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Biosystems - An International Journal Dealing with all Aspects of Plant Official Journal of the Societa Botanica Italiana

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A new infrafamilial taxonomic setting for , with a key to genera and tribes

L. Peruzzi

To cite this article: L. Peruzzi (2016): A new infrafamilial taxonomic setting for Liliaceae, with a key to genera and tribes, Plant Biosystems - An International Journal Dealing with all Aspects of Plant Biology, DOI: 10.1080/11263504.2015.1115435

To link to this article: http://dx.doi.org/10.1080/11263504.2015.1115435

Published online: 11 Jan 2016.

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Download by: [La Trobe University] Date: 22 February 2016, At: 03:53 Plant Biosystems, 2016 http:/dx.doi.org/10.1080/11263504.2015.1115435

A new infrafamilial taxonomic setting for Liliaceae, with a key to genera and tribes

L. PERUZZI*

Dipartimento di Biologia, Università di Pisa, Pisa,

Abstract Based on currently available morphological, karyological, and phylogenetic information, a taxonomic setting of Liliaceae is provided. The is here organized in 6 tribes, for a total of 15 genera and about 900 . An identification key for tribes and genera is also provided.

Keywords: Calochorteae, , Lilieae, Medeoleae, monocots, Streptopeae, , Tricyrtideae, Tulipeae

Luke 12: 27 Consider the lilies, how they grow: they 2003, 2009). The genera belonging to families with- neither toil nor spin; but I tell you, not even Solomon in in are marked by the presence of septal all his glory clothed himself like one of these nectaries at the base of , by dark brown to blackish, rich in phytomelan, with cells of the outer coat collapsed (Dahlgren et al. 1985). By contrast, Introduction according to the same authors, the genera belonging to families within Liliales show nectaries on , The family Liliaceae was subjected to several – even seeds light brown, lacking phytomelan, with cells of dramatic – circumscription changes over the last 2–3 the outer coat intact. Notably exceptions to this rule decades (see, Peruzzi et al. 2009 for a short review). are Iridaceae and Orchidaceae, currently placed in However, a general agreement concerning the in- Asparagales on phylogenetic grouds (Chase et al. cluded taxonomic groups and its sister relationship 1995; APG 1998, 2003, 2009), but placed with- with , within Liliales, has been reached in Liliales by Dahlgren et al. (1985), based on the in the last 20 years (Chase et al. 1995; APG 1998, above-cited character states. However, Iridaceae and 2003, 2009; Patterson & Givnish 2002; Fay et al. Orchidaceae have three to two–one , respec- 2006; Leitch et al. 2007; Peruzzi et al. 2009; Kim tively, and both have inferior ovary (Goldblatt et al. et al. 2013; Petersen et al. 2013). In particular, the 1998; Vogel 1998), while Liliales have mostly superi- Downloaded by [La Trobe University] at 03:53 22 February 2016 most important papers providing a strong phylogenetic or ovary or, if inferior, have six stamens (Vogel 1998). backbone for the family are those of Patterson and Liliaceae are easy to distinguish from the remain- Givnish (2002), Fay et al. (2006), Kim et al. (2013), ing nine families presently recognized in Liliales and Petersen et al. (2013); the first authors focused (APG 2009), thanks to several evident morphological on Liliaceae, the others with Liliales but with a large features. They share the absence of base sheath- sampling of genera and families. ing with , Rhipogonaceae, and Smi- Traditional angiosperm classifications used to in- lacaceae, but Liliaceae are never climbers or clude most of the monocots bearing showy as the three above-cited families, or even as Alstro- with six tepals, six stamens, and a trilocular superior emeriaceae ( Luzuriageae) and Petermanniace- ovary in Liliaceae (e.g. Cronquist 1981). Since the ae (Conran 1998; Conran & Clifford 1998a, 1998b, seminal studies of Dahlgren et al. (1985), the genera 1998c). In addition, Liliaceae are never parasitic formerly classified under Liliaceae have been distrib- as (Neinhuis & Ibisch 1998); they uted among many smaller families organized in two have not inferior ovary as (tribe Al- main orders: Asparagales and Liliales (APG 1998, stroemerieae), Corsiaceae, and

Correspondence: Lorenzo Peruzzi, Dipartimento di Biologia, Unita di Botanica, Universita di Pisa, via Derna 1, 56126 Pisa, Italy. Email: lorenzo.peruzzi@ unipi.it

© 2016 Societa Botanica Italiana 2 L. Peruzzi

(Bayer 1998; Kubitzki 1998; Neinhuis & Ibisch 1. Tribe Streptopeae Baker, J. Linn. Soc., Bot. 1998); they do not show resupinate as most 14: 522. 1875. (Figure 1A–C) Alstroemeriaceae (Bayer 1998; Conran & Clifford 1998a); they lack cells with raphide crystals, occur- = Scoliopeae Baker, J. Linn. Soc., Bot. 14: 509. ring in (Tamura 1998c, 1998d) and, 1875. finally, show anthers extrorse, and not mostly int- = Scoliopinae S.Watson, Proc. Amer. Acad. Arts 14: rorse as in (Nordenstam 1998). 222. 1879. Liliaceae as currently circumscribed include sev- = Streptopoideae Mabberley ex Reveal, Phytoneu- eral plants of relevant economic importance for their ron 2012–37: 219. 2012. [23 Apr 2012] remarkable beauty, such as (American lily – C. nuttallii Torr. is the official of Utah, Included genera: D.Don (6 species), USA and its are also edible), , Fritillar- Torr. (2 species), Michx. (7 ia, Tulipa, , one of the oldest ornamental plants species) of the Western world being indeed L. candidum L. Plants herbaceous, never climbers, rhizomatous; Some species of Calochortus, , Fritil- fruit a berry or a (in Scoliopus); monosporic laria, (incl. Lloydia), Lilium, , and embryo-sac formation of Polygonum-type, nucel- Tulipa are edible or used as drugs, especially in la with long basal part, placentation axile (Tamura (Tamura 1998a, 1998b). 1998b); chromosomes generally short 1–5 μm (but However, a critical, integrative, and supported 5–13 μm in Scoliopus); genome size 4–15(30) pg, infrafamiliar taxonomic setting is still missing. This x = 7–9: x = 8(9) in Prosartes, x = 8–9 in Scoliopus, is exactly the aim of this paper, which takes into ac- x = (7)8 in Streptopus (Peruzzi et al. 2009). count the morphological, karyological, and phyloge- The tribe Streptopeae represents one of the ear- netic information available in the literature. liest branching lineages within Liliaceae, for which some authors suggest a sister relationship with Calo- chortus + Tricyrtis (Patterson & Givnish 2002), others Taxonomic setting with Tricyrtis (Kim et al. 2013) or with Calochortus Family Liliaceae Juss., Gen. Pl.: 48. 1789. nom. cons. (Fay et al. 2006) only. Despite this, the established phylogenetic relationships among the three genera = Tulipaceae Batsch, Dispos. Gen. Pl. Jenens.: 48. are the following (Patterson & Givnish 2002; Fay 1786. et al. 2006; Kim et al. 2013): ((Prosartes, Scoliopus), = Erythroniaceae Martynov, Tekhno-Bot. Slovar: Streptopus). 238. 1820. 2. Tribe Calochorteae Melchior, Pflanzenfam. = Calochortaceae Dumort., Anal. Fam. Pl.: 53. ed 12, 2: 520. 1964. (Figure 1D) 1829. = Fritillariaceae Salisb., Gen. Pl.: 56. 1866. = Calochortoideae Thorne & Reveal ex Reveal, Phy- = Medeolaceae. S.Watson in Takht., Sist. Magnoli- toneuron 2012–37: 216. 2012. [23 Apr 2012] of.: 291, 31. 1987. Included genera: Calochortus Pursh. (ca. 65 = Scoliopaceae Takht., Bot. Zhurn. Moscow & Len- species) Downloaded by [La Trobe University] at 03:53 22 February 2016 ingrad. 81(2): 86. 1996. Plants herbaceous, never climbers, bulbous; fruit = Tricyrtidaceae Takht., Divers. Classif. Fl. Pl.: 482. a septicide capsule; monosporic embryo-sac forma- 1997. nom. cons. tion of Polygonum-type, nucella with long basal part, placentation axile (Tamura 1998b); chromosomes Plants herbaceous, never climbers or shrubs, nev- generally short, 1–6(13) μm; genome size 4–15(30) er parasitic, bulbous or rhizomatous; leaf sheaths ab- pg, x = 6–10 (Peruzzi et al. 2009). sent, leaves never resupinate; flowers with two whorls The tribe Calochorteae represents a lineage cer- of 3 + 3 tepals, two whorls of 3 + 3 stamens (rare- tainly distinct from others, but of uncertain phy- ly reduced to one), with extrorse anthers, syncarpic logenetic placement: sister to Tricyrtis for Patterson superior ovary made up of three carpels; presence and Givnish (2002) and Petersen et al. (2013), sister of nectaries on tepals; hermaphrodite (rarely male to Streptopeae for Fay et al. (2006), or even sister sterile, but relatively often female sterile) flowers; to Medeoleae + Lilieae + Tulipeae for Kim et al. fruit a capsule (loculicide, septicide) or a berry; (2013). Concerning the phylogenetic relationships seeds light brown, lacking phytomelan, with cells of among species within Calochortus, a detailed cpDNA the outer coat intact; cells lacking raphide crystals; phylogeny is available (Patterson & Givnish 2004). monosporic or tetrasporic embryo-sac formation ­(Tamura 1998a, 1998b; Peruzzi et al. 2012; Zhang 3. Tribe Tricyrtideae [Trycirteae] K.Krause in En- et al. 2014); x = 6–10, 12–13 (Peruzzi et al. 2009). gler, Pflanzenfam. ed. 2, 15: 268. 1930. (Figure 1E) A new infrafamilial taxonomic setting for Liliaceae 3

Figure 1. Flower diversity in the former “Calochortaceae” Tamura, currently tribes Scoliopeae, Calochorteae and Tricyrtideae. A, Prosartes (P. trachycarpa S.Watson; NPS Photo, J.W. Stockert, 1974, public image); B, Scoliopus (S. bigelowii Torr.); C, Streptopus (S. amplexifolius (L.) DC.); D, Calochortus (C. superbus Purdy ex Howell); E, Tricyrtis (T. formosana Baker).

Figure 2. Flower diversity in the tribe Medeoleae. A, (C. borealis (L.) Raf.); B, (M. virginiana L., picture by D.G. Smith).

= Tricyrtidoideae Thorne & Reveal, Bot. Rev. Lan- = Medeoloideae (Benth. & Hook.f.) M.N.Tamura caster. 73: 78. 2007. [29 Jun 2007] in Kubitzki, The families and genera of vascular Included genera: Tricyrtis Wall. (18 species) plants 3: 350. 1998. Downloaded by [La Trobe University] at 03:53 22 February 2016 Plants herbaceous, never climbers, rhizomatous; = Medeolinae S.Watson, Proc. Amer. Acad. Arts 14: fruit a septicide capsule; monosporic embryo-sac 222. 1879. formation of Polygonum-type, nucella with short ba- sal part, placentation parietal (Tamura 1998b); chro- Included genera: Clintonia Raf. (5 species), Me- mosomes generally short, 1–6(13) μm; genome size deola L. (1 species) 4–15(30) pg, x = 13 (Peruzzi et al. 2009). Plants herbaceous, never climbers, rhizomatous; The tribe Tricyrtideae represents a lineage cer- fruit a berry; tetrasporic 4-nucleate embryo-sac tainly distinct from others, but of uncertain phyloge- (Clintonia-type) formation, nucella with a short ba- netic placement: sister to Calochortus for Patterson sal part; vesicular-arbuscular mycorrhizae (VAM) of and Givnish (2002) and Petersen et al. (2013), sis- Clintonia-type (Tamura 1998a); chromosomes gen- ter to Medeoleae + Lilieae + Tulipeae for Fay et al. erally large, x = 7 (Peruzzi et al. 2009). (2006), or even sister to Streptopeae for Kim et al. The tribe Medeoleae is placed with high support (2013). Concerning the phylogenetic relationships and unanimously as the group sister to Lilieae + Tu- among species within Tricyrtis, a cpDNA phylogeny lipeae (Chase et al. 1995; Patterson & Givnish 2002; is available (Hong & Jury 2012), and a new species Fay et al. 2006; Kim et al. 2013; Petersen et al. was discovered recently (Peng et al. 2007). 2013). Concerning the phylogenetic relationships among species within Clintonia, a cpDNA phylogeny 4. Tribe Medeoleae Benth. & Hook.f., Gen. Pl. 3: is available (Hayashi et al. 2001). 750, 762. 1883. (Figure 2) 4 L. Peruzzi

some authors are still describing new species under the former generic name (Gao et al. 2012a). Studies more focused on were published by Türktaş et al. (2012) and Day et al. (2014), while Lilium evolution was studied by Nishikawa et al. (1999), Hayashi and Kawano (2000), Ikinci et al. (2006), Rešetnik et al. (2007), Ikinci and Oberprieler (2010), Muratović et al. (2010), and Gao et al. (2012b, 2013). The established phylogenetic relatioships among the four genera are the following: (Notholirion, (Cardiocrinum, (Fritillaria, Lilium))), in all the cited phylogenetic studies. 6. Tribe Tulipeae Duby, Bot. Gall. 1: 461. 1828. (Figure 4)

= Gageeae Rouy, Fl. 12: 380. 1910. = Lloydieae Buxb., Bot. Arch. 38: 389. 1937. = Tulipoideae Kostel, Allg. Med.-Pharm. Fl. 1: 168. 1831.

Included genera: Honda (5 species), L. (15 species), Gagea Salisb. (= Lloydia Salisb.; ca. 300 species), Tulipa L. (ca. 150 species) Plants herbaceous, never climbers, bulbous, composed by only 1 scale; anthers pesudo-basifixed; fruit a loculicide capsule with seeds not winged; tet- Figure 3. Flower diversity in the tribe Lilieae. A, Notholirion rasporic 7–8 nucleate embryo-sac formation, nucella (N. campanulatum Cotton & Stearn); B, Cardiocrinum (C. with a short basal part; VAM not of Clintonia-type giganteum (Wall.) Makino); C, Fritillaria (F. messanensis (Tamura 1998a); chromosomes generally large, Raf. subsp. messanensis); D, Lilium (L. jankae A.Kern.). 2–11 μm (1–6 μm in Gagea), genome size (3)4– 25(70) pg, x = (9)12, polyploidy common (Peruzzi 5. Tribe Lilieae Lam. & DC., Syn. Pl. Fl. Gall.: et al. 2009). 159. 1806. (Figure 3) The tribe Tulipeae results with high support and unanimously as the group sister to Lilieae (Chase et al. = Eaton, Bot. Dict., ed. 4: 27. 1836. 1995; Patterson & Givnish 2002; Fay et al. 2006; Included genera: Notholirion Wall. (5 species), Kim et al. 2013; Petersen et al. 2013). All these Cardiocrinum (Endl.) Lindl. (3 species), Fritil- studies also support the independence of the laria L. (ca. 130 species), Lilium L. (= Amana from Tulipa. Two new species were also Downloaded by [La Trobe University] at 03:53 22 February 2016 Franch.; ca. 120 species) recently discovered for the former genus (Tan et al. Plants herbaceous, never climbers, bulbous, bulb 2007; Han et al. 2014). The phylogenetic relationships composed by 2–3 to many scales; anthers dorsifixed; and classification of the large genus Tulipa were fruit a loculicide capsule with seeds usually winged; thoroughly investigated by Türktaş et al. (2013) and tetrasporic 7–8-nucleate embryo-sac formation, Christenhusz et al. (2013), and those of Erythronium nucella with a short basal part; VAM not of Clinto- by Allen et al. (2003) and Clennett et al. (2013). nia-type (Tamura 1998a); chromosomes generally Concerning the genus Gagea, the largest among large, genome size (15)30–65 (130) pg, x = (9)12, Liliaceae, many evolutionary studies were published in polyploidy rare (Peruzzi et al. 2009). recent years (Peterson et al. 2004, 2008, 2009, 2010, The tribe Lilieae is placed with high support and 2011; Peruzzi et al. 2008a, 2008b, 2011; Zarrei et al. unanimously as the group sister to Tulipeae (Chase 2009, 2012; Peruzzi 2012; Tison et al. 2013), in parallel et al. 1995; Patterson & Givnish 2002; Fay et al. with the discovery and description of new species. The 2006; Kim et al. 2013; Petersen et al. 2013). The inconsistency of the genus Lloydia, now synonymized phylogenetic relationships among the large genera with Gagea (Peruzzi et al. 2008b), was first evidenced by Fritillaria and Lilium were investigated by Rønsted Peterson et al. (2004), and confirmed by all subsequent et al. (2005). The same authors also first revealed phylogenetic studies. Gagea always results sister to the the inconsistency of the genus Nomocharis, now syn- other three genera, whose relationships are instead not onymized with Lilium (Peruzzi et al. 2009), albeit fully resolved (Kim et al. 2013; Petersen et al. 2013). A new infrafamilial taxonomic setting for Liliaceae 5

Figure 4. Flower diversity in the tribe Tulipeae. A, Amana (A. edulis (Miq.) Honda, from http://wplan.sakura.ne.jp/hyakka/amana.html); B, Erythronium (E. dens-canis L.); C, Tulipa (T. sylvestris L.); D, Gagea (G. peduncularis (C.Presl) Pascher).

Infrafamilial identification key for Liliaceae 4. Stamens 6; outer and inner tepals similar; style subentire; fruit a berry ...... 5 The morphological information is derived from 5. axillary; filaments flattened at ­Tamura (1998a, 1998b); Patterson and Givnish base, less than 3 mm long; ovules 6–8 in each locule (2002) and Tan et al. (2005). (Figure 1C) ...... Streptopus 1. strongly tripartite (if subentire, the 5. Inflorescence terminal; filaments filiform, more lowers are incospicuous) (Calochortaceae sensu than 6 mm long; ovules 2–6 in each locule (Figure ­Tamura) ...... 2 1A) ...... Prosartes Downloaded by [La Trobe University] at 03:53 22 February 2016 1. Stigma (more or less) trilobate (if tripartite, the 6. Plants rhizomatous; fruit a berry ...... flowers are incospicuous) and subsessile ...... (Medeoleae) 7 ...... (Liliaceae sensu Tamura) 6 6. Plants bulbous; fruit a loculicide capsule ...... 2. Outer tepals with nectary glands globosely ...... (Lilioideae sensu Tamura) 8 pouched or shortly spurred; stylodia apically bifid 7. Presence of cauline leaves; flowers nodding; (Figure 1E) ...... (Tricyrtideae) Tricyrtis tepals pale greenish yellow, recurved; style trisected 2. Outer tepals not as above; stylodia always unifid (Figure 2B) ...... Medeola ...... 3 7. Absence of cauline leaves; flowers erect to hori- 3. Plants bulbous; fruit a septicide capsule; outer zontal; tepals white to yellow, spreading; style trilo- 3 tepals much smaller than inner 3 (Figure 1D) ...... bate (Figure 2A) ...... Clintonia ...... (Calochorteae) Calochortus 8. Bulb composed by 2–3 to many scales; seeds 3. Plants rhizomatous; fruit a berry or a capsule; usually winged; anthers generally dorsifixed ...... outer 3 tepals similar to or much larger than inner 3 ...... (Lilieae) 9 ...... (Streptopeae) 4 8. Bulb composed by only 1 scale; seeds not 4. Stamens 3; outer tepals petaloid, inner tepals winged; anthers pseudo-basifixed ...... narrowly linear; style tripartite; fruit a capsule­ ...... (Tulipeae) 12 (Figure 1B) ...... Scoliopus 9. Leaves broad, reticulate; perigone tubular, not recurved (Figure 3B) ...... Cardiocrinum 6 L. Peruzzi

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