergenic spacer and part of the 18S rDNA gene. ssp. denticulatus using rDNA and cpDNAmarkers. In pursuit of these aims the rDNA and cpDNA genomes of representatives from all subspecific taxa of S. Dataanalysis vulgaris, and of S. squalidus and S.vernalishave been analysed. As a control S. cambrensis (2n =6x = 60), Sequencedivergence estimates for cpDNA were obtained by a maximum likelihood method (Nei, 1987; the allohexaploid hybrid of S. vulgaris and S. squalidus, which could has been included and the genomes of S. jacobaea and eq. 5.50 and 5.51) using only the mutations positively be inferred as site mutations. Other muta- S. paludosus have been used as outgroups. tions were ignored in these estimates, which therefore underestimates the degree of divergence. Phylogenetic Materials and methods analysis was conducted only on site mutations using the branch and bound Wagner parsiomony program PENNY P/ant material in the package PHYL-W (Felsenstein, 1985). The branch Achenes from single individuals of Senecio cambrensis and bound option is guaranteed to find all the most parsimonious trees. Restriction site mutations were Rosser, S. jacobaea L., S. paludosus L., S. squalidus L., S. vernalis Waldst. & Kit., S. vulgaris L. ssp. denti- polarized using the outgroup S. paludosus (Section culatus (0. F. Muell.) P. D. Sell, S. vulgaris L. ssp. vu!- Doria). garis var. hibernicus Syme and S. vulgaris L. ssp. The data from the rDNA analysis were treated rather differently due to the large degree of intertaxon vulgaris var. vulgaris, representing 19 accessions (Table 1) were grown as stated in Harris & Ingram (1991a). All variation and the difficulty of assigning length or site 114 S. A. HARRIS & A. INGRAM Table1Locationsof the Senecio taxa studied Grid Number of Taxon Location reference individuals Source Code Section Senecio S. vulgaris ssp. vulgaris var. Migvie, Aberdeenshire (M) NJ437068 1 RJA Vi vulgaris York(P) SE590510 1 PA V2 Mochdre,Wales(P) SH822781 1 PA V3 Salamander Street, Edinburgh (P) NT276763 1 PA V4 S. vulgarisssp. vulgarisvar Mochdre, Wales SH822781 1 PA HI hibernicus Brymbo, Wales SJ296539 1 PA 112 Salamander Street, Edinburgh NT276763 1 PA H3 York 5E590510 1 RJA H4 S. vulgaris ssp. denticulatus Ainsdale, Lancashire SD295 124 1 PA Dl S. squalidus Salamander Street, Edinburgh NT276 763 1 PA Si Brymbo, Wales SJ296539 I PA S2 Stoke SP360780 1 PA S3 York SE590510 1 PA S4 Sheffield SK350870 1 PA S5 S. cambrensis Salamander Street, Edinburgh NT276763 1 SAH Cl Brymbo, Wales SJ296539 1 PA C2 S. vernalis Schiusserlacker Weide, Eppelheim near
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