1 Origin and Distribution

The genus Lilium L. (family Liliaceae) is constituted of about 110 species dispersed around the world that are distributed between the 100 and 600N in Asia (50 to 60 species), North America (approximately 24 species), and Europe (approximately 12 species) (Bryan, 1989; McRae, 1998; Liang and Tamura, 2000; Wang et al., 2015). All species of Lilium are indigenous to the hilly region of the Northern Hemisphere up to Siberia and South Canada up to Nilgirimountains of India and Florida in the South (Figure 1). Although no fossil record available, Lilium, an important genus of the core Liliales, appears to have evolved approximately 12 million years ago inthe Himalayas(Patterson and Givnish, 2002; Gao et al., 2015). Southwest and north of China is considered natural home for 55 speciesof wild lily and is believed to be its centre of genetic diversity (De Jong, 1974). The East coast of Asia, the West Coast of North America and the Mediterranean region are the three most richly garnished places. Far East is the home of almost half of the world’s lilies and majority of our finest garden lilies originated there. A few species have been found in Northeast India (Liliumwallichianum, L. napalense and L. polyphyllum) also. A species may be either confined like, Lilium regale found only in one Chinese valley; or can be globe-trotter like Liliummartagonwhich is recognized from Siberia across to Poland and down to the Balkans. The trumpet lily(Liliumformosanum) indigenous to Taiwan, grows from sea-level to 3600 m. The worldwide distribution of total lily cultivars and species and their distribution is registered in the lily Register from Wisley, Great Britain from 1960-1993 (Table 1 and Table 2) (Mynett, 1996).

2 History

With a history across thousands of years, the lily has been recognized in almost every sphere of human existence. Going back through the ages, various descriptions have been given referring to lilies. The early European writer, Pliny the Elder (23-73AD) expressed this flower as being ‘as far and noble as the rose’; an opinion that has been shared by others including Wahlafrid Strabo, Bartholomew, Mattioli and Holland. Dioscorides, a Greek herbalist in the 1st Century, observed the medicinal virtues of lilies, namely that of Liliumcandidum and healing qualities of other types were also recognized by Asian and American civilizations. The lily was favoured by both the Greek and Romans, and later became a sacred symbol in the monastery gardens of the Middle Ages, featuring in many herbals and illuminated manuscripts. By the 17th century, several different lilies were known in the European regions such as L. chalcedonicum, L. martagon, L. bulbiferum and L. candidum, and these were depicted in the works of Parkinson and Gerard. However, it was the botanical expeditions that various plant collectors undertook to Asia in the 1800s and 1900s, that led to the discovery of many species of lily in China and Japan. Bulbs were shipped to Europe and England in vast numbers and introduced into gardens by plant nurseries. Since that time, lily species have spread throughout the world and many still retain their status as popular garden subjects, despite being sidelined by the ever growing number of hybrids. Lilium regale, L. longiflorum, L. auratum, L. candidum, and L. lancifolium are several examples of these. Meanwhile, for some native species existing in the wild, it is a matter of trying to survive the often harsh results that human intrusion brings.

3 Botany

Lilium is an herbaceous perennial from family Liliaceae and subclass Monocotyledonae. These are generally propagated by bulbs, composed of fleshy scales which act as store for food reserves, helping in growth during the subsequent season. The scaled are attached to the short stems also known as axis or basal plate. It is the most important segment from which roots emerges; also scales, and new growth buds arise from this region. Lilium specie can be identified from its scale’s colour but this may vary on exposure to light. Lilium bulb may be either concentric or rhizomatous, while most European and Asiatic lilies have concentric bulbs. Some species such asLiliumlankongense, L. nepalense, and L. wilsonii, have stoloniferous habit wherethe stem bear bulblets away from the mother bulb as it travels underground for some distance before emerging. The Eastern American species (L. canadense, L. michiganense, and L. superbum) shows best development of rhizomatous type bulb while the Western American species, L.pardalinum and L. parryiare some typical examples of modification of rhizomatous type of bulbs.

Length of mature lilies’ flowering stem may vary from few inches in Liliumnanum or other high alpine species, to as tall as 250 cm, in Liliumleucanthum var. centifolium or L. superbum. The stems may arise straight from the bulb, as in L. regale or may travel some distance horizontally undergroundbefore emerging, as in L. lankongense and L. nepalense. The leaves may be eitherlanceolate (broad) as in L. auratum var. platyphyllum or may be narrow grass like, as in L.pumilum. In most of the oriental or trumpet species the leaves are alternately arranged or they might be arranged in whorl, as some North American species while in some species, such as L. taliense, a naked, asparagus-like stem is produced that rises 30 cm or more before the leaves expand. Whorling of leaves is also noticed in L. candidum and L. x testaceum, but their leaves size reduces from the base upward. Small purple bulbils in the axils of leaves are also observed in some species e.g. L. lancifolium.

The lily inflorescence may be a raceme, an umbel, or a single terminal flower. A great deal of vividness in form and colour is observed which adds on to the attractiveness of the genus. Trumpet (Lilium longiflorum and L. regale), Turk’s-cap (Liliummartagon), and bowl shaped (Liliumauratum) are the basic forms. Lilies are also distinguished as per the carriage of the flower being upright, pendant or outfacing. Flowers possess six stamens consisting of slender filaments which bears anther containing the pollens. Lily pollen may be soft yellow to dark brown in colour depending on the species or hybrid. Stigma is tri-lobed borne at the tip of long slender style, with an ovary at the base. Nectar is secreted from the nectar furrow present in most species, as a groove at the base of each tepal;to attract pollinating insects and birds. 

Seeds are flat contained in structures called, capsules, which may be either short as in Liliumcandidum or long, slender capsule as in L. formosanum.The capsule is divided into three sections each containing seeds stacked in two rows; which are separated by thin papery divisions. A fertile seed can be distinguished by the presence of a dark mass at the centre of the seed, which is marked as the line through the endosperm. Seeds of few species have papery extensions or wings for facilitating easy dispersal by wind such as those of Liliumauratum or the wing tissue might be very little as those of L. polyphyllum.

4 Classification and Species

Comber (1949) divided the genus Lilium into seven taxonomic sections Martagons (5 species), Americans or Pseudolirium (21 species), Lilium/Candidum/Liriotypus (15 species), Orientals or Archelirion (7 species), Asiatics or Sinomartagon (46 species), Trumpets or Leucolirion (11 species), and Daurolirion or Oxypetala (2 species), based upon 15 morphological and physiological attributes, which was later revised by Lighty (1968) and De Jong (1974). Origin and distribution of each species within each section is shown in Table 3.

5 Hybrid Lilies

All lilies species and their hybrids belong to the genus ilium. There are nine groups under which they are defined and maintained by the International Lily Register. The name of these divisions gives a broad indication of the attributes of the hybrids (Table 4).

The Archelirion, Leucolirion and Sinomartagon are considered to be the major economic groups due to availability of greater genetic diversity and vivid morphological characteristics. The wild species (2n=2x=24) yields fertile hybrids within each sections and are more or less crossable (McRae, 1990; Van Tuyl et al., 2002). Thehybridization within these three sections has led to development of five prime lily cultivar groups viz; Asiatic, Longiflorum, Oriental, Longiflorum x Asiatic and Longiflorum x Oriental (Figure 2 and Table 5).

1. The white trumpet-shaped flowers of longiflorum hybrids possesing distinctive fragrance, which can be cultivated all round the year originated as a resultof intra or interspecific hybridization among the Leucolirion sections i.e. LiliumlongiflorumThunb. × Liliumformosanum Wallace. (McRae, 1990).
2. The cultivation of Asiatic hybrids can be tracked down to the early 1800s in Japan, which are obtained as a result of inter or intra-specific hybridization among at least 12 species of the Sinomartagon section (Shimizu, 1987).During the 1930s and early 1940s, the Mid-Century hybrids developed at Oregon bulb Farms, the United States, were a great achievement in Asiatic hybrids (McRae, 1998). Besides possessing a wide array of colours with diverse flowering periods (Woodcock and Stearn, 1950) few of the species of this section showed resistance to Fusarium and viruses (McRae, 1998).
3. The fragrant Oriental hybridsare cultivated and used in breeding since 1950s. These were derived frominter or intra-specific crosses among five species of Archelirion. (McRae, 1998). Majority of oriental hybrids are resistant to Botrytis.

6 Breeding and Domestication

Lily is grown throughout the world, as one of the most significant flowering crop from past fifty years. Within the first decade of the 20^th century, interspecific cross among the section Sinomartagon including Liliummaculatum, L. davidii, L. dauricum, L. bulbiferum and L. tigrinum was performed by Japan and the US (De Graaff, 1970). The importance of lily crop was discovered in 1970 and thereafter several hybrid groups, such as, the ‘Harlequin hybrids’, ‘the Mid-Century hybrids’, the ‘Preston hybrids’, and the ‘Patterson hybrids’, etc. were developed (De Graaff, 1970; McRae, 1998; Rockwell et al., 1961). In 1944, Jan de Graaffbred a Mid-Century Hybrid ‘Enchantment’ which proved to be a turning point and revolutionized lily breeding and cultivation. Little later, after the World War II the Dutch too began with their Lily breeding program. Presently, most of the lily cultivars grown are polyploids.

For over 30 years, Asiatic hybrids were the prominent cultivars. During this period the interspecific hybridization of predominantly L. auratum and L. speciosumof the section Archelirion, gave rise to thy oriental hybrids. Large sized lily flowers, predominantly pink and white in colour were introduced, from which, a Minnesota breeder Leslie Wood riff bred the upward facing Oriental hybrids, which predominated for over 25 years.

Assortments of intersectional hybrids were produced using various pollination techniques such as cut styles, embryo rescue and polyploidization (Asano, 1978, 1980; Asano and Myodo, 1977a, b; Van Tuyl et al., 1991; Lim, 2000; Barba-Gonzales, 2005; Barba-Gonzalez et al., 2006). Thestarting array of intersectional hybrids Longiflorum x Asiatic hybrids or LA hybrids were produced as a result of interspecific hybridization among various sections; about 20 years later than the Oriental hybrids. Repeated backcrossing of chromosome doubled F1 LA hybrid with an Asiatic hybrid has rendered them, triploid. Recently these hybrids have replaced the Asiatic hybrid group attaining an imperative position in the market.

The breeding of other intersectional crosses, primarily triploid hybrids like OA (Oriental x Asiatic hybrids), OT (Oriental x Trumpet) and LO (Longiflorum x Oriental), began. The replacement of Orientals by the recent OTs can be predicted from the earlier experiences of the LA-hybrids largely taking the place of the Asiatic hybrids and the Longiflorums replaced by LO-hybrids. Apart from the major seven groups of lily hybrids (O, A, L, T, LA, LO and OT), various other successful breeding of species occurred. The interspecific crosses of L. candidum with L. longiflorum and L. henryii were excluded from this assortment. Several other crosses were made using Longiflorum as the female and species like L. auratum, L. bakerianum, L. canadense, L. concolor, L. dauricum, L. henryii, L. kelloggii, L. lankongense, L. lophophorum, L. monadelpum, L. martagon, L. hansonii, L. nepalense, L. pardinum, L. pumilum and L. semper vivoideum as male parent. Similarly, L. dauricum, L. nepalense and L. pardalinum were used as male with Oriental as the female parent.

Cultivar ‘Stargazer’ was the topmost grown cultivar for over 25 years. Lily varieties are protected by Plant Breeder’s Rights, while only Star Gazer was excluded from this right. Tissue culture techniques have come into vogue for the development of fresh lily cultivars. The assortment shifts, as witnessed from the past trends, for the future development of several other groups, breeding attempts have major contribution. The OT and the Longiflorum hybrids may most likely be replaced by the Orientals and the LO-hybrids in the forthcoming years. Several Crossed species: L. hansonii and L. martagon (section Martagon), L. candidum and L. monadelpum (section Lilium), L. canadense and L. pardalinum (section Pseudolirium), L. bakerianum, L. nepalense and L. henryi are potential species to be used in developing new groups. Transfer of desirable traits from wild species to the array is being carried with the assistance of Molecular cytogenetics (Lim, 2000; Barba-Gonzalez, 2005; and Khan, 2009) and molecular assisted breeding (Shanin et al., 2009).

Genetic transformation is another tool being sought after in lily for over 25 years (Cohen, 2011). It is widely used in Genetic studies although no cultivar has been developed till date using genetic transformation. Detailed genetic maps including 6 QTLs for Fusarium-resistance, of two lily populations, were published (Shain et al., 2010). The wide genetic variation already accessible to breeder can be manifested for mixing of different desirable traits into one, through the practical understanding of DNA-sequences linked to horticultural traits.

7 Cytogenetics

Lily has been long used as a model plant by various cytogeneticsts since Strasburger (1880), for chromosomal studies including the description of meiotic stages, crossing over (Fogwill, 1958; Stern and Hotta, 1977) and duration of female meiotic stages (Bennett and Stern, 1975), chromosome banding (Holm, 1976; Son, 1977; Song, 1987; 1991), fertility of interspecific hybrids (Brock, 1954; Asano, 1984), Synaptonemal complexes (Holm and Rasmussen, 1984; Anderson et al., 1994) and chromosome morphology (Sato, 1932; Stewart, 1947; Noda, 1978; Stack, 1991 and others). The basic chromosome number of all the lilium species is x=12 having two metacentric whereas 10 acro-centric chromosomes. The genome size of Lilium species varies from 69.5pg/2C (Lilium henryi) up to 96 pg/2C (Liliumparryi) (Bennet and Smith, 1991; Van Tuyl and Boon, 1997). The basic nomenclature of Lilium karyotypes is based on the order of chromosomes in sequences of decreasing short-arm length; with 1 representing the longest short arm and 12 the shortest (Stewart, 1947; Lim et al., 2000). Both diploids and triploids are found in L. lancifolium alone while all the other species are diploid. Van Tuyl and Boon (1997) studied the variation in DNA content within the genus Lilium. It was discovered that interspecific hybrids generally have intermediate DNA content to that of parents. Lilium longiflorum has been a model crop for studying gametophytic self incompatability due to presence of strong S.I. mechanism.

8 Molecular Breeding and Physical Mapping in Lilium

Species of the genus Lilium have the largest genomes among plants except Fritillaria (Bennett and Smith 1991) and have been extensively used for cytological analysis in the past (Mather, 1940; Stewart, 1947; Brown and Zohary, 1955; Fogwill, 1958; Bennett and Stern, 1975; Noda, 1991). Nevertheless, no reliable molecular or cytogenetic maps are available for lily so far. At present, breeding programs aim at combining desirable traits within different plant species complexes and are mainly focused on introgression procedures (Kosmala et al., 2006 and 2007). The main thrustarea is the transfer of genes conferring to a particular trait from a wild species into a cultivar. Markers associated with genes conferring particular characters can facilitate the marker-assisted selection program to obtain new cultivars with desired traits. For this purpose, genetic or molecular maps have been constructed in several crops and integrated in cytogenetic maps of respective genomes (Khrustaleva et al., 2005; Humphreys et al., 2005).

Multiple approaches have been used to develop integrated maps, primarily by combining the information from molecular maps and physical distribution of these markers in the genome through cytogenetic techniques. Such maps are constructed by insertion of large DNA clones like yeast artificial chromosomes (YAC) and bacterial artificial chromosomes (BAC) and comparison of these maps with genetic maps (Wu et al., 2003). The other techniques used are in situ hybridization of BACs and YACs on plant chromosomes with recombination maps (Kulikova et al., 2001). One of the current developments in lily breeding is the introduction of molecular breeding techniques for the incorporation of disease resistances in commercially successful lily cultivars. Fusarium, Botrytis and virus (LMoV) resistance are the most important goals in lily breeding. Screening methods to determine resistance against these pathogens in several lily cultivars have been developed (Straathof and Van Tuyl, 1994; Straathof and Löffler, 1994). However, it takes a long time before resistance symptoms become visible, and therefore, faster selection methods are needed.

In lily molecular marker techniques have been used for the identification of cultivars and interspecific hybrids (Yamagishi, 1995; Yamagishi et al., 2002), identifying genetic diversity (Arzate-Fernández et al., 2005), genetic analysis of anthocyanin pigmentation (Abe et al., 2002) and for finding RAPD-markerslinked to Fusariumoxysporumresistance in Asiatic hybrids (Straathofet al. 1996). Van Heusden et al. (2002) used AFLPs and a QTL approach to locate markers linked to LMoV virus on Asiatic genome. A total of 251 AFLP markers based on 100 descendents of a lily backcross population were used for the construction of a genetic map. Based on these approaches it was found that LMoV (TBV) resistance was clearly a monogenic trait and could reliably be mapped on linkage group 9. Despite the difficult screening for Fusarium resistance, four significant QTLs were mapped to linkage groups 1, 5, 13 and 16 respectively.

Insertion of genes that are absent in lily can be achieved through techniques genetic transformation. Several researchers have successfully accomplished both Agrobacterium and microprojectile mediated transformation in lily (Bino et al., 1992; Van der Leede-Plegt et al., 1992; Watad et al., 1998). The GUS gene was successfully transmitted into next generation. For future applications, a marker-free system is required.

Du et al., (2017) sequenced nine Lilium chloroplast genomes and retrieved seven published chloroplast genomes for comparative and phylogenetic analyses. The genomes ranged from 151,655 bp to 153,235 bp in length and had a typical quadripartite structure with a conserved genome arrangement and moderate divergence. A comparison of sixteen Lilium chloroplast genomes revealed ten mutation hotspots. Single nucleotide polymorphisms (SNPs) for any two Lilium chloroplast genomes ranged from 8 to 1,178 and provided robust data for phylogeny. Except for some of the shortest internodes, phylogenetic relationships of the Lilium species inferred from the chloroplast genome obtained high support, indicating that chloroplast genome data will be useful to help resolve the deeper branches of phylogeny.

9 Utilization of Genetic Diversity

Germplasm conservation is necessary to prevent genetic erosion or narrowing of genetic base to protect endangered species from getting extinct and availability of genetic material for developing new superior varieties. Conservation is done keeping in view the requirements for future generations aiding in survival. A great deal of genetic variation and novel horticultural traits, are present in lily with approximately 7000 cultivars available in the market or wild. Commercially important characters include:

Resistance against various pests and pathogens such as Fusarium, Botrytis and several viruses (TBV, LSV and LVX).

Novel attributes such as vibrant colour, flower shape, size, sturdy stem, form and fragrance.

Physiological characteristics such as low-light intensity and heat tolerance, precocious flowering, leaf scorch, year-round forcing ability, long shelf life, and bulb growth speed. Some well-known examples of valuable characters among species and different sections shown in Table 5.

Blending or introgression of different desirable traits from an alien species into a single cultivar is done through interspecific hybridization or recurrent back crossing. Presence of pre and post fertilization barriers in lilium species is a major challenge for its interspecific hybridization. Although interspecific hybridization has successfully developed hybrids using methods, such as cut style pollination, embryo rescue and ovule culture (Van Tuyl et al., 1991; 2000). Utilization of novel techniques like mentor pollination ovary and ovule culture and in vitro pollination has helped in producing numerous interspecific hybrids in 80s and 90s (Van Tuyl et al., 1982; 1988; 1991; Wolf and Van Tuyl, 1984).

Skim (1942) used embryo culture to develop plants from L.henryi x L.regale. Immature hybrid embryos between L. ‘Shikayama’ x L. henryi and L. longiflorum x L. ‘Sugehime’ were reported by Asano and Myodo (1977b).  Ascher (1973a, b) successfully obtained the plants of L. ‘damson’ x L. longiflorum. Asano (1980) developed several hybrids between L. longiflorum x L. candidum, L. longiflorum x L. dauricum, L. longiflorum x L. candidum, L. longiflorum x L. amabile, and L. longiflorum x L. pumilum, x L. ‘Sasatame’ x L. henryi, L. ‘Royal Gold’ x L. speciosum and L. regale x L.  leichtliniimaximowiczii through interspecific hybridization. Later, Van Tuyl and coworkers (1991 and 2002) obtained numerous intersectional hybrids successfully. Examples include L. longiflorum x L. canadense (Pseudolirium section); L. longiflorum (Leucolirion section) x L. monadelphum (Lilium section), L. longiflorum x L. martagon (Martagon section), L. longiflorum x L. lankongense (Sinomartagon section), L. longiflorum x L. rubellum (Archelirion section), L. longiflorum x Oriental hybrids, Oriental x Asiatic hybrids.

The cultivar ‘Black Beauty’ was developed by crossing L. speciosum var. rubrum x L. henryi which turned out to be infertile and tetraploid. Lilium cv. ‘Arc Besque’ developed by crossing ‘Black Beauty’ (4n) x ‘Journey End’ (4n), which is six feet tall has intense red flat spreading tepals about 8 inches from tip to tip and is usually disease resistant. The first pink coloured Easter lily ‘Rote Horn’ was developed by hybridizing L .longiflorum and L. elegans (Asano and Nyoda, 1978). ‘Yukinohikari’ developed by Takizawa (1977) is a hybrid of L. formolongi x L. auratum and consequently displays vigorous growth and multiple flowers from a small bulb. ‘Elegant lady’ (triploid LLR), developed as a result of interspecific hybridization among L. longiflorum and a LLRR F1 interspecific hybrid is a successful example. It is an early flowering; fragrant hybrid which bears a pink coloured, tubular flower. GISH confirms the presence of several recombinant chromosomes between the L and A genomes as in the LA hybrid ‘Fangio’(2n=3x=36; triploid, A genome=24, L genome=12). Techniques such have embryo culture and cut style pollination have been utilized for developing Asiatic hybrid lilies such as ‘Li-9’ (‘Mona’ x L. concolor var pulchellum) which produces multiple scapes per bulb (Oomiya et al., 2005). Mynett (2007) obtained a yellow and orange late flowering cultivar in Asiatic lilies by crossing ‘Yellow Blaze’ very late flowering cultivar and L. wilsonii. The Akita Perfectural Agricultural Experiment Station, Japan has developed a series of Asiatic hybrids that are male sterile (Shibata, 2002). “Akita Petit White’ was the first male sterile cultivars released commercially by this station followed by ‘Akita Petit Lemon’, Akita Petit Gold’ and ‘Akita Petit Cream’ having yellow perianth were released (Asari et al., 2005). These were the selection from the progeny of reciprocal crosses between two Asiatic lilies, ‘Connecticut King’ and ‘Menton’. Korea released new FA hybrid ‘Supia’ and FAA hybrid ‘Pink Pearl’. Few new FO hybrid lines, ‘FO 03-16’ line, OA hybrid ‘OA 05-1’ line, and OH hybrid ‘OH 02-1’ line were also developed at Korea (Rhee and Kim, 2008).

10 Conclusion

Lilium is one of the important genus of geophytes widely grown throughout the world. The genus possess a great genetic diversity in many valuable horticultural traits which is manifested in flower colour, forms, shape, fragrance, resistance to diseases, and many physiological characteristics. It is important to conserve available diversity existing among the genus, to breed better and superior quality new cultivars. From the past trend the popularity of large flowered Orientals taking over the Asiatic hybrids in 1970s and 1980s, it can be assumed that there is need for more complex hybrids as demonstrated by The LA-hybrids. Recently, various FO, LO, OT and OA hybrids are emerging. With the same pace, an indistinguishable group of hybrid lilies shall developed possessing nearly similar characters for various species and hybrids group. Several advanced techniques like GISH/FISH-techniques and molecular assisted breeding shall be utilized for breeding for novel characteristicssuch as resistance to virus, Botrytis, Fusarium etc. Furthermore, chloroplast genome data may help to better understand the concept of evolution and adaption further assisting in development and resolving the deeper phylogeny.

Authors’ contributions

All the authors have equally contributed in the compilation and checking of the manuscript.

Acknowledgements

The authors are highly thankful to the Indian Council of Agricultural Research, New Delhi for supporting of this research programme.

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