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The Patterns of Evolution and Ornamental Plant Breeding Wolfgang Horn TU München Chair for Floriculture Crops and Horticultural Plant Breeding D-85350 Freising Germany Keywords: Begonia, Primula, interspecific hybridisation, polyploidy, review, history Abstract A review is presented of the origin and development of sexually and asexually propagated ornamental crop species, with special emphasis on Primula malacoides and Begonia semperflorens-cultorum. INTRODUCTION It is considered fitting at this meeting to look back on the origin of our ornamentals, and to follow their pathways during development, though there have been reviews of this topic in the past (Darlington, 1963; Horn, 1968). I should like to begin with some citations worthy of note. • Interest in the patterns of evolution extends beyond the historical, because they are also the methods currently used by plant breeders (Allard, 1960) • The development of cultivated plants is the most important point of contact between plant breeding and evolution • Plant breeding since Mendel is evolution directed and expedited by man • Origin of cultivated plants is evolution under conscious or unconscious assistance of human beings. • Plant breeders are applied evolutionists (even if they have rarely noticed the fact) (Simmonds, 1976). • Ornamental crop evolution – genetic change in crop populations – is probably at least as rapid now as ever it has been and, in some crops, much more rapid. There are many unanswered questions concerning the origin and domestication of cultivated species. A. v. Humboldt stated 200 years ago that we knew nothing about the original sources of our most useful plants. Then came Darwin and genetics. Experimental evidence for the evolution of cultivated plants has long employed plant-breeding researchers. The history of most ornamentals started in the 17th and 18th century when botanists, plant collectors, missionaries, medical doctors on board of ships brought back new plants from the East and from the New World to Europe. Ornamental plants, existing in an enormous number of species, most of them little, but many much, improved. It is advantageous that their improvement being mostly recent and often very well recorded. Ornamental plants, therefore, are especially well suited to study in which way cultivated plants have arisen from wild species. GENERAL ASPECTS In one way or the other, cultivated plants must have arisen from wild progenitor species. I will not go too much in detail, but since the days of Darwin and the early days of genetics it has became clear that the main patterns in which they evolved are: • Mutations, which are the primary source of genetic variability and supply the raw materials for selection and recombination. Gene mutation is the basic factor for plants to evolve. New genes (better: alleles) arise continuously and may enable the plant to meet new environmental conditions more successfully. • Recombination; the combination of variants provides further variability. It has certainly played and is still playing an important role in developing new ornamentals. Since Mendel it is known that new recombinants arise in F2 and later generations. During the early development of ornamentals, strains carrying heritable Proc 21st IS on Breeding Ornamentals, Part II Eds: G. Forkmann & S. Michaelis Acta Hort 651, ISHS 2004 19 variations were grown near each other and natural hybrids occured, and greater numbers of combinations of variants resulted. A large number of interaction effects arise from the many gene combinations and result in unforeseen character modifications. Progeny from species hybrids that are heterozygous for a large number of genes produces an immense variation. Where asexual propagation is possible, interspecific hybridisation permits the development of new types even if they are sterile. Variation by gene recombination will have a determinative effect only if it is combined with selection. Survival of the fittest means of the best adapted, and genetic adaptation is accomplished primarily by gene recombination. • Selection shapes the raw material that is sifting for superior, adapted, biologically fit, desired genotypes. Steady selection pressure could slowly and gradually alter characters by accumulating small additive effects of many genes. Sorting out the superior types is accomplished by both human and natural selection and is often a combination of both. Selection is the most difficult part of plant breeding. Man selected severely among variants, molding them into something of greater use to him. Variants useful to man often would have expired in natural conditions but for human interference. Under cultivation mutant types have been favored because they appealed to the curiosity of man. For centuries, selection was the only method practised for the improvement of plants, and the natural seedlings of selected plants were the only material from which a choice was possible. Selection thus operated on the maternal side only, the pollen was derived by chance from other individuals, and there was no selection of the paternal parent (Crane & Lawrence, 1952). When selecting for ornamental breeding aims, aesthetic value, production costs, postproduction longevity, quality and marketability are important. • Isolation is effected by reproductive barriers, control of mating and spontaneous gene exchange. • Drift produces rapid changes of gene frequencies in small populations. Selection, isolation and genetic drift are mentioned here in passing only, a closer look at mutations and recombination plus polyploidy will follow. Regarding mutations one can differentiate between nuclear, extra-nuclear mutations and polyploidy. As to recombination, variants are combined through intra-specific hybridization possibly followed by auto-polyploidy, or through inter-specific hybridization possibly followed by allo-polyploidy. There are quite a number of ornamentals where only mutations transformed a wild species into a plant cultivated in our greenhouses. Examples may be found amidst foliage plants such as Ananas comosus, Aglaonema, several Ficus spp., Hedera helix, which are still near the wild species and often modified by bud sports only. Numerous variegated plants are grown in floriculture, and are examples of extranuclear mutation. One group of variegations develop from plastid mutations. Cells with mutant plastids give rise to white or yellow cell lineages. By forming stable periclinal chimeras the plastid mutations are preserved. Mutant plastids may be transmitted by the eggs into the next generation. It is relatively easy to develop variability by introducing new types through hybridization within or between species, and by changing the chromosome number. Polyploidy has certainly played and is still playing an important role. New tetraploids arise and are produced from diploid and from tetraploid × diploid crosses, apparently via unreduced gametes. It is evident that the accident of the unreduced gamete may be of considerable importance to the plant breeder, in the first place because it is the commonest way in which polyploids arise, and secondly because it is the means whereby selected genes may be transferred from the diploid to the tetraploid condition. As will be shown later on polyploids have some advantages but genetics of autopolyploids is much more complicated than that of diploids or allopolyploids (amphidiploids). The degree of heterozygosity is usually much greater. In tetraploids often some dosage effects are observed. 20 EVOLUTION OF ORNAMENTAL PLANTS Asexually and Sexually Propagated Crops In asexually propagated ornamental species all patterns of evolution are found; interspecific crosses followed by polyploidy, and somatic mutations – bud mutations or sports – are of special importance in nearly all genera (Table 1). In Narcissus e.g. we find all four patterns. The origin of the garden forms (Wylie, 1952) through selection, interspecific crosses and polyploidy is shown in Fig. 1. In Rhododendron simsii cultivars from bud sports have great importance (Table 2). Interspecific crosses and polyploidy had a great impact on the development of cultivated Begonia spp. as well as of Impatiens hawkeri hybrids (New Guinea Impatiens) and Kalanchoe hybrids (Fig. 2, 3, 4). It is quite obvious that sports play no role whatsoever in sexually propagated crops (Table 3). In this group, mutation and recombination within species and in several cases autopolyploidy are of importance. In contrast, Begonia × tuberhybrida has been developed from interspecific crosses (Fig. 4, Table 4) in the 19th century, and mutations such as double flowers (firstly observed in 1873), white and yellow flower colour (1874/75) as well as polyploidy (1877) produced horticulturally valuable characters. Since abt. 1880 tetraploidy has made sexual propagation (F1-hybrids) possible after clonal propagation was the rule. The history of Primula praenitens, the Chinese primrose, following its introduction to Europe since 1820 is not easy to trace in regard to the appearance of definite mutations. Differences found can be assigned to a limited number of genes through genetic investigations (Table 5). Certain gene mutations appear to have occured more than once (Crane and Lawrence, 1952). The years from 1860 to 1885 saw the production of numerous cultivars, developed by variation within a single species. There are diploid and tetraploid forms of the Chinese primrose in cultivation. Evolution within One Species: Primula malacoides The fairy primrose is a fine example how from a diploid pale lilac flowering wild species with a low variability a tetraploid pot plant species with a great variability has been developed. Of Chinese origin, it was first described in France in 1886, and the first seeds were offered in Great Britain in 1908. Since 1919 breeding took place in the USA, Switzerland and especially in Germany. Once in cultivation several horticulturally important mutants were isolated: white and pink flowers (1914/15), rounded petals (1923), compact growth (1927) and large tetraploid flowers (1924). Many diploid and, mainly, tetraploid cultivars have been developed. Flower traits are given in Table 6. Allele dosage effects have been observed regarding flower colour (Table 7). Somewhat surprisingly tetraploids produced much more seeds per flower than diploids (Table 8). This is characteristic for tetraploids from unreduced gametes (meiotic origin) in contrast to colchiploid tetraploids (mitotic origin). Already Navashin (1926) and Greenleaf (1941, 1942) have observed such differing fertility of meiotically and mitotically originated polyploids. In P. malacoides in diploid crosses unreduced gametes occured in very low frequencies in both sexes, while in crosses between different ploidy levels much more unreduced gametes are formed, and differences between genotypes have been found (Table 9). In 4x × 2x crosses they are produced relatively often, and in the males only, and in 2x × 4x in somewhat lower frequency, and in the females only. In 2x × 2x crosses only 5 ‰ tetraploids occurred (Table 10). In crosses between different ploidy levels, there are combinations, where 4x × 2x produced most polyploids and vice versa, though on the average, 4x × 2x produced more. The high frequency of 4x progeny from 2x × 4x crosses may be caused by an advantage of unreduced gametes in such crosses, and possibly by a better viability of tetraploid embryos while triploid embryos are rarely viable (Skiebe 1966). In 4x × 2x crosses, however, more 3x than 4x types originated. Remarkably, all diploids from 2x × 4x crosses are matrocline. They came from haplo-diplo- and diploparthenogenesis. It has been observed very often in different genera and species, that the rate of 21 polyploid progeny from such crosses varies with the genotype of partners and from year to year. Skiebe (1966) e.g. has found in the fairy primrose in one year, 51 % tetraploids and in another year 80 % from identical crosses. On the other hand, in some 4x × 2x crosses up to 98 % tetraploids originated, depending on the genotype of the seed parent. Similarly, in Cyclamen polyploids from unreduced gametes have been very successful. Evolution Including Interspecific Crosses: Begonia semperflorens Fine examples of the origin of an ornamental plant by interspecific crosses and polyploidy can be found in the genus Begonia. The fibrous-rooted begonia (B. × semperflorens-cultorum, B. cucullata var. hookeri) came to Germany from Brazil by chance in 1821. It was not until 1870 when its good outdoor performance as bedding plant was detected and gene mutations regarding new flower and leave colours (1879, 1888) were selected, the production of cultivars was intensified in France and Germany. 1890 a dwarf mutant was found. Following the introduction of B. schmidtiana (white flowering) in the late 1870ies and crosses between both species, which have the same chromosome number, fast progress was made. Their diploid hybrid was nearly sterile and reproduced in Germany as cv. ‘Erfordia’ (syn. Blütenmeer, Rosamunde) regularly from 1894 until 1964 by crossing the parental species (Skiebe, 1966). Therefore, it was the very first F1 hybrid cultivar in plant breeding. Then in the late 1890ies allo-tetraploid forms have originated in Germany and France (“B. semperflorens gracilis”, Fig. 5) and the resulting truebreeding cultivars surpassed the diploids (Zeilinga, 1962; Skiebe, 1966, 1970). The first tetraploid F1-hybrid cultivars have been produced in Germany by Benary seedgrowers (G. Besoke), from 1909 until 1961 (‘Primadonna’ and ‘Feuerzauber’). From 1922 onwards also diploid hybrid cultivars have been developed. From crosses between diploid and tetraploid the first triploid hybrid cultivars originated (Benary 1934 ‘Rosa Tausendschön’, syn. Rosalinde, Rosa Media), which were nearly sterile but showing exceptional performance, and with long lasting flowers. As Skiebe (1966, 1970) could demonstrate (Fig. 6), triploids originating in the F2 of the cross B. semperflorens × schmidtiana and in the B1F1 of the backcross to B. schmidtiana. Tetraploids were found in the B1F2 of the backcross to B. semperflorens and after crossing the mentioned triploids. In this way Skiebe resynthesized the fibrous-rooted begonia from old genotypes. OUTLOOK The plant breeder can learn from nature. Plant breeding since Mendel is evolution directed and controlled by man. Mendelian variation, interspecific hybridization and polyploidy are the methods of transforming wild species into cultivated plants. In fact, ornamental crop evolution is probably at least as rapid now as ever it has been and, in some crops, much more rapid. Even nowadays breeders accelerate plant evolution under domestication, mainly by recombination. Transformations and transposon-induced changes are the new way of mutation. Transformations and somatic hybridisation are new ways of recombination. Techniques like embryo rescue and in vitro pollination have permitted hybridizations till now impossible. We also realize that the progress in molecular biology led to an advance of evolutionary biology, and molecular data offer very easy and reliable methods for the reconstruction of relationships between our cultivated plants and their progenitors. So in different ways new lanes have been opened for plant breeding and phylogenetic evolutionary research. Literature Cited Allard, R.W. 1960. Principles of plant breeding. John Wiley & Sons, New York, London. Crane, M.B. and Lawrence, W.J.C. 1952. Genetics of garden plants. McMillan, London. Darlington, C.D. 1963. Chromosome botany and the origins of cultivated plants. Allen & Unwin, London. Greenleaf, W.H. 1941. Sterile and fertile amphidiploids: Their possible relation to the 22 origin of Nicotiana tabacum. Genetics 26: 301-324. Greenleaf, W.H. 1942. Genic sterility in tabacum-like amphidiploids of Nicotiana. Journ. Genet. 43: 69-96. Heursel, J. 1999. Azalea’s, oorsprong, veredeling en cultivars. Lannoo, Tielt/Terra, Warnsveld, Belgium. Horn, W. 1968. Genetische Ursachen der Variation bei Zierpflanzen. Gartenbauwissenschaft 33: 317-333. Jahr, W. 1970. Polyploidie bei Fliederprimeln. Tagungsbericht 101: 121-133. Deutsche Akad. Landwirtschaftswiss., Berlin. Navashin, M. 1926. Variabilität des Zellkerns bei Crepis-Arten in Bezug auf die Artbildung. Z. Zellforsch. Mikrosk. Anatomie 4: 171-215. Seyffert, W. 1959. Untersuchungen über interallele Wechselwirkungen. III. Naturwissensch. 46: 271-272. Simmonds, N.W. 1976. Evolution of crop plants. Longman, London. Skiebe, K. 1958. Die Bedeutung von unreduzierten Gameten für die Polyploidiezüchtung bei der Fliederprimel Primula malacoides. Züchter 28: 353-359. Skiebe, K. 1966. Die züchterische Entwicklung von Begonia semperflorens-cultorum in Deutschland. Züchter 36: 168-171. Skiebe, K. 1970. Polyploidie bei Begonia semperflorens cultorum. Tagungsbericht 101: 109-119. Deutsche Akad. Landwirtschaftswiss., Berlin. Wylie, A.P. 1952. The history of garden narcissi. Heredity 6: 137-156. Zeilinga, A.E. 1962. Cytological investigations of hybrid varieties of Begonia semperflorens. Euphytica 11: 126-136. 23 Tables Table 1. Patterns of evolution - Asexually propagated ornamental species. Bud mutations Mutation and recombination within spp. between spp. Polyploidy Auto- Allo- Alstroemeria x x x Begonia cheimantha x x x Chrysanthemum x x x Dahlia x x x Dianthus caryophyllus x Erica hybrids x Euphorbia pulcherrima x Freesia x x x Gladiolus x x x x x x x x Hibiscus rosa-sinensis Hyacinthus x x (x) x x Impatiens NG (x) x x Kalanchoe (x) x x Lilium hybrids (x) x (x) Narcissus x x x Pelargonium x (x) x Rhododendron simsii x x (x) Rosa x x x Tulipa x x x 24 (x) x Table 2. Rhododendron simsii hybrids – cultivars from bud sports. Source cv. Year of origin No. of sports Year Avenir 1911 9 1936-1969 Hellmut Vogel 1967 25 1972-1994 Knut Erwen 1934 10 1958-1998 Mme. Petrick 1880 17 (35) 1911-1948 Paul Schäme 1890 15 (21) 1928-1960 Vervaeneana 1886 1887-1928 Table 3. Patterns of evolution – Sexually propagated ornamental species. Mutation and recombination within spp. Ageratum Antirrhinum Begonia fibrous-rooted Begonia tuberous-rooted Callistephus Campanula persicifolia Coreopsis Cyclamen Gaillardia Impatiens walleriana Lathyrus odoratus P. malacoides P. obconica Petunia Primula praenitens Rudbeckia Tagetes erecta Tagetes patula Viola wittrockiana x x (x) x x x x x x x x x between spp. Polyploidy Auto- Allo- x (x) x x x x x x x x (x) x x x x x x x x x x x x x x 25 Table 4. Origin of tuberous begonia (sect. Huszia). Species / colour 1st flower Great Britain No. of chromosomes B. cinnabarina red 1948 2n = 26 B. boliviensis red 1867 2n = 28 B. pearcei yellow 1866 2n = 26 B. veitchii red 1867 2n = 28 B. davisii red 1876 2n = 28 B. dregei white 1836 2n = 26 South Africa (sect. Augustia) Table 5. History of Primula praenitens gene mutations arisen in cultivation. Year Introductions from China Stellata Allele 1820–1826 abt. 1821 ch Purplish-crimson flowers 1824 G White flowers 1827 D Fertile double magenta and white 1838 M Crimson forms figured 1846 B Large eyes recorded 1864 A Coral flowers 1906 K Ivy leaf 1907 iv Maple leaf 1929 mp Dazzler type 1933 dz Auto-tetraploids 1909 (extracted from Crane and Lawrence, 1952) 26 Table 6. Flower traits in 2x and 4x Primula malcoides. 2x wild type 2x cvs 4x cvs no. flowers (main shoot) 41.4 36.5-68.5 48.4-58.9 no. umbels 4.5 3.7-5.6 4.9-6.2 flower size 1.1 1.7-1.9 2.1-2.9 distance between umbels (1/2) 2.1 2.2-3.7 2.4-3.2 Distance : flower size (1/2) 2:1 1.3-2.0 : 1 0.8-1.6 : 1 flowering period [d] 17.8 19.1-26.1 26.1-31.2 Table 7. Polyploidy in Primula malacoides – Allele dosage effects and flower colour. Genotype Relative concentrations HCC Petunidin Malvidin bbbb 1.00 traces 820 bbb+ .63 .37 822 bb++ .34 .66 724 b+++ .08 .92 025 ++++ traces 1.00 27 27 Table 8. Fertility of diploids and tetraploids in Primula malacoides. Cross No. flowers No. seeds total No. seeds per flower 2x B1F1.1 150 2883 19 2x B1F1.2 90 2871 32 4x B1F1.1 150 16080 107 4x B1F1.2 90 3784 42 2x F1 × F1 240 4631 19 4x F1 × F1 240 21415 89 (Data from Skiebe 1958) Table 9. Primula malacoides – number of unreduzed gametes in 2x cultivars. Cross Plants tested 2x gametes eggs pollen per plant 2x x 2x 4489 3 3 .0013 2x x 4x 97 61 0 .6280 4x x 2x 39 0 51 1.3080 Table 10. Frequencies of polyploids in Primula malacoides – results from crosses. Plants tested No. of % 4x 2x 3x 4x 2x x 2x 8476 8471 1 2x x 4x 146 15 31 100 68.4 4x x 2x 47 0 9 38 80.9 28 4 .005 Figures Fig. 1. Origin of the garden forms of narcissi (Wylie, 1952). Fig. 2. Origin of Impatiens Neuguinea cultivars. Origin Madagascar, introduced to Paris 1927 29 Fig. 3. Development of Kalanchoe cultivars. Fig. 4. Origin of cultivated Begonias. 30 Fig. 5. Origin of Begonia semperflorens (Zeilinga, 1962). Fig. 6. Polyploidy in Begonia semperflorens (Skiebe, 1970). 31