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Genetic Basis of Speed of Development in Senecio Vulgaris L

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Genetic Basis of Speed of Development in Senecio Vulgaris L Heredity 77 (1996) 544—554 Received 19 January 1996 Genetic basis of speed of development in Senecio vulgaris L. var. vulgaris, S. vulgaris ssp. denticulatus (O.F. Muell.) P.D. Sell, and Senecio vernalis Waldst. & Kit. HANS PETER COMES* & JOACHIM W. KADEREIT Institut für Spezielle Botanik u. Botanischer Garten, Johannes Gutenberg-Universitat Mainz, Bentze/weg 9, 55099 Mainz, Germany Thegenetic basis of differences in speed of development from germination to first bud formation was investigated in Senecio vulgaris var. vulgaris and S. vulgaris ssp. denticulatus, and also in S. vernalis sampled from Israel and Germany. In the case of S. vulgaris, F2 segregation analysis and the recovery of very late and very early lines from extreme F2 phenotypes showed that differences can be explained by a single major gene model, whereas segregation data from F2 and backcross progenies in S. vernalis are not incompatible with a digenic model of inheritance. Senecio vernalis from Israel and S. vulgaris var. vulgaris reached the different developmental stages in a substantially shorter time than did C. European S. vemalis and S. vulgaris ssp. denticulatus. In both species the increased speed of development was achieved through drastic abbreviation of the rosette stage of development rather than through an acceleration of the entire developmental programme. It is suggested that the genes controlling speed of development in S. vulgaris and S. vemalis may be homologous to major heterochronic genes identified from mutants of Arabidopsis thaliana (e.g. early flowering [elfl—3]). Keywords:earlyflowering mutants, genetic basis, life history trait, Senecio vemalis, Senecio vulgaris, speed of development. Introduction required for development from germination to first flower bud formation, anthesis, and fruiting. Infor- Speedof development is an important variable in mation concerning the genetic control of these flow- theories of life history evolution (Sibly & Antono- ering characters is rapidly increasing in well-defined vics, 1992), as it is generally assumed to affect total experimental mutant systems, particularly Arabidop- lifetime fecundity (Lewontin, 1965; MacArthur & sis thaliana (L.) Heynh. (Koorneef et aL, 1991; Sung Wilson, 1967). At the macroevolutionary level, varia- et aL, 1992; Zagotta et at., 1992; Bernier et at., 1993), tion in developmental timing in a derivative taxon and many species of agronomic importance, for relative to its progenitor is commonly referred to as example maize (e.g. Freeling et at., 1992; see also heterochrony (Diggle, 1992). A full understanding of Bernier, 1988 for a review). In addition, other such major evolutionary changes requires an under- cereals with genomes suitably mapped at the standing of the genetic basis of phenotypic differ- molecular level have recently been shown to provide entiation. A knowledge of the inheritance of speed excellent material for RFLP marker studies of major of development is also of value in testing key genes controlling flowering time and developmental assumptions of genetic models of life history varia- rate (Triticum aestivum, Law et al., 1993; Hordeum tion (Anderson & King, 1970; Lande, 1982; Charles- vulgare, Laurie et at., 1994). In contrast, the genetics worth, 1984, 1990). of developmental timing in most wild plant taxa is Developmental timing in plant species can be poorly known (Murfet, 1977; Bernier, 1988). More- objectively determined by the number of days over, only very few studies of natural plant popula- tions have provided evidence of the type and *Correspondence: School of Biological and Medical Sciences, direction of evolutionary change in developmental University of St Andrews, St Andrews, Fife KYI6 9TH, U.K. timing by merging qualitative or quantitative genetic 544 1996The Genetica! Society of Great Britain. GENETICS OF SPEED OF DEVELOPMENT IN SENEC/O 545 information with hypotheses of progenitor-derivative rare taxon from the coasts of W. Europe and the relationships (Stephanomeria, Gottlieb, 1973, 1982; mountains of S. Spain and Sicily (Kadereit, 1984a, Mimulus, Macnair & Cumbes, 1989; Fenster & and unpublished results), where it occurs in both Ritland, 1994; Fenster et a!., 1995). A general natural and disturbed habitats (Comes, 1995a; conclusion gained from the studies cited above is Kadereit, unpublished results). Morphologically, var. that there is wide variation in the genetics of devel- vulgar/s and ssp. denticulatus are normally distin- opmental timing, and consequently there is no single guished by the presence of ray fiorets in the latter. type of genetic system —eitherMendelian inherit- Presence vs. absence of ray fiorets is governed by ance involving only a few genes with major effects, alternative alleles at a single locus (Trow, 1912). The or polygenic inheritance —thatunderlies the two taxa differ dramatically in two life history phenotypic differences. characters, with var. vulgar/s normally exhibiting no In this paper we examine the genetic basis of pronounced seed dormancy and up to twice the intraspecific differences in speed of development speed of development of ssp. denticulatus (Kadereit, from germination to first reproduction in two closely 1984a; Comes, 1995a). The difference in seed related species of Senecio L. (Compositae), S. dormancy appears to be regulated by a single gene vulgaris L. and S. vemalis Waldst. & Kit. Substantial with two alleles in ssp. denticulatus from Jersey differences were analysed between S. vulgaris var. (Kadereit, 1984a). Presence of seed dormancy was vulgaris and S. vulgaris ssp. denticulatus (O.F. Muell.) recessive to the absence of seed dormancy in British P. D. Sell on the one hand, and between populations var. vulgar/s. Seed dormancy, however, has also been of S. vemalis from Israel and Germany on the other shown to occur in var. vulgar/s from the Mediterra- hand. An almost twofold difference in speed of nean, where the winter-rain climate does not permit development has been observed in the former case the formation of more than one generation per year (Kadereit, 1984a, and unpublished results; Comes, (Ren & Abbott, 1991; Comes, 1995b). Seed 1995a), and a difference of almost identical magni- dormancy here appears to be regulated digenically tude was reported more recently in material of S. (Comes, 1995b). vernalis from different geographical regions (Comes, On the basis of morphological/phenological, 1995b). geographical and ecological considerations it has The genetic basis of the large difference in speed been argued that ssp. denticulatus should be of development in both S. vulgaris and S. vemalis is regarded as the progenitor of the weedy var. the subject of the present analysis. In the case of the vulgar/s, or as close to such (Kadereit, 1984b). On former taxon, it is conceivable that its polyploid the assumption that the differentiation of var. genomic constitution may lead to difficulties in inter- vulgar/s coincided with its geographical/ecological preting patterns of segregation. However, there is separation from ssp. denticulatus, var. vulgar/s may well-documented evidence in S. vulgaris of both have arisen in late glacial or early postglacial times. disomic inheritance at the ray floret locus (Trow, At that time ssp. denticulatus, which was probably 1912) and fixed heterozygosity at a number of distributed in Mediterranean coastal habitats during isozyme loci (AAT-3,c.EST-1,PGI-2; Ashton & the glacial period, reacted to climatic changes by Abbott, 1992), thus justifying the assumption that retreating into higher altitudes in the Mediterranean the species contains a diploidized genome. area, and north along the coasts, i.e. into those areas where it can be found today. At that time many new habitats would have become available for var. Material and methods vulgar/s. Senecio vulgar/s Senec/overnal/s Senecio vulgar/s (common groundsel, 2n =4x=40) consists of three taxonomic units, namely ssp. Seneciovemalis (spring groundsel, 2n =2x=20)is vulgans var. vulgaris, ssp. vulgar/s var. hibernicus widely distributed in C. to E. Europe, S. W. Asia, Syme, and ssp. denticulatus. Subspecies vulgar/s var. Siberia, S. Russia, and Afghanistan (Alexander, vulgar/s and ssp. denticulatus were the two taxa of S. 1979). The expansion of its range into C. Europe in vulgaris investigated in the present study. the last 200 years has been well documented (Hegi, Var. vulgar/s is considered to be native to W. 1987). In C. Europe S. vemalis mostly behaves as a Eurasia (Kadereit, 1984b), but is now distributed winter annual and is polymorphic for seed more or less worldwide, mainly as a ruderal and dormancy, which is regulated by a recessive allele of agricultural weed. In contrast, ssp. denticulatus is a a single gene (Comes, 1995b). In contrast, material The Genetical Society of Great Britain, Heredity, 77, 544—554. 546 H. P. COMES&J. W. KADEREIT from the E. Mediterranean appears to be fixed for data were pooled. This analysis also revealed that seed dormancy, and develops substantially faster neither block (i.e. local environmental) factors nor from germination to first reproduction (Comes, family x block effects (i.e. gene-environment interac- 1995b). tions) were significant (data not shown). The Although there is no doubt that the C. European material was scored daily for the number of days populations of S. vernalis are of introduced status, it from (1) germination to bud formation, (2) germina- is not known whether this material is directly tion to first anthesis, and (3) germination to first derived from populations in the E. Mediterranean. fruiting. It seems likely, however, that E. Mediterranean To investigate the underlying genetic model populations of S. vernalis lie within the range the further, a simple one-generation divergent selection species occupied before man started to alter the experiment was carried out. Nine individuals from 'natural' distribution of the species. In this respect, the F2 were selected for extreme low and high therefore, C. European populations may be consid- phenotypic values for the traits under study. Selec- ered as derived, relative to E. Mediterranean popu- ted plants were selfed and used for the production lations. Truly native populations of S.
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