EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, thalloid, with single-celled apical meristem, showing gravitropism; rhizoids +, unicellular; acquisition of phenylalanine lysase [PAL], phenylpropanoid metabolism [lignans +, flavonoids + (absorbtion of UV radiation)], xyloglucans +; plant [protoplasm dessication tolerant], ectohydrous [free water outside plant physiologically important]; cuticle +; cell wall also with (1->3),(1->4)-ß-D-MLGs [Mixed-Linkage Glucans]; chloroplasts per cell, lacking pyrenoids; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles in vegetative cells 0, metaphase spindle anastral, predictive preprophase band of microtubules, phragmoplast + [cell wall deposition spreading from around the spindle fibres], plasmodesmata +; antheridia and archegonia jacketed, stalked; spermatogenous cells monoplastidic; blepharoplast, bicentriole pair develops de novo in spermatogenous cell, associated with basal bodies of cilia [= flagellum], multilayered structure [4 layers: L1, L4, tubules; L2, L3, short vertical lamellae] + spline [tubules from L1 encircling spermatid], basal body 200-250 nm long, associated with amorphous electron-dense material, microtubules in basal end lacking symmetry, stellate array of filaments in transition zone extended, axonemal cap 0 [microtubules disorganized at apex of cilium]; male gametes [spermatozoids] with a left-handed coil, cilia 2, lateral; oogamy; sporophyte dependent on gametophyte, embryo initially surrounded by haploid gametophytic tissue, plane of first division horizontal [with respect to long axis of archegonium/embryo sac], suspensor/foot +, cell walls with nacreous thickenings; sporophyte multicellular, with at least transient apical cell [?level], sporangium +, single, dehiscence longitudinal; meiosis sporic, monoplastidic, microtubule organizing centre associated with plastid, cytokinesis simultaneous, preceding nuclear division, sporocytes 4-lobed, with a quadripolar microtubule system; spores in tetrads, sporopollenin in the spore wall, initially laid down in association with several trilamellar layers [white-line centred layers, i.e. walls multilamellate]; nuclear genome size <1.4 pg, LEAFY gene present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes.
Many of the bolded characters in the characterization above are apomorphies of subsets of streptophytes along the lineage leading to the embryophytes, not apomorphies of crown-group embryophytes per se.
All groups below are crown groups, nearly all are extant. Characters mentioned are those of the immediate common ancestor of the group,  contains explanatory material, () features common in clade, exact status unclear.
Abscisic acid, ?D-methionine +; sporangium with tapetal layer, columella + [developing from endothecial cells], seta developing from basal meristem [between epibasal and hypobasal cells; stomata +, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and in rhizoids/root hairs; spores trilete; polar transport of auxins and class 1 KNOX genes expressed in the sporangium alone; shoot meristem patterning gene families expressed; MIKC, MI*K*C* and class 1 and 2 KNOX genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns.
[Anthocerophyta + Polysporangiophyta]: archegonia embedded/sunken in the gametophyte; sporophyte long-lived, chlorophyllous; sporophyte-gametophyte junction interdigitate, sporophyte cells showing rhizoid-like behaviour.
Sporophyte branched, branching apical, dichotomous; sporangia several, each opening independently; spore walls not multilamellate [?here].
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Photosynthetic red light response; plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; (condensed or nonhydrolyzable tannins/proanthocyanidins +); sporophyte soon independent, dominant, with basipetal polar auxin transport; lignins +; vascular tissue +sieve cells + [nucleus degenerating], tracheids +, in both protoxylem and metaxylem, plant endohydrous [physiologically important free water inside plant]; endodermis +; stem with an apical cell; branching dichotomous; leaves spirally arranged, blades with mean venation density 1.8 mm/mm2 [to 5 mm/mm2]; sporangia adaxial on the sporophyll, derived from periclinal divisions of several epidermal cells, wall multilayered [eusporangium]; columella 0; tapetum glandular; gametophytes exosporic, green, photosynthetic; basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; placenta with single layer of transfer cells in both sporophytic and gametophytic generations, root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Sporophyte branching ± indeterminate; root apex multicellular, root cap +, lateral roots +, endogenous; endomycorrhizal associations + [with Glomeromycota]; G-type tracheids +, with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangia borne in pairs and grouped in terminal trusses, dehiscence longitudinal, a single slit; cells polyplastidic, microtubule organizing centres not associated with plastids, diffuse, perinuclear; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; LITTLE ZIPPER proteins.
Sporophyte woody; lateral root origin from the pericycle; branching lateral, meristems axillary; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
Plants heterosporous; megasporangium surrounded by cupule [i.e. ovule +, cupule = integument]; pollen lands on ovule; megaspore germination endosporic [female gametophyte initially retained on the plant].
EXTANT SEED PLANTS / SPERMATOPHYTA
Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins particularly with guaiacyl and p-hydroxyphenyl [G + H] units [sinapyl units uncommon, no Maüle reaction]; root stele with xylem and phloem originating on alternate radii, cork cambium deep seated; shoot apical meristem interface specific plasmodesmatal network; stem with vascular cylinder around central pith [eustele], phloem abaxial [ectophloic], endodermis 0, xylem endarch [development centrifugal]; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; cork cambium superficial; leaves with single trace from vascular sympodium [nodes 1:1]; stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; axillary buds exogenous, (none; not associated with all leaves); prophylls two, lateral; leaves with petiole and lamina, development basipetal, blade simple; plant heterosporous, sporangia borne on sporophylls, sporophylls spiral; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], primexine + [involved in exine pattern formation and deposition of sporopollenin from tapetum], exine and intine homogeneous; megasporangium indehiscent; ovules unitegmic, parietal tissue 2+ cells across, megaspore tetrad linear, functional megaspore single, chalazal, sporopollenin 0; gametophytes dependent on sporophyte, apical cell 0, rhizoids 0; male gametophyte development initially endosporic, tube developing from distal end of grain, gametes two, developing after pollination, with cell walls; female gametophyte initially syncytial, walls then surrounding individual nuclei; embryo cellular ab initio, endoscopic, plane of first cleavage of zygote transverse, suspensor +, short-minute, embryonic axis straight [shoot and root at opposite ends; plant allorhizic], cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, whole nuclear genome duplication [zeta duplication], two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.
ANGIOSPERMAE / MAGNOLIOPHYTA
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANITA grade?], lignin also with syringyl units common [G + S lignin, positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], hemicelluloses as xyloglucans; root apical meristem intermediate-open; root vascular tissue oligarch [di- to pentarch], lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0, hypodermis suberised and with Casparian strip [= exodermis +]; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, associated gelatinous fibres [g-fibres] with innermost layer of secondary cell wall rich in cellulose and poor in lignin; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, cytoplasm not occluding pores of sieve plate, companion cell and sieve tube from same mother cell; sugar transport in phloem passive; nodes 1:?; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance to increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, venation hierarchical-reticulate, secondary veins pinnate, veins (1.7-)4.1(-5.7) mm/mm2, endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, ± haplomorphic; protogynous; parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P +, members each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], sporangium pairs dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, endothecium +, endothecial cells elongated at right angles to long axis of anther; (tapetum glandular), cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine lamellate only in the apertural regions, thin, compact; nectary 0; carpels present, superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus at most short [shorter than ovary], hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, stigma wet, extragynoecial compitum +; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across [crassinucellate], nucellar cap?; megasporocyte single, hypodermal, functional megaspore, chalazal, lacking cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; ovule not increasing in size between pollination and fertilization; pollen grains land on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollen tube elongated, unbranched, growing between cells, growth rate (20-)80-20,000 µm/hour, apex of pectins, wall with callose, lumen with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, cilia 0, siphonogamy; double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; mature seed much larger than ovule when fertilized, small , dry [no sarcotesta], exotestal; endosperm diploid, cellular, heteropolar [micropylar and chalazal domains develop differently, first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous; dark reversal Pfr → Pr; Arabidopsis-type telomeres [(TTTAGGG)n]; nuclear genome size <1.4 pg [1 pg = 109 base pairs], whole nuclear genome duplication [epsilon duplication]; protoplasm dessication tolerant [plant poikilohydric]; ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, paleo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]].
[NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]]: wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; pollen monosulcate [anasulcate], tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.
[AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood +; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; carpels plicate; nucellar cap + [character lost where in eudicots?]; 12BP [4 amino acids] deletion in P1 gene.
[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; sesquiterpene synthase subfamily a [TPS-a] [?level], polyacetate derived anthraquinones + [?level]; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [possible position]; pollen tube growth intra-gynoecial [extragynoecial compitum 0]; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid.
[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (extra-floral nectaries +); (veins in lamina often 7-17 mm/mm2 or more [mean for eudicots 8.0]); (stamens opposite [two whorls of] P); (pollen tube growth fast).
MONOCOTYLEDONS / MONOCOTYLEDONEAE / LILIANAE Takhtajan
Plant herbaceous, perennial, rhizomatous, growth sympodial; non-hydrolyzable tannins [(ent-)epicatechin-4] +, neolignans, benzylisoquinoline alkaloids 0, hemicelluloses as xylans; root apical meristem?; root epidermis developed from outer layer of cortex; trichoblasts in atrichoblast [larger cell]/trichoblast cell pairs, the former further from apical meristem, in vertical files; endodermal cells with U-shaped thickenings; cork cambium in root [uncommon] superficial; stele oligo- to polyarch, medullated [with prominent pith], lateral roots arise opposite phloem poles; primary thickening meristem +; vascular bundles in stem scattered, (amphivasal), vascular cambium 0 [bundles closed]; tension wood 0; vessel elements in root with scalariform and/or simple perforations; tracheids only in stems and leaves; sieve tube plastids with cuneate protein crystals alone; stomata parallel to the long axis of the leaf, in lines; prophyll single, adaxial; leaf blade linear, main venation parallel, the veins joining successively from the outside at the apex, transverse veinlets +, unbranched [leaf blade characters: ?level], vein/veinlet endings not free, margins entire, Vorläuferspitze +, base broad, ensheathing the stem, sheath open, petiole 0, colleters + ["intravaginal squamules"]; inflorescence terminal, racemose; flowers 3-merous [6-radiate to the pollinator], polysymmetric, pentacyclic; P = T, each with three traces, median T of outer whorl abaxial, aestivation open, members of whorls alternating, [pseudomonocyclic, each T member forming a sector of any tube]; stamens = and opposite each T member [primordia often associated, and/or A vascularized from tepal trace], anther and filament more or less sharply distinguished, anthers subbasifixed, endothecium from outer secondary parietal cell layer, inner secondary parietal cell layer dividing; pollen reticulations coarse in the middle, finer at ends of grain, infratectal layer granular; G , with congenital intercarpellary fusion, opposite outer tepals [thus median member abaxial], placentation axile; ovule with outer integument often largely dermal in origin, parietal tissue 1 cell across; antipodal cells persistent, proliferating; fruit a loculicidal capsule; seed small to medium sized [mean = 1.5 mg], testal; embryo long, cylindrical, cotyledon 1, apparently terminal, with a closed sheath, unifacial [hyperphyllar], both assimilating and haustorial, plumule apparently lateral; primary root unbranched, not very well developed, stem-borne roots numerous, hypocotyl short, (collar rhizoids +); no dark reversion Pfr → Pr; duplication producing monocot LOFSEP and FUL3 genes [latter duplication of AP1/FUL gene], PHYE gene lost.
[ALISMATALES [PETROSAVIALES [[DIOSCOREALES + PANDANALES] [LILIALES [ASPARAGALES + COMMELINIDS]]]]]: ethereal oils 0; raphides + (druses 0); leaf blade vernation supervolute-curved or variants, (margins with teeth, teeth spiny); endothecium develops directly from undivided outer secondary parietal cells; tectum reticulate with finer sculpture at the ends of the grain, endexine 0; (septal nectaries + [intercarpellary fusion postgenital]).
[PETROSAVIALES [[DIOSCOREALES + PANDANALES] [LILIALES [ASPARAGALES + COMMELINIDS]]]]: cyanogenic glycosides uncommon; starch grains simple, amylophobic; leaf blade developing basipetally from hyperphyll/hypophyll junction; epidermis with bulliform cells [?level]; stomata anomocytic, (cuticular waxes as parallel platelets); colleters 0.
[[DIOSCOREALES + PANDANALES] [LILIALES [ASPARAGALES + COMMELINIDS]]]: nucellar cap 0; endosperm nuclear [but variation in most orders].
[LILIALES [ASPARAGALES + COMMELINIDS]]: (inflorescence branches cymose); protandry common.
Age. The age of this node is ca 124 m.y. by Janssen and Bremer (2004), rather older than the estimates in Bremer (2000); (Wikström et al. 2001) proposed an age of (116-)111, 102(97) m.y., Magallón and Castillo (2009) suggested ages of 135.7 and 120.1 m.y., and Magallón et al. (2013, 2015) ages of around 96.1 m.y.a. and ca 116.9 m.y.a. respectively; estimates are (131-)122(-109) m.y. in Merckx et al. (2008a), 121-97 m.y. in Mennes et al. (2013, see also 2015), around 106 or 95 m.y. in S. Chen et al. (2013), ca 123 m.y. in Givnish et al. (2014b) and (125-)117, 116(-111) m.y. in Hertweck et al. (2015: c.f. ages for [Asparagales + commelinids]).
Phylogeny. For discussion on the relationships of Liliales, see Petrosaviales.
LILIALES Perleb Main Tree.
(Plants geophytes); storage fructans, chelidonic acid, steroidal saponins +; root hairs from unmodified rhizodermal cells, (velamen +); (cuticular waxes as platelets transversely arranged in parallel series); leaf blades elliptical, (main veins seven or fewer); inflorescence terminal; T large (small), free, (spotted), tepal nectaries +; anthers extrorse; style often long, stigma capitate; ovules many/carpel, parietal tissue none, nucellar cap +; P deciduous; tegmen with cellular structure; endosperm with thick pitted walls, hemicellulosic; mitochondrial sdh3 gene lost. - 10 families, 67 genera, 1,558 species.
Note: (....) denotes a feature common in the clade, exact status uncertain, [....] includes explanatory material. Possible apomorphies are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is partly because many characters show considerable homoplasy, in addition, basic information for all too many is very incomplete, frequently coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there is the not-so-trivial issue of how ancestral states are reconstructed (see above).
Age. Crown group Liliales were dated to ca 117 m.y. by Janssen and Bremer (2004), rather older than the estimates in Bremer (2000: Campynemataceae sister to the rest); estimates are (131-)118(-78) m.y. in Merckx et al. (2008a), 100 m.y.a. in Givnish et al. (2014b), (131-)121(-117) or (112-)105(98) m.y. in Hertweck et al. (2015), and 105-43 and 104-67 m.y. in Mennes et al. (2013, 2015 respectively).
See also Mennes et al. (2015) for ages in the order - note topology.
Evolution. Bacterial/Fungal Associations. Mycorrhizal asssociations in Liliales are commonly of the Paris-type where the hyphae are intercellular and form coiled structures between the cells (see F. A. Smith & Smith 1997).
Genes & Genomes. Very large genomes with a C value of 35 picograms or more are found in some Melanthiaceae, Liliaceae and Alstroemeriaceae (Leitch et al. 2005).
Chemistry, Morphology, etc. Inflorescence morphology in Liliales needs attention. Liliaceae and Alstroemeriaceae, at least, have distinctive radially-elongated endothecial cells (Manning & Goldblatt 1990). Glucomannan seed reserves are reported from some species of Liliaceae-Lilioideae and Colchicaceae-Colchiceae (Jakimow-Barras 1973). For chromosome size, see Vijayavalli and Mathew (1990 - as Liliaceae) and Tamura (1995).
There is much information in Rudall et al. (2000), including a summary of pollen variation; see Conran et al. (2009b) for information on leaf and stomata, Schlittler (1953a) for inflorescences, Endress (1995b) for some floral development, El-Hamidi (1952) for gynoecium, and Fukuhara and Shinwari (1994) for seed coat anatomy; for pollen of Japanese representatives, see Handa et al. (2001), for details of ovule morphology, etc., see Oganezova (2000b).
Phylogeny. The topology of relationships within Liliales has been for some time uncertain. Liliaceae, Smilacaceae, Rhipogonaceae and Philesiaceae always form a clade, but relationships in it are unclear, either [[Smilacaceae [Rhipogonaceae + Philesiaceae]] Liliaceae] (J. S. Kim et al. 2013; Givnish et al. 2014b) or [[[Rhipogonaceae + Philesiaceae] [Smilaceae + Liliaceae]] (Givnish et al. 2006; Chase et al. 2006; Fay et al. 2006c); support varies. J. S. Kim et al. (2012, esp. 2013) found a weakly-supported [Melanthiaceae + Petermanniaceae] clade forming a trichotomy with Colchicaceae et al. and Liliaceae et al., and although the position of Campynemataceae as sister to the rest of the order had no bootstrap support, it has commonly been found (e.g. Givnish et al. 2006; Chase et al. 2006). Although Corsiaceae were included in none of these studies, Campynemataceae and Corsiaceae were found to be basal in the order in Fay et al. (2006c). Petermanniaceae are variously associated with Colchicaceae, Melanthiaceae and Alstroemeriaceae (see also J. Davis in Vinnersten & Reeves 2003; Graham et al. 2005). Although early work (Rudall et al. 2000) suggested that Petermannia should be included in Colchicaceae, the sample had been misidentified (see Chase et al. 2006). Indeed, Colchicaceae and Alstroemeriaceae (and Luzuriagaceae, here included in the latter family) are commonly linked (Vinnersten & Bremer 2001; Tamura et al. 2004a; Davis et al. 2004; Janssen & Bremer 2004; Givnish et al. 2014b). See also Chase et al. (1995a), Patterson and Givnish (2002), and Chen et al. (2007: Bayesian analysis, support for many branches weak).
Neyland (2002a), analysing variation in 26S ribosomal DNA, thought that Corsiaceae were sister to other Liliales. However, Neyland, in Rudall and Eastman (2002), suggested that Corsia was sister to Campynema, and similar relationships were recovered by Hertweck et al. (2015: [Campynema + Arachnitis], the latter with an extremely long branch]. Although this position in Neyland (2002a) had only weak support, it is largely consistent with morphological evidence. Davis et al. (2004), Fay et al. (2006c) and Petersen et al. (2012) also found Corsiaceae to be associated with Liliales. Analysis of 26S rDNA sequences suggested that Corsiaceae were polyphyletic; Arachnitis perhaps being sister to Thismia and/or Burmannia (Burmanniaceae-Dioscoreales: Neyland & Hennigan 2003; G. Petersen et al. 2006b: combined analysis).
In the whole chloroplast genome analyses of Givnish et al. (2014b: Campynemataceae and Corsiaceae still outstanding) the family relationships below all have strong support. Mennes et al. (2015) found good support both for a monophyletic Corsiaceae and for a clade [Campynemataceae + Corsiaceae], which may be sister to other Liliales, although this position was not always recovered and relationships within other Liliales were somewhat different from those suggested by Givnish et al. (2014b); analysis of plastid genomes found Arachnitis to be on a very long branch indeed (Mennes et al. 2015).
Classification. Combining Smilacaceae and Rhipogonaceae was an option in A.P.G. II (2003), but relationships in this area are uncertain (see above).
Previous Relationships. Cronquist (1981) circumscribed Liliales very broadly, and his order now makes up the bulk of Liliales and Asparagales and other things besides.
Includes Alstroemeriaceae, Campynemataceae, Colchicaceae, Corsiaceae, Liliaceae, Melanthiaceae, Petermanniaceae, Philesiaceae, Rhipogonaceae, Smilacaceae.
Synonymy: Campynematinae Reveal, Smilacineae Reveal - Alstroemeriales Hutchinson, Campynematales Doweld, Colchicales Dumortier, Liriales K. Koch, Melanthiales Link, Paridales Link, Smilacales Link, Trilliales Takhtajan, Veratrales Dumortier
[Corsiaceae + Campynemataceae]: ovary inferior, styluli +.
Age. the age of this clade is around (93-)70(-47) m.y.o. (Mennes et al. 2015).
CORSIACEAE Beccari, nom. cons. Back to Liliales
Plant echlorophyllous, myco-heterotrophic, associated with glomeromycote fungi; rhizomatous or almost cormose; chemistry?; vessels?; root endodermis not obvious; epicuticular wax platelets parallel, stomata ?type; leaves spiral to two-ranked, venation parallel, sheath closed; (plant ?dioecious); flowers single, terminal; monosymmetric; T large, median T of outer whorl adaxial, standard-like [= "labellum"]; ?nectary [= callus on labellum in Corsia?]; (A basally adnate to style [gynostemium] - Corsia); (A 5 + staminode opposite "labellum" - C. dispar); (pollen porate - Corsia); (placentation parietal), style (short/none), (± unbranched); ovules many/carpel, integuments two cells across, parietal tissue 1 cell across, nucellar cap?, funicle long; fruit dehiscing laterally with three valves, from base and separating from placentae or apex; seeds minute, testal; (endosperm also with starch), embryo undifferentiated; n = 9; seedling?
3[list]/30. S. China, S. South America, Papuasia-Australia (map: from van Royen 1972; Ibisch et al. 1996). [Photo - Flower]
Age. Crown-group Corsiaceae are (76-)53(-30) m.y.o. (Mennes et al. 2015).
Evolution. Divergence & Distribution. The age of Corsiaceae is compatible with a Gondwana break-up explaining the current distribution of the family, but other explanations are possible, too (Mennes et al. 2015).
Ecology & Physiology. For the glomeromycote fungi, all notably similar, associated with Arachnitis, see Bidartondo et al. (2002).
Pollination Biology. The flowers of most species of Corsia are presented inverted and the labellum is erect or hangs down, the stamens, etc., being underneath it, however, in C. dispar the extreme curvature of the ovary just beneath the flower results in the labellum being abaxial (Jones & Gray 2008). The megaspore mother cell seems to have two cell layers above it; is this a nucellar cap? (Rübsamen 1986).
Bacterial/Fungal Associations. Glomus is involved in the myco-heterotrophic association, and is related to species involved in similar associations in other vascular plants (Winther & Friedman 2008).
Chemistry, Morphology, etc. For information, see Rübsamen (1986: general), Neinhuis and Ibisch (1998: general), and Rudall and Eastman (2002: morphology).
CAMPYNEMATACEAE Dumortier Back to Liliales
Rhizome short, vertical, or 0; vessels 0; fibrous leaf bases persistent; chemistry?; stomata type?; leaf base sheathing [?type]; inflorescence morphology?, axis bracteate; flowers medium-sized, T green, not spotted; A adnate to base of T, tapetum 2- or multinucleate; (pollen inaperturate - Campynemanthe); style branches erect; ovules 3-many/carpel, crassinucellate; fruit a capsule or indehiscent, T enlarging, persistent; seeds angled, exotestal and endotegmic, with phlobaphene. or flattened; embryo minute; n = 11, chromosomes to 3µm long; seedling?
2[list]/4. New Caledonia and Tasmania (map: from van Balgooy 1984).
Age. The age of crown-group Campynemataceae has been estimated at ca 73 m.y. (Janssen & Bremer 2004), ca 36.5 m.y. (Chacón et al. 2012b) or 70-16 m.y. (Mennes et al. 2015).
Chemistry, Morphology, etc. Campynemanthe has a subumbellate inflorescence, introrse anthers (see illustration in Kubitzki 1998b) partly superior ovary, and dentate leaf apex; Campynema has extrorse anthers, multinuclear tapetal cells and an inferior ovary.
Additional information is taken from Kubitzki (1998b: general), Dahlgren and Lu (1985: Campynemanthe) and Lowry et al. (1987: cytology and embryology).
[Campynemataceae [[Petermanniaceae [Colchicaceae + Alstroemeriaceae]], Melanthiaceae, [[Philesiaceae + Rhipogonaceae] [Smilacaceae + Liliaceae]]]]: ? Does this clade exist?
Age. The age of this node is estimated to be around 97.4 m.y. by Magallón et al. (2015).
[[Petermanniaceae [Colchicaceae + Alstroemeriaceae]] [Melanthiaceae [Liliaceae [Smilacaceae [Philesiaceae + Rhipogonaceae]]]]]: root hypodermal cells dimorphic or not; rhizome +, ± woody; leaf blade venation reticulate, base not sheathing.
Age. The age for this node is estimated at (123-)114, 86(-72) m.y. (Bell et al. 2010), (92.5-)82(-71.5) m.y. (Vinnersten & Bremer 2001: Petermannia in Colchicaceae!), (112-)96, 87(-81) m.y. (Wikström et al. 2001), ca 125.5 and 114.4 m.y. (Magallón & Castillo 2009), ca 79.5 or 54.8 m.y. (S. Chen et al. 2013), or ca 87.9 m.y.a. (Magallón et al. 2015: note topology) - in the last four studies, Petermanniaceae were not included).
Chemistry, Morphology, etc. Gatin (1920) looked at pedicel anatomy at taxa scattered through this clade; it was generally quite complex, although not in Smilax.
[Petermanniaceae [Colchicaceae + Alstroemeriaceae]]: primary root of seedling well developed.
PETERMANNIACEAE Hutchinson, nom. cons. Back to Liliales
Plant climbing, with leaf-opposed tendrils; saponins 0; velamen +; vessels also in stem and leaf; stem with prickles; leaves spiral, petiole short, blade with midrib and 5-7 main veins; inflorescence cymose; pedicels not articulated; T 1-veined, medium-sized; tapetum amoeboid; (pollen inapertuarte); ovary inferior, placentation parietal, stigma wet; ovules many/carpel, outer integument 3-4 cells across, parietal tissue 2-3 cells across, nucellar cap ?2-layered; fruit a berry; exo- and endotesta thickened, mesotesta "several-layered", a cuticle, tegmen crushed; n = 5; first leaves cataphylls.
1/1: Petermannia cirrosa. Central part of the E. coast of Australia, rare (Map: from Fl. Austral. 46. 1986).
Age. Fossil Petermanniopsis is reported from the early Eocene of Australia (Conran & Christophel 1999); the fossil has paracytic stomata - probably plesiomorphic. .
Evolution. Divergence & Distribution. Diversification rates in the Petermanniaceae clade have slowed down (Hertweck et al. 2015).
Chemistry, Morphology, etc. The inflorescences and tendrils are terminal, but they become leaf-opposed when they are evicted by the strong growth of an axillary shoot.
Additional information is taken from Conran and Clifford (1998: general) and Prychid and Rudall (1999: crystals), Tomlinson and Ayensu (1969: anatomy), and Björnstad (1970) and Conran (1988), both embryology.
[Colchicaceae + Alstroemeriaceae]: ?
Age. The age of this node is around (71.3-)59, 58(-51.2) m.y. (Wikström et al. 2001), (71.3-)59, 58(-51.2) m.y. (Vinnersten & Bremer 2001), ca 76 m.y.a. (Janssen & Bremer 2004), (83-)62, 59(-40) m.y. (Bell et al. 2010), (116.7-)96.5, 93.4(-73.4) m.y. (Chacón et al. 2012b) or ca 59.1 m.y. (Magallón et al. 2015).
Evolution. Genes & Genomes. The GC content of the genome shows a notable increase in this clade (Smarda et al. 2014).
Chemistry, Morphology, etc. For fructose oligosaccharide accumulation (only one record for Alstroemeriaceae s.l.), see Pollard (1982).
COLCHICACEAE de Candolle, nom. cons. Back to Liliales
Flavones +, steroidal saponins 0; raphides 0; cuticular wax with parallel platelets; leaves conduplicate, blade with midrib (0), base sheathing; inflorescence various, flowers axillary; T towards base U-shaped and folded around each stamen in bud, connate or not, (A latrorse, introrse), sexine thick, (pollen operculate); (G [2, 4]), styluli +, or style ± branched, or stigma with recurved lobes, wet or dry; ovules 2-many/carpel, ± ascending, orientation various, (unitegmic), micropyle bistomal; antipodal cells multinucleate; capsule septicidal; seeds rounded, strophiole, sarcotesta or aril +; exotesta with thick walls (less so - Colchicum), phlobaphene +; endosperm (with starch), embryo small; chromosomes 1-16 µm long; cotyledon photosynthetic or not, bifacial (ligulate).
15[list]/245 - six tribes below. Temperate to tropical, but not in South America (map: see Meusel et al. 1965; Fl. Austral. 46. 1986; Hong 1993; Nordal et al. 2001; del Hoyo & Pedrola-Monfort 2006, 2008).
Age. Crown-group Colchicaceae are estimated to be ca 64 m.y.o. (Chacón et al. 2012b) or as little as (41.1-)34, 33(-24.9) m.y. (Vinnersten & Bremer 2001) or ca 44 m.y.o. (Janssen & Bremer 2004).
1. Uvularioideae A. Gray
Rhizomes +; leaves 2-ranked, (petiole +); inflorescence umbellate or flowers single, axillary; flowers campanulate, pendulous; pollen disulcate; nucellar cap massive; fruit septicidal, or a berry; endotesta enlarged; n = 7, 8, chromosomes 5-16 µm long.
2/15: Disporum (10). W. and E. North America, East Asia to W. Malesia.
Age. Crown-group Uvularioideae have been dated to (33.7-)26, 20(-15.1) m.y. (Vinnersten & Bremer 2001) or ca 28 m.y. (Chacón et al. 2012b: note topology).
Synonymy: Uvulariaceae Kunth, nom. cons.
2. Burchardioideae [?published]
Flowers with spreading or funnel-shaped tepals.
Age. If this subfamily exists, it has been dated to around (37.1-)29(-20.9) m.y. by Vinnersten and Bremer (2001).
2A. Burchardieae J. C. Manning & Vinnersten
Corm with papery scales; leaves spiral; inflorescence umbellate, axis with leaves; capsule septicidal; seeds ± angular; n = 24.
Synonymy: Burchardiaceae Takhtajan
2B. Tripladenieae Vinnersten & J. C. Manning
Rhizomes +; (stem lignescent); leaves 2-ranked, (petiole +); inflorescence umbellate, or flowers single; (nectaries paired, stalked); n = 7, 18.
3/5. Australia and New Guinea.
3. Colchicoideae Burmeister
Tunicated corm +; alkaloids with a 7-C tropolone ring +; (vessels in stem); leaves spiral; inflorescence racemose, or flowers single; nectary on filament bases; (antipodal cells persistent).
9/210. Old World.
Age. This node is ca 40.1 m.y.o. (Chacón et al. 2012b).
3A. Colchiceae Reichenbach
(Plants climbers), by (leaf tendrils - Gloriosa), (rhizomatous); (vessels in stem - Sandersonia), (leaves whorled), (petiole short, base not sheathing); (flowers monosymmetric by style position - Gloriosa); (T connate); nectaries median on tepal or on stamen base (0); (pollen polyporate); antipodal cells divide; (capsule septicidal); n = 7, 9-12, etc., chromosomes 2.8-14.3 µm long.
5/170: Colchicum (150). Africa, Europe, Central to tropical South East Asia.
Age. The age of this node is (20.6-)16, 15(-9.1) m.y. (Vinnersten & Bremer 2001).
Synonymy: Bulbocodiaceae R. A. Salisbury, Merenderaceae Mirbel
[Iphigenieae + Anguillarieae]: ?
Age. This node has been dated to ca 29 m.y. (Chacón et al. 2012b).
3B. Iphigenieae Hutchinson
Flowers single; nectaries 0; n = 11.
2/10: Iphigenia (9). Old World Tropics, South Africa.
3C. Anguillarieae D. Don
Inflorescence racemose or spicate, bracts 0; (tepals connate); capsule septicidal; n = 7, 10, 11.
2/38: Wurmbea (37). Africa, Australia.
Evolution. Divergence & Distribution. Colchicum may have diverged from other Colchiceae 13.4±1.5 m.y.a., probably in southwestern Africa (del Hoyo et al. 2009). For chromosome evolutiom in the family, see Chacón et al. (2014).
Ecology & Physiology. Colchicaceae are well represented in the taxa that have water-catching leaves with very distinctive morphologies that are particularly prominent in the foggy deserts of Namaqualand, South Africa (Vogel & Müller-Doblies 2011).
Seed Dispersal. Myrmecochory predominates in the family (Lengyel et al. 2009, 2010).
Chemistry, Morphology, etc. The tropolone alkaloids, with their remarkable seven-carbon rings, have given plant chemists headaches for a century or more. The protoalkaloid colchicine has been reported from some Melanthiaceae, probably also Liliaceae, as well as one or two other monocots not immediately related to Liliales (Tofieldiaceae, Hyacinthaceae [= Asparagaceae-Scilloideae]: Gibbs 1954), although a recent survey suggests that it is restricted to Colchicaceae (Vinnersten & Larsson 2010: sampling good).
Androcymbium [= Colchicum] longipes has tepals ca 4.5 cm long, each with a basal claw ca 3.5 cm long representing the part of the tepal adnate to the filament. There is considerable variation in nectary morphology and position within the family, but details of nectary evolution are unclear. Cave (1968) described Androcymbium as having a nucellar cap, although from the illustration if looks as if there is parietal tissue 2-3 cells across, similarly, illustrations in Vesque (1878) suggest that parietal tissue in Uvularia is ca 4 cells across.
Additional information is taken from Nordenstam (1998; general); for embryology, see Ono (1929), Cave (1968 and references), for Disporum, see Shinwari et al. (1994a, b), for Uvularia, etc., see Hayashi et al. (1998), for the floral morphology of Kunthera, see Endress (1995b), and for bulbs, etc., see Buxbaum (1936) and Tillich (1998).
Phylogeny. Molecular studies suggest considerable phylogenetic structure within the family. It initially appeared that "Uvularieae" might be paraphyletic and basal. [Uvularia + Disporum] (N. Temperate) and [Schelhammera + Tripladenia] (Australian) were successively the first two branches of Colchicaceae, and Drymophila was also around here (e.g. Rudall et al. 2000; Fuse & Tamura 2000; Vinnersten & Reeves 2003). These genera, and some others, have rhizomes, flavonols, and their nucellar epidermal cells are enlarged. Although Colchicaceae are noted for their alkaloids, such secondary metabolites are absent from these basal clades (e.g. Kite et al. 2000). There was uncertainty over the relative positions of Uvularia and Burchardia (Fay et al. 2006c for a summary); Vinnersten and Manning (2007) thought that Burchardia, sister to the rest of the family, might be paraphyletic. J. S. Kim et al. (2013) placed Uvularieae basal while the three species of Burchardia they examined were in the next clade up. This latter result was confirmed in a more detailed study by Nguyen et al. (2013), however, Chacón et al. (2014) found Wurmbea to be sister to the rest of the family; although they sampled all species, this position had little support.
Relationships in the rest of the family found by J. S. Kim et al. (2013) are consistent with those in the phylogeny above. Androcymbium, Colchicum, Merendera and Bulbocodium form a well supported clade with (currently) little internal resolution, but the whole clade may be characterisable (Vinnersten & Reeves 2003; del Hoyo & Pedrola-Monfort 2006). For Colchicum, see Persson (2007); Androcymbium was not included (see also del Hoyo & Pedrola-Monfort 2008; del Hoyo et al. 2009; Persson et al. 2011).
Classification. The tribal classification above is that of Vinnersten and Manning (2007); I follow Nguyen et al. (2013) for subfamilies.
Generic limits in general need much attention (Fay et al. 2006c; Vinnersten & Manning 2007). See Manning et al. (2007) for the combination of Colchicum and Androcymbium; the recognition of Colchicum may make Androcymbium paraphyletic (see del Hoyo et al. 2009; Persson et al. 2011). The sections of Androcymbium are often not monophyletic (del Hoyo & Pedrola-Monfort 2008)
Previous Relationships. Drymophila was included in Luzuriagaceae by e.g. Tahktajan (1997) and placed far distant from Colchicaceae, whilst Uvularia and Disporum used to be part of Convallariaceae (= Ruscaceae s. str., = Asparagaceae-Nolinoideae) and indeed are superficially like genera of that family such as Polygonatum.
ALSTROEMERIACEAE Dumortier, nom. cons. Back to Liliales
Leaves resupinate; inflorescence ± cymose; (placentation parietal); testa and tegmen thin-walled; endosperm walls thick, pitted; karyotype bimodal.
5/170. Central and South America, the Antipodes.
Age. Crown group Alstroemeriaceae may be (62.6-)55, 48(-37.5) m.y.o. (Vinnersten & Bremer 2001), (86.8-)64.2, 57.5(-37.8) m.y.o. (Chacón et al. 2012b) or ca 76 m.y.o. (Janssen & Bremer 2004).
1. Alstroemerieae Bernhardi
(Climber - Bomarea), swollen storage roots +; flavonols, tuliposides + [α-methylene-γ-butyrolactone - glucose esters]; (velamen +); cuticular wax with parallel platelets; leaves spiral; inflorescence subumbellatee (flowers axillary), bracteoles lateral; flowers monosymmetric, T spotted, median member of the outer whorl adaxial, inner whorl often with nectariferous claw; A latrorse, basi/centrifixed; ovary inferior, stigma wet; ovules many/carpel, nucellar cap 0, micropyle?; fruit capsular [?type] or indehiscent; testa also ± thick-walled, (sarcotesta + - Bomarea), tegmen collapses; embryo short to medium; n = 8, 9, chromosomes 6-19 µm long; cotyledon not photosynthetic (photosynthetic - annual Alstroemeria graminea]).
3[list]/165: Bomarea (100), Alstroemeria (65). Tropical and temperate Central and South America (map: from Aker & Healy 1990; Hofreiter 2006 - the cultivated Bomarea edulis is particularly widely distributed). [Photo - Flower, Fruit.]
Age. Crown group Alstroemerieae may be (27.1-)18, 17(-10.5) m.y.o. (Vinnersten & Bremer 2001), (47.8-)31.9, 29.0(-18.2) m.y. old (Chacón et al. 2012b), or ca 30 m.y.o. (Janssen & Bremer 2004).
2. Luzuriageae Bentham & Hooker
Plant shrubby, ± climbing, stems perennial, usu. branched; chelidonic acid, fructans?; leaves two-ranked, petiole +/0, blade conduplicate or supervolute, sheath +, open; (inflorescence a cincinnus); pedicels articulated; (T rather small); (A introrse); tapetum amoeboid; style deeply branched [Drymophila], stigma dry; ovules few to many/carpel, ?morphology; fruit a berry; seeds rounded, coat with thin walls, (exotesta shed); endosperm development?; n = 10; cotyledon ?not photosynthetic, ?primary root.
2[list]/5. Peru to Tierra del Fuego, Falkland Islands, New Zealand and southeast Australia, inc. Tasmania. (Map: from Fl. Austral. 46. 1986). [Photos - Collection, Luzuriaga polyphylla, Luzuriaga radicans, Luzuriaga Flower.]
Age. Crown group Luzuriageae are dated to (40.5-)32, 23(-17.3) m.y. (Vinnersten & Bremer 2001), ca 56 m.y. (Janssen & Bremer 2004), and (55.5-)35.9(-19.5) m.y. or ca 23 m.y. (Chacón et al. 2012b).
Synonymy: Luzuriagaceae Lotsy
Evolution. Divergence & Distribution. See Hofreiter (2007) and especially Chacón et al. (2012b) for the biogeography and ecology of the whole clade.
Genes & Genomes. Chacón et al. (2012a) found that there was extensive variability in the rDNA sites on the chromosomes, perhaps suggesting extensive genome rearrangements despite invariance in chromosome number.
Chemistry, Morphology, etc. Some information on Alstroemerieae is taken from E. Bayer (1998: general), Sanso and Hunziker (1998: cytology), and Sarwar et al. (2010: pollen). Information on Luzuriageae is taken from Conran and Clifford (1985 [e.g. stigma], 1998).
Phylogeny. See Rudall et al. (2000a), Sanso and Xifreda (2001) and Aagesen and Sanso (2003).
Classification. For generic limits in Alstroemerieae, see Sanso and Xifreda (2001).
[Melanthiaceae [Liliaceae [Smilacaceae [Philesiaceae + Rhipogonaceae]]]]: ?
Age.The age of this clade may be (72.8-)67, 63(-53.6) m.y.o (Vinnersten & Bremer 2001), (108-)96, 83(-68) m.y.o. (Bell et al. 2010) or 105-43 m.y.o. (Mennes et al. 2013).
MELANTHIACEAE Borkhausen, nom. cons. Back to Liliales
Leaves often evergreen; flavones, flavonols or flavonoids +; cuticle wax with parallel platelets; (leaf margins toothed), base sheathing; inflorescence (branched) racemose; (T 3, 4); A (latrorse; adnate to base of T); G (1) , placentation axile to parietal, style branched to the base, stigma dry (wet); ovules many/carpel, position variable, parietal tissue ca 1 cell across; T persistent in fruit, ± green; seed coat?, (phlobaphene +); endosperm helobial, embryo short (long); chromosomes 1-6 µm long; cotyledon bifacial or not, hypocotyl at most short; x = 9, genome size [1Cx] 1-5.5 pg.
16[list]/170 - five groups below. N. temperate, esp. East Asia and E. North America, to Peru (map: see Meusel et al. 1965; Frame 1990; Fl. N. Am. 26: 2002; Seberg 2007). [Photos - Collection 1.]
Age. The age for crown Melianthaceae is estimated be (61.8-)54, 42(-34.2) m.y. (Vinnersten & Bremer 2001: note topology) or ca 97 m.y. (Janssen & Bremer 2004).
1. Melanthieae Grisebach
± Bulbous; highly oxygenated esterified C-nor-D homosteroidal alkaloids; (monocot secondary thickening +); styloids also +; (leaves curved-plicate, sheath closed [Veratrum]); anthers kidney bean-shaped, opening by valves, thecae confluent; (antipodal cells persistent); capsule septicidal [ventricidal]; (seeds flat, winged); n = 8 (10), many polyploid.
7/100: Veratrum (50), Schoenocaulon (25). North Temperate, Schoenocaulon to Peru.
Synonymy: Veratraceae Salisbury
[[Helionadeae + Chionographideae] [Xerophylleae + Parideae]]: ?
Age. The age of this node may be some (76-)70, 66(-60) m.y. (Wikström et al. 2001), or (85-)67, 59(-43) m.y. (Bell et al. 2010).
[Helionadeae + Chionographideae]: calcium oxalate crystals cuboidal; bracts 0; anther thecae ± confluent; pollen intectate.
2. Helionadeae Fries
Raphides 0; pollen spinulate; (style +, long); seeds linear, long-caudate at both ends; n = 17.
1/9. E. North America, East Asia.
Synonymy: Heloniadaceae J. Agardh
3. Chionographideae Nakai
Flowers often imperfect; T with 1 nerve; nectaries 0; pollen 4-porate, with clavate processes; capsule septicidal; seeds winged (at one end); n = 6?, 12 (21, 22).
2/6. E. North America, East Asia.
Synonymy: Chionographidaceae Takhtajan
[Xerophylleae + Parideae]: anther thecae distinct.
Age. Bell et al. (2010) estimated the age of this node at some (67-)49, 43(-27) m.y., Wikström et al. (2001) suggested an age of (59-)54, 50(-45) m.y..
4. Xerophylleae S. Watson
Plant ± bulbous; pericycle 2-3 cells thick; styloids also +; leaf long-linear, xeromorphic; T nectaries 0; ovules 2-4/carpel; n = 15, chromosomes ca 2.65 µm long.
1/2. North America.
Synonymy: Xerophyllaceae Takhtajan
5. Parideae Bartling
Rhizome monopodial; flavonols +; raphides 0, cuboidal crystals +; stomata tetracytic; leaves whorled, with (petiole), midrib, and broad blade, venation reticulate; flowers single, terminal, (to 12-merous); P = K + C, K (0) 3-10, C (0) 3-6(-8); A 6-24, introrse to extrorse; G [3(-10)], (septal nectaries +), placentation axile to parietal, (style unbranched), stigma dry; ovules many/carpel, position variable, parietal tissue 1-2 cells across, nucellar cap 2-4 cells across, suprachalazal zone short; embryo sac bisporic [chalazal dyad], eight-celled [Allium-type]; fruit a berry or (septicidal and) loculicidal capsule, A also persistent in fruit; seeds rounded, (aril or sarcotesta +); endosperm also helobial [Trillium], starchy, embryo minute, undifferentiated; n = 5, chromosomes heteromorphic, 6-40+µm long, genome size [1Cx] 31.2-56.6 pg; cotyledon unifacial (with petiole and blade - Paris).
3-5/ca. 80: Trillium (50, or 70 when circumscribed broadly). North Temperate (for map, see Farmer 2006). [Photos: collection.]
Age. The age for this node is estimated at (23.3-)16, 9(-3.9) m.y. (Vinnersten & Bremer 2001: note topology).
Synonymy: Paridaceae Dumortier, Trilliaceae Chevallier, nom. cons.
Evolution. Divergence & Distribution. Paridae are a young clade, but show a notable amount of both floral and vegetative divergence from other members of the family. There has been a massive increase in genome size thoughout the clade (Pellicer et al. 2013), the lowest genome size known in the clade being from Pseudotrillium rivale.
Bacterial/Fungal Associations. Melanthieae are susceptible to infection by rust fungi (Holm 1982).
Genes & Genomes. The range of chromosome sizes in this family is at least 10-fold and that of C-values, over 200-fold (Pellicer et al. 2010a, 2013, 2014); Trillium hagae has a genome size of 2C = 264.9 pg (Zonneveld 2010).
Chemistry, Morphology, etc. There is no fructose oligosaccharide accumulation in Trillium, at least. Narita and Takahashi (2008, see also Takahashi 1994) discuss shoot and floral development in Parideae, noting that in apetalous Trillium, but not in apetalous Paris, the carpels are opposite the sepals; they think the petals are derived from stamens, although no other Liliales have the three whorls of stamens that this hypothesis would entail (see also Ronse de Craene 2010). There are raphides in the ovule, but nowhere else. Although the embryo of Trillium is minute when the seed is dispersed, it grows to about the length of the seed before germination.
The alkaloids of Veratrum and its relatives are very complex and distinctive (Kite et al. 2000). Xerophyllum is particularly distinctive in its vegetative anatomy (Ambrose 1975). Except for Helionadeae, syncarpy in Melanthiaceae tends to be rather weak. In a number of taxa, including Veratrum and Paris, the tepals become greener and persist in fruit (e.g. Weberling 1989); other taxa, including Trillium, have persistent sepals.
General information is taken from Ambrose (1975, 1980), Tamura (1998: Melanthiaceae, Trilliaceae), Zomlefer (1996: Trilliaceae, 1997a [nice table], especially 2001: Melanthiaceae) and Zomlefer et al. (2006); see also Arber (1925). For secondary thickening, see Cheadle (1937), for floral morphology, see Endress (1995b); for embryological information, see Ono (1929), Berg (1962) and Cave (1968) and references; for chromosome numbers in Melanthieae, see Zomlefer et al. (2014), and for genome size and chromosome number and their ancestral reconstructions, see Pellicer et al. (2013).
Phylogeny. Possible relationships are [Veratrum [Trillium and relatives + the rest] (Tamura et al. 2004a; see also Fuse & Tamura 2000), however, Xerophyllum was not included and support for the basal dichotomy was weak. Consistent with this earlier work, the topology [Melanthieae [[Heloniadeae + Chionographideae] [ Xerophylleae + Parideae]]] has been recovered (Zomlefer et al. 2006; J. S. Kim et al. 2013). Farmer (2006) discussed the relationships of the Trillium group (as Trilliaceae), in Parideae; the backbone of the phylogeny in Parideae remains distinctly poorly supported (see also Kazempour Osaloo & Kawano 1999 for a phylogeny).
Classification. In the past this has been recognised as one or two separate families, Trilliaceae, and sometimes also Paridaceae; generic limits are uncertain.
Botanical Trivia. The genome of Paris japonica, at over 150 picograms, is the largest known of any organism (Pellicer et al. 2010a).
Previous relationships. Veratrum in particular looks superficially like Maianthemum (inc. Smilacina), a member of Ruscaceae s. str., Asparagaceae s.l.; these and most other Melanthiaceae were all included in Cronquist's (1981) Liliaceae.
[Liliaceae [Smilacaceae [Philesiaceae + Rhipogonaceae]]]: leaf base not sheathing.
Age. The age of this node may be about 58 m.y. (Givnish et al. 2014b), or, with the topology [[Philesiaceae + Rhipogonaceae] [Smilacaceae + Liliaceae]], some (60.9-)54, 52(-42.3) m.y.o. (Vinnersten & Bremer 2001), ca 55.6 m.y.a. (Magallón et al. 2015: again, note topology), ca 91 m.y.o. (Janssen & Bremer 2004) or ca 64.7 m.y.o. (Chacón et al. 2012b).
Evolution. Divergence & Distribution. See Patterson and Givnish (2002) for characters of this group.
LILIACEAE Jussieu, nom. cons. Back to Liliales
Flavonols +, chelidonic acid 0; raphides 0; bracteole lateral; T often spotted; A (latrose), anthers often centrifixed; (pollen operculate); (placentation parietal), stigma dry (wet); ovules 2-many/carpel, ± pendulous, (outer integument 3-6 cells across), nucellar cap (0-)1-3 cells across, (podium short), (funicular obturator +); antipodal cells not multinucleate; testal cells all ± thickened, some with brown contents; (embryo short); cotyledon ± photosynthetic, bifacial, hypocotyl 0; x = 8; genome size [1Cx] ca 6.7 pg.
19[list]/610: five groups below. North Temperate, especially East Asia and North America (map: see Meusel et al. 1965; Fl. N. Am. 26: 2002).
Age. The crown-group age for Liliaceae is estimated at (57-)53, 48(-44) m.y. (Wikström et al. 2001) or (78-)53, 52(-40) m.y. (Bell et al. 2010).
1. Lilioideae Eaton
Embryo sac tetrasporic, three chalazal megaspores fuse, divide twice [Fritillaria-type]; (elaiosomes +); exotesta palisade or lignified [level?]; chromosomes long [see below].
11/595. (Cold) temperate, esp. North America, East Asia.
Age. The age for this node is estimated at (33-)30, 27(-24) m.y. (Wikström et al. 2001), (36.9-)30, 29(-22.5) m.y. (Vinnersten & Bremer 2001: note topology), or (45-)31, 28(-18) m.y. (Bell et al. 2010).
1a. Medeoleae Bentham
Clintonia type VAM; (leaves whorled), (with parallel venation); suprachalazal nucellus prominent; seeds rounded, elaiosome 0; exotesta palisade, outer wall thickened; embryo minute; n = 7, 14, 16, chromosomes heteromorphic 7.7-20.1 µm long, ?1C value.
2/6. North America, East Asia. [Photos - Collection.]
Age. The age for crown Medeoleae is estimated to be (29.8-)21, 16(10.7) m.y. (Vinnersten & Bremer 2001: note topology).
Synonymy: Medeolaceae Takhtajan
1b. Lilieae Ritgen
Plant bulbous, with contractile roots; tuliposides + [α-methylene-γ-butyrolactone - glucose esters], γ-methyleneglutamic acid, di- and triferulic acid sucrose esters +; leaves with parallel venation, reticulum not developed, (base sheathing - some Tulipa); flowers often large; style 0 or long, stigma crested/shortly lobed; nucellar cap?; capsule loculicidal; seeds often flattened; exotesta palisade or lignified?, tegmen also persisting; endosperm pentaploid, thick-walled, not pitted [Erythronium]; n = (9, 11-)12(-13), chromosomes (hetermorphic), (1.8 [Gagea]-)5-27 µm long, genome size [1C] 6.6-100+ pg; (cotyledon unifacial; not photosynthetic - Lilium canadense [Arber 1925]).
9/595: Fritillaria (130), Lilium (120), Gagea ([70-]90[-275]), Tulipa (90). (Cold) temperate, esp. North America, East Asia. [Photos - Collection, Nectaries.]
Age. The age for this node is estimated at (34.5-)28, 24(-17.2) m.y. (Vinnersten & Bremer 2001: note topology).
Synonymy: Erythroniaceae Martynov, Fritillariaceae R. A. Salisbury, Liriaceae Borkhausen, Tulipaceae Borkhausen
[Calochortoideae + Streptopoideae]: (flowers 3-merous); ovules with nucellar cap; placental epidermis papillate; chromosomes short [see below].
Age. The age for this node is around (49-)44, 37(-32) m.y. (Wikström et al. 2001) or (65-)46, 42(-27) m.y. (Bell et al. 2010).
2. Calochortoideae Dumortier
(Bulbs - Calochortus); (γ-methyleneglutamic acid +); (vessels in stem); (leaves sheathing), (with parallel venation, reticulum not developed); (bracetoles 2, lateral - Tricyrtis); (outer T ± calycine), tepals usu. ± bearded; nectaries ± saccate; (placentation parietal); capsule septicidal, seeds ± flattened; seed coat thin walled; n = 7-10, (11), 12, chromosomes 1.1-5.5 µm long.
2/85: Calochortus (65), Tricyrtis (20). Temperate East Asia and E. North America (map: from Fl. N. Am. 26: 2002). [Photo - Flower.]
Synonymy: Calochortaceae Dumortier, Compsoaceae Horaninow, nom. illeg., Tricyrtidaceae Takhtajan, nom. cons.
3. Streptopoideae Reveal
Leaf base sheathing or not?; (P whorls very different - Scoliopus); (A 3 - Scoliopus); nucellar podium well developed, very long, thin; embryo sac bisporic [chalazal dyad], eight-celled [Allium-type] - Streptopus; seeds ± rounded, striate, with phlobaphene; endotesta cells thickened on anticlinal and inner periclinal walls; n = 8 (9), chromosomes 1.1-5.6(-13.2 - Scoliopus) µm long.
3/15. N. (cool) temperate, esp. East Asia and E. and W. North America (map: from Fl. N. Am. 26: 2002).
Synonymy: Scoliopaceae Takhtajan
Evolution. Divergence & Distribution. Patterson and Givnish (2002) emphasized the similarities among the large-flowered heliophilous Liliaceae, with their bulbs, capsules, and linear leaves with parallel venation, and those among the broad-leaved, reticulate-veined, smaller-flowered, rhizomatous, baccate, woodland Liliaceae (e.g. Prosartes, Tricyrtis) respectively, and suggest that the latter morphology is plesiomorphous in this part of Liliales ("concerted convergence" and "concerted plesiomorphy": see also Givnish 2003; especially Givnish et al. 2004b, 2005, 2006b).
Bacterial/Fungal Associations. For fungi on Liliaceae s.l., see Savile (1961).
Genes & Genomes. For genome size and chromosome length and much else, see Peruzzi et al. (2009) and also Pellicer et al. (2013), and for genome size in Tulipa, see Zonneveld (2009). Lilium and relatives have very large genomes, those of Tulipa and relatives rather smaller (and that of Gagea may be only some 6.6 pg (1C value); the genome of Medeola is also quite large, so large genomes may be a feature of Lilioideae as a whole (Pellicer et al. 2013). Indeed, 1C values in Fritillaria range from 190-540 times the size of the Arabidopsis genome, being around 30-85 Gb in size, and substantial variation can occur between closely related clades (Ambrozovâ et al. 2011; Day et al. 2014). In Fritillaria, at least, the large genomes are made up of many different repeat families, the repeated DNA not being removed (Kelly et al. 2015).
In Lilium and relatives, the largest chromosomes are 14-22.9 µm long and the smallest are 7.3-12 µm, while in Tulipa and relatives the comparable figures are 5.5-12.3 µm and 1.8-5.2 µm respectively. This emphasizes the differences between the two groups within Lilieae - and the taxa being compared all had n = 12 (Peruzzi et al. 2009). For chromosomes in Lilieae, see Gao et al. (2012) and for those in Lilioideae, see Xie et al. (1992).
At least some mitochondrial genes show an accelerated rate of change in this clade (G. Petersen et al. 2006).
Chemistry, Morphology, etc. For the distribution of tuliposide and the possibly biosynthetically related γ-methyleneglutamic acid, the latter reported also from Haworthia (Asparagales:Asphodelaceae, see Fowden and Steward (1957) and Slob et al. (1975). Lilium, at least, has storage mannans in the vegetative tissues (Meier & Reid 1982).
In Streptopus (Streptopoideae) the pedicel is adnate to the stem. The flowers of Lilium are shown with the median member of the outer whorl in the adaxial position (Spichiger et al. 2004; see also Eichler 1874). For floral development, see Tzeng and Yang (2001); B-class genes are not expressed in the outer whorl of tepals (see also Asparagaceae:Asparagoideae). The pollen grains of the family are relatively large (e.g. 74-139 µm long - Handa et al. 2001), and the sulcus of Lilium grains can be seen even under a dissecting microscope. Medeola has been described as having crassinucellate ovules and lacking a nucellar cap, but illustrations suggest that it has an ovule rather like that of other Liliaceae (Berg 1962 and references). In Clintonia the chalazal megaspores degenerate and the endosperm is diploid (Lord 2009). There are a variety of seed dormancy mechanisms in the family, and the embryo may grow extensively after dispersal but before germination - Cardiocrinum is an example (Kondo et al. 2006).
Some general information is taken from Schnarf (1929, 1948) and Tamura (1998: Calochortaceae, Liliaceae); for rootstock, growth, etc., see Buxbaum (1938, 1958), Tillich (1998), and Levichev (2013), for some chemistry, see L. Chen et al. (2009), for floral anatomy of Fritillaria, see Novikoff and Kazemirska (2012), and for chromosome numbers, etc., see Peruzzi et al. (2009) and Yin et al. (2014).
Phylogeny. The limits of the family adopted here are congruent with a phylogeny presented by Hayashi and Kawano (2000), although the sampling there was poor. The clade [Clintonia + Medeola] is consistently sister to the rest of Lilioideae (e.g. Patterson & Givnish 2002; Fay et al. 2006c), from which it differs somewhat morphologically. Calochortus and relatives are not monophyletic in Rudall et al. (2000), but their paraphyly is not clear, either. However, support in general is stronger in Patterson and Givnish (2002: esp. ndhF and combined trees) and Rønsted et al. (2005), although that for the [Calochortoideae + Streptopoideae] clade is still not very high. In Fay et al. (2006c: two genes), the positions of neither Calochortus and Tricyrtis had any support. In the summary tree in Peruzzi et al. (2009), Lilioideae and Streptopoideae are well supported, as is some structure within the former, Calochortus, but not Tricyrtis, linked with the latter. Indeed, the monophyly of Calochortoideae is questionable, Tricyrtis linking with Streptopoideae in J. S. Kim et al. (2013).
Streptopus, Scoliopus and Prosartes make up the three genera included in Streptopoideae (e.g. Shinwari et al. 1994a, b; S.-C. Chen et al. 2007), even appearing linked in morphological analyses (Patterson & Givnish 2002). Fay et al. (2006c) found the strongly supported relationships [Streptopus [Scoliopus + Prosartes]], c.f. the character optimizations in Patterson and Givnish (2002).
For a phylogeny of Fritillaria and Lilium, see Rønsted et al. (2005a) and especially Day et al. (2014). The monophyly of Fritillaria is not yet established, with Fritillaria subgenus Liliorhiza being of uncertain position (?sister to Lilium and the rest of Fritillaria). For more detailed phylogenies of Lilium, see C. S. Lee et al. (2011: Korean species), Gao et al. (2013: esp. chromosomes) and Du et al. (2014: Chineae species). The latter study focused on high-altitude East Asian species, and found that different genes gave different topologies, one more consistent with morphological relationships, the other with geography. For the relationships of Gagea and Lloydia, the latter para/polyphyletic, see Peterson et al. (2008) and Zarrei et al. (2009). Hybridization is important in speciation in Gagea (Peterson et al. 2009).
Classification. Lloydia is to be included in Gagea (Peterson et al. 2008; Zarrei et al. 2009). For a classification of Fritillaria, see Rix (2001), and for that of Tulipa, see Christenhusz et al. (2013).
Previous Relationships. Cronquist (1981) and many earlier authors circumscribed Liliaceae very broadly, for instance, Cronquist included some 280 genera and 4,000 species in the family. Ex-Liliaceae are now scattered widely through Liliales and Asparagales in particular. Streptopus and Scoliopus (Streptopoideae) have been included in a narrowly-drawn Uvulariaceae, but the other members of that family are in Colchicaceae above, while Prosartes used to be included in Disporum, also now in Colchicaceae (Shinwari et al. 1994a, b).
[Smilacaceae [Philesiaceae + Rhipogonaceae]]: lianes/vines; stem fructans 0; vessel elements in stems, with scalariform perforation plates; leaf with petiole and blade, blade with midrib, venation reticulate; endothecium with spiral thicekenings; fruit a berry; testa disintegrates; endosperm with thick, pitted walls.
Classification. Rudall et al. (2000) suggested that Philesiaceae could be included in Smilacaceae - see characters like pollen, endosperm storage, disintegrating testa, and absence of stem fructans.
SMILACACEAE Ventenat, nom. cons. Back to Liliales
Lianes or vines (herbs), stems monopodial (sympodial by apical abortion); flavonols +; (primary thickening meristem +); vessel elements (in stem 0) and leaves, with scalariform perforation plates; stem bundles in a ring [?]; mucilage cells +; cuticle ± with parallel platelets, stomatal type irregular, unoriented; leaves two-ranked, blade formed from the primordial leaf apex, with 4-6 main veins, (vein endings free), vernation conduplicate, involute or supervolute-involute, petiole with paired lateral tendrils, spines +/0; plant dioecious; inflorescence umbellate; flowers small, <8 mm across; T with single trace, median member of outer whorl adaxial, outer 3 valvate, (± connate); staminate flowers: A 3-12, (± connate - Heterosmilax s. str.), latrorse to introrse, bisporangiate, monothecal; nectariferous trichomes on A; primary parietal layer gives rise to two secondary parietal layers, the outer producing the endothecium and middle layer, the inner producing the tapetum only [dicotyledonous type], (exothecium also with thickenings); pollen inaperturate, ± spherical, ± spinulose, ektexine thin, endexine thick; ?pistillode; carpellate flowers: staminodes +; style short/0, branches stigmatiferous, long, stigma dry; ovule 1(-2)/carpel, ± apical, pendulous, (straight), apotropous, outer integument 6-10 cells across, inner integument ca 2 cells across, parietal tissue 3-5 cells across, hypostase +; seeds rounded (subangled), testa ± elastic, tegmen persistent, exo- and endotegmen with cuticle; endosperm with aleurone and fatty oils; embryo minute to small; n = 14-16 [x = ?8], chromosomes 1.25-5.4(-9.7) µm long; cotyledon not photosynthetic, primary root well developed, epicotyl elongated, ligule +.
1[list]/210. Pantropical to temperate (map: from Fl. Austral. 46. 1986; Fl. N. Am. 26: 2002; Australia's Virtual Herbarium xii.2013; Seberg 2007; Qi et al. 2013). [Photo - Flower, Fruit.]
Age. Divergence within this clade may have begun at the end-Eocene ca 40 m.y.a. (Qi et al. 2012).
Evolution. Divergence & Distribution. Smilax aspera (East Africa, Mediterranean, Indian continent) may be sister to the rest of the genus, within which there are two clades, largely New World and largely Old World (Cameron & Fu 2006; Qi et al. 2012, 2013). C. Chen et al. (2014) looked at the biogeography of Smilax aspera (see below) in particular, but their fossil constraints were questioned by Denk et al. (2015). Within the New World clade, there may have been three shifts to the Old World (Denk et al. 2015).
Kong et al. (2007) discuss phylogeny and karyotype evolution.
Chemistry, Morphology, etc. Smilax tends to have trilacunar nodes. The leaf blade develops from the upper part of the leaf primordium (Martin & Tucker 1985: blade develops from the "leaf apex"; Bharathan 1996). There is considerable variation in the leaf base, which may be more or less expanded and sheathing; there has been some debate as to whether the paired tendrils are stipules or not (Colomb 1887; Sinnott & Bailey 1914), but they are certainly show precocious development (Martin & Tucker 1985). The prophyll is drawn with a closed sheath by Andreata (1997). Overall, foliar variation in Smilax is considerable, and fossils properly to be included in it have been placed in Mahonia (= Berberis), Quercus and Ilex (Denk et al. 2015).
There are suggestions that the umbel is basically cymose in construction, and that plant growth may be sympodial (Andreata 1997; see also Martin & Tucker 1985).
Some information is taken from Arber (1925), but see especially Conran and Clifford (1985: vernation, seedling, etc.) and Conran (1998: general); for pollen, see S.-C. Chen et al. (2006b), for ovules, etc., see Martins et al. (2012) and Ao (2013) and for chromosome numbers, etc., see Peruzzi et al. (2009).
Phylogeny. Molecular analyses result in the Old and New World species of the genus largely forming separate clades, a result not found in morphological analyses (c.f. Cameron & Fu 2006 and S.-C. Chen et al. 2006a). In the former study, Smilax aspera is sister to the rest of the family, although S. vitiensis was not included (see also Qi et al. 2012, esp. 2013), in the latter, S. vitiensis is in this position and S. aspera is apparently well embedded, although not with much support.
Classification. The morphology-based infrageneric classification is not supported by recent work (Qi et al. 2013).
Previous Relationships. Smilacaceae of Cronquist were more broadly circumscribed; the twelve genera he included are now scattered throughout Liliales and some are in Asparagales (see Asparagaceae-Lomandroideae).
[Philesiaceae + Rhipogonaceae]: cuticular wax with parallel platelets; blade vernation conduplicate-flat or curved; chromosomes heteromorphic.
Age. The age of this node is estimated as (55.4-)47, 33(-25.4) m.y. (Vinnersten & Bremer 2001: note topology) or ca 50.7 m.y. (Chacón et al. 2012b).
Evolution. Divergence & Distribution. Diversification in this clade has slowed down (Hertweck et al. 2015: c.f. topology).
Classification. Kim et al. (2013) suggested that the two families could be merged.
PHILESIACEAE Dumortier, nom. cons. Back to Liliales
(Shrub), epiphytic; chelidonic acid?; velamen +; tannin and mucilage cells 0; vessels 0 [Carlquist]; (stomata ?type, oriented transverse to long axis of leaf [Philesia]); leaves two-ranked or spiral, blade with 2 main veins; (P whorls very different - Philesia); A connate basally, (free), anthers dehiscing by pores, (introrse - Lapageria); ?endothecial thickening; pollen inaperturate, surface spinose; placentation intrusive parietal, stigma dry or wet; ovules many/carpel, parietal tissue ca 1 cell across; seed exo- and endotegmic; endosperm development?, with aleurone layer and fatty oils; n = 15, 19, chromosomes 2.5-12 µm long; cotyledon not photosynthetic, primary root well developed.
2[list]/2. S. Chile. [Lapageria Flower.]
Chemistry, Morphology, etc. Some information is taken from Conran and Clifford (1985, 1998); see Carlquist (2012a) for xylem anatomy.
Synonymy: Lapageriaceae Kunth
RHIPOGONACEAE Conran & Clifford Back to Liliales
Stems with prickles; flavonols +; mucilaginous cells +; stomata unoriented; leaves opposite, blade with 4 near-basal main veins; inflorescence various, but ± racemose; flowers rather small [8 mm across]; A latrorse to introrse; tapetum amoeboid; pollen prolate, surface reticulate; style short, unbranched, stigma lobed, wet; ovules 2/carpel, ?morphology; seeds rounded (subangled); exo- and endotegmen with cuticle; endosperm with starch, ?embryo; n = 15; seedling?, ligule 0.
1[list]/6. New Zealand to New Guinea (map: from Fl. Austral. 46. 1986, fossil localities [see below] in green).
Age. Fossil Rhipogonum is reported from the Eocene of Tasmania (Conran et al. 2009b) and from around 52.2 m.y.a. in Patagonian deposits (Carpenter et al. 2014).
Evolution. Divergence & Distribution. Rhipogonum had a broad distribution in the southern hemisphere, despite its current rather restricted distributuion (Carpenter et al. 2014; Wilf & Escapa 2014).
Chemistry, Morphology, etc. Some information is taken from Arber (1925), but see especially Conran and Clifford (1985: vernation, seedling, etc.; 1986: general), and Conran (1998: general, under Smilacaceae); for pollen, see S.-C. Chen et al. (2006b).