Liliaceae - Anthericum Ramosum

The lily family, Liliaceae, consists of about 15 genera and 610 species of flowering plants within the order Liliales. They are monocotyledonous, perennial, herbaceous, often bulbous geophytes. Plants in this family have evolved with a fair amount of morphological diversity despite genetic similarity. Common characteristics include large flowers with parts arranged in threes: with six colored or patterned petaloid tepals (undifferentiated petals and sepals) arranged in two whorls, six stamens and a superior ovary. The leaves are linear in shape, with their veins usually arranged parallel to the edges, single and arranged alternating on the stem, or in a rosette at the base. Most species are grown from bulbs, although some have rhizomes. First described in 1789, the lily family became a paraphyletic "catch-all" ( wastebasket) group of lilioid monocots that did not fit into other families and included a great number of genera now included in other families and in some cases in other orders. Consequently, many sources and descriptions labelled "Liliaceae" deal with the broader sense of the family.

The family evolved approximately 68 million years ago during the Late Cretaceous to Early Paleogene epochs. Liliaceae are widely distributed, mainly in temperate regions of the Northern Hemisphere and the flowers are insect pollinated. Many Liliaceae are important ornamental plants, widely grown for their attractive flowers and involved in a major floriculture of cut flowers and dry bulbs. Some species are poisonous if eaten and can have adverse health effects in humans and household pets.

A number of Liliaceae genera are popular cultivated plants in private and public spaces. Lilies and tulips in particular have had considerable symbolic and decorative value, and appear frequently in paintings and the decorative arts. They are also an economically important product. Most of their genera, ''Lilium'' in particular, face considerable herbivory pressure from deer in some areas, both wild and domestic.

Description

The diversity of characteristics complicates any description of the Liliaceae morphology, and confused taxonomic classification for centuries. The diversity is also of considerable evolutionary significance, as some members emerged from shaded areas and adapted to a more open environment (see Evolution).

General

The Liliaceae are characterised as monocotyledonous, perennial, herbaceous, bulbous (or rhizomatous in the case of Medeoleae) flowering plants with simple trichomes (root hairs) and contractile roots. The flowers may be arranged (inflorescence) along the stem, developing from the base, or as a single flower at the tip of the stem, or as a cluster of flowers. They contain both male (androecium) and female (gynoecium) characteristics and are symmetric radially, but sometimes as a mirror image. Most flowers are large and colourful, except for Medeoleae. Both the petals and sepals are usually similar and appear as two concentric groups (whorls) of 'petals', that are often striped or multi-coloured, and produce nectar at their bases. The stamens are usually in two groups of three (trimerous) and the pollen has a single groove (monosulcate). The ovary is placed above the attachment of the other parts (superior). There are three fused carpels (syncarpus) with one to three chambers (locules), a single style and a three-lobed stigma. The embryo sac is of the ''Fritillaria'' type. The fruit is generally a wind dispersed capsule, but occasionally a berry (Medeoleae) which is dispersed by animals. The leaves are generally simple and elongated with veins parallel to the edges, arranged singly and alternating on the stem, but may form a rosette at the base of the stem.

Specific

; Inflorescence : Usually indeterminate (lacking terminal flower) as a raceme (''Lilium''); sometimes reduced to a single terminal flower (''Tulipa''). When pluriflor (multiple blooms), the flowers are arranged in a cluster or rarely are subumbellate (''Gagea'') or a thyrse (spike).

; Flowers : Hermaphroditic, actinomorphic (radially symmetric) or slightly zygomorphic (bilaterally symmetric), pedicellate (on a short secondary stem), generally large and showy but may be inconspicuous : (Medeoleae). Bracts may (bracteate) or may not (ebracteate) be present. The perianth is undifferentiated ( perigonium) and biseriate (two whorled), formed from six tepals arranged into two separate whorls of three parts (trimerous) each, although ''Scoliopus'' has only three petals, free from the other parts, but overlapping. The tepals are usually petaloid (petal like) and apotepalous (free) with lines (striate) or marks in other colors or shades. The perianth is either homochlamydeous (all tepals equal, e.g. ''Fritillaria'') or dichlamydeous (two separate and different whorls, e.g. ''Calochortus'') and may be united into a tube. Nectar is produced in perigonal nectaries at the base of the tepals.

; Androecium : Six stamens in two trimerous whorls, with free filaments, usually epiphyllous (fused to tepals) and diplostemonous (outer whorl of stamens opposite outer tepals and the inner whorl opposite inner tepals), although ''Scoliopus'' has three stamens opposite the outer tepals. The attachment of the anthers to the filaments may be either peltate (to the surface) or pseudo-basifixed (surrounding the filament tip, but not adnate, that is not fused) and dehisce longitudinally and are extrorse (dehiscing away from center). The pollen is usually monosulcate (single groove), but may be inaperturate (lacking aperture: ''Clintonia'', some ''Tulipa'' spp.) or operculate (lidded: ''Fritillaria'', some ''Tulipa'' spp.), and reticulate (net patterned: ''Erythronium'', ''Fritillaria'', ''Gagea'', ''Lilium'', ''Tulipa'').

; Gynoecium : Superior ovary (hypogynous), syncarpous (with fused carpels), with three connate (fused) carpels and is trilocular (three locules, or chambers) or unilocular (single locule, as in ''Scoliopus'' and ''Medeola''). There is a single style and a three lobed stigma or three stigmata more or less elongated along the style. There are numerous anatropous (curved) ovules which display axile placentation (parietal in ''Scoliopus'' and ''Medeola''), usually with an integument and thinner megasporangium. The embryo sac ( megagametophyte) varies by genera, but is mainly tetrasporic (e.g. ''Fritillaria''). Embryo sacs in which three of the four megaspores fuse to form a triploid nucleus, are referred to as ''Fritillaria-type'', a characteristic shared by all the core Liliales.

; Fruit : A capsule that is usually loculicidal (splitting along the locules) as in the Lilioideae, but occasionally septicidal (splitting between them, along the separating septa) in the Calachortoideae and wind dispersed, although the Medeoleae form berries (baccate). The seeds may be flat, oblong, angular, discoid, ellipsoid or globose (spherical), or compressed with a well developed epidermis. The exterior may be smooth or roughened, with a wing or raphe (ridge), aril or one to two tails, rarely hairy, but may be dull or shiny and the lack of a black integument distinguishes them from related taxa such as Allioideae that were previously included in this family, and striate (parallel longitudinally ridged) in the Steptopoideae. The hilum (scar) is generally inconspicuous. The bitegmic (separate testa and tegmen) seed coat itself may be thin, suberose (like cork), or crustaceous (hard or brittle). The endosperm is abundant, cartilaginous (fleshy) or horny and contains oils and aleurone but not starch (non-farinaceous). Its cells are polyploid (triploid or pentaploid, depending on the embryo sac type). The embryo is small (usually less than one quarter of seed volume), axile (radially sectioned), linear (longer than broad) or rarely rudimentary (tiny relative to endosperm) depending on placentation type, and straight, bent, curved or curled at the upper end.

; Leaves : Simple, entire (smooth and even), linear, oval to filiform (thread-like), mostly with parallel veins, but occasionally net-veined. They are alternate (single and alternating direction) and spiral, but may be whorled (three or more attached at one node, e.g. ''Lilium, Fritillaria),'' cauline (arranged along the aerial stem) or sheathed in a basal rosette. They are rarely petiolate (stem attached before apex), and lack stipules. The aerial stem is unbranched.

; Genome : The Liliaceae include a species with one of the largest genome size within the angiosperms, '' Fritillaria assyriaca'' ( 1C=127.4 pg), while '' Tricyrtis macropoda'' is as small as 4.25 pg. Chromosome numbers vary by genus. Some genera like ''Calochortus'' (x=6-10), ''Prosartes'' (6,8,9,11), ''Scoliopus'' (7,8), ''Streptopus'' (8, 27) and ''Tricyrtis'' (12–13) have a small and variable number of chromosomes while subfamily Lilioideae have a larger and more stable chromosome number (12) as have the Medeoleae (7).

; Phytochemistry : The seeds contain saponins but no calcium oxalate raphide crystals, chelidonic acid (unlike Asparagales) or cysteine derived sulphur compounds (allyl sulphides), another distinguishing feature from the characteristic alliaceous odour of the Allioideae. ''Fritillaria'' in particular contains steroidal alkaloids of the cevanine and solanum type. Solanidine and solanthrene alkaloids have been isolated from some ''Fritillaria'' species. ''Tulipa '' contains tulipanin, an anthocyanin. (see also: Toxicology)

Characteristics often vary by habitat, between shade-dwelling genera (such as ''Prosartes'', ''Tricyrtis'', '' Cardiocrinum'', ''Clintonia'', ''Medeola'', ''Prosartes'', and ''Scoliopus'') and sun loving genera. Shade-dwelling genera usually have broader leaves with smooth edges and net venation, and fleshy fruits (berries) with animal-dispersed seeds, rhizomes, and small, inconspicuous flowers while genera native to sunny habitats usually have narrow, parallel-veined leaves, capsular fruits with wind-dispersed seeds, bulbs, and large, visually conspicuous flowers. (See also ''Evolution'').

Taxonomy

The taxonomy of the Liliaceae has a very complex history. The family was first described in the eighteenth century, and over time many other genera were added until it became one of the largest of the monocotyledon families, and also extremely diverse. Modern taxonomic systems, such as the APG which is based on phylogenetic principles using molecular biology, have redistributed many of these genera resulting in the relatively small family that is currently recognised. Consequently, there are many different accounts of the Liliaceae in the literature and older uses of the term occur commonly. To distinguish between them, the Latin terms ''sensu lato'' and ''sensu stricto'' are frequently used (together with their abbreviations, ''s.l.'' and ''s.s.'') to denote the broader or stricter sense of the circumscription respectively, e.g. Liliaceae ''s.s.''.

History

The family Liliaceae was described by Michel Adanson in 1763 and formally named by Antoine Laurent de Jussieu in 1789. Jussieu defined this grouping as having a calyx of six equal colored parts, six stamens, a superior ovary, single style, and a trilocular (three-chambered) capsule. By 1845, John Lindley, the first English systematist, unhappily acknowledged the great diversity in the circumscription of the family, and that it had expanded vastly, with many subdivisions. As he saw it, the Liliaceae were already paraphyletic ("catch-all"), being all Liliales not included in the other orders, but hoped that the future would reveal some characteristic that would group them better. He recognized 133 genera and 1200 species. By the time of the next major British classification – that of Bentham and Hooker in 1883 (published in Latin) – several of Lindley's other families had already been absorbed into the Liliaceae. Over time the family became increasingly broad and somewhat arbitrarily defined as all species of plants with six tepals and a superior ovary, eventually coming to encompass about 300 genera and 4,500 species within the order Liliales under the Cronquist system (1981). Cronquist merged the Liliaceae with the Amaryllidaceae, making this one of the largest monocotyledon families.

Many other botanists echoed Lindley's earlier concerns about the phylogeny of the Liliaceae, but various schemes to divide the family gained little traction. Dahlgren (1985) suggested there were in fact forty – not one – families distributed over three orders (predominantly Liliales and Asparagales). In the context of a general review of the classification of angiosperms, the Liliaceae were subjected to more intense scrutiny. Considerable progress in plant phylogeny and phylogenetic theory enabled a phylogenetic tree to be constructed for all of the flowering plants, as elaborated by the Angiosperm Phylogeny Group (1998).

Modern APG classification and phylogeny

The Angiosperm Phylogeny Group (APG) made rapid progress in establishing a modern monophyletic classification of the flowering plants by 2009. Despite establishing this relative degree of monophyly (genetic homogeneity) for the family Liliaceae, their morphology remains diverse and there exists within the Liliaceae clade or grouping, a number of subclades (subgroups). Particularly enigmatic were ''Clintonia'', ''Medeola'', ''Scoliopus'', and ''Tricyrtis''.

Of the fifteen genera within the Liliaceae, the ten genera of the Lilioideae subfamily form one morphological group that is characterised by contractile bulbs and roots, and a Fritillaria-type embryo-sac (megagametophyte with four megaspores). Within the Lilioideae, ''Clintonia'' and the closely related ''Medeola'' form a subclade, and are now considered a separate tribe (Medeoleae). The other major grouping consists of the five genera constituting the Streptopoideae (including ''Scoliopus'') and Calochortoideae (including ''Tricyrtis'') subfamilies characterised by creeping rhizomes, styles which are divided at their apices, and by megagametophyte development of the ''Polygonum''-type (a simple megaspore and triploid endosperm) embryo-sac.

Evolution and biogeography

The development of a phylogenetic approach to taxonomy suggested the Liliales formed some of the earliest monocots. Molecular analysis indicates that divergence amongst the Liliales probably occurred around 82 million years ago. The closest sister family to the Liliaceae are the Smilacaceae with the Liliaceae separating 52 million years ago. Liliaceae thus arose during the late (Maastrichtian) Cretaceous to early (Paleocene) Paleogene periods. Major evolutionary clades include the Lilieae (''Lilium, Fritillaria, Nomocharis, Cardiocrinum, Notholirion'') from the Himalayas about 12 mya and the Tulipeae (''Erythronium'', ''Tulipa'', ''Gagea'') from East Asia at about the same time. The Medeoleae (''Clintonia'' and ''Medeola'') may have appeared in North America but were subsequently dispersed, as may have the Streptopoideae and Calochortoideae. Liliaceae fossils have been dated to the Paleogene and Cretaceous eras in the Antarctic.

The Liliaceae probably arose as shade plants, with subsequent evolution to open areas including deciduous forest in the more open autumnal period, but then a return of some species (e.g. '' Cardiocrinum''). This was accompanied by a shift from rhizomes to bulbs, to more showy flowers, the production of capsular fruit and narrower parallel-veined leaves. Again, some reversal to the broader reticulate-veined leaves occurred (e.g. ''Cardiocrinum'').

Subdivisions and genera

Suprageneric subdivisions

Due to the diversity of the originally broadly defined Liliaceae ''s.l.'', many attempts have been made to form suprageneric classifications, e.g. subfamilies and tribes. Classifications published since the use of molecular methods in phylogenetics have taken a narrower view of the Liliaceae (Liliaceae ''s.s.''). The Angiosperm Phylogeny Website (APweb) recognizes three subfamilies, one of which is divided into two tribes.

Genera

Various authorities (e.g. ITIS 16, GRIN 27, WCSP, NCBI, DELTA ) differ on the exact number of genera included in Liliaceae ''s.s.'', but generally there are about fifteen to sixteen genera, depending on whether or not '' Amana'' is included in ''Tulipa'' and ''Lloydia'' in ''Gagea''.

Currently the APWeb lists fifteen genera, arranged as shown in this table:Gagea