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Journal of Plant Research

, Volume 131, Issue 3, pp 411–428 | Cite as

Floral structure and development in Nartheciaceae (Dioscoreales), with special reference to ovary position and septal nectaries

  • Hiroshi Tobe
  • Yu-Ling Huang
  • Tomoki Kadokawa
  • Minoru N. Tamura
JPR Symposium Floral development –Re-evaluation of its importance–

Abstract

We present a comparative study of the floral structure and development of Nartheciaceae, a small dioscorealean family consisting of five genera (Aletris, Lophiola, Metanarthecium, Narthecium, and Nietneria). A noticeable diversity existed in nine floral characters. Analyses of their respective character states in the light of a phylogenetic context revealed that the flowers of Nartheciaceae, whose plesiomorphies occur in Aletris and Metanarthecium, have evolved toward in all or part of Lophiola, Narthecium, and Nietneria: (1) loss of a perianth tube; (2) stamen insertion at the perianth base; (3) congenital carpel fusion; (4) loss of the septal nectaries; (5) unilocular style; (6) unfused lateral carpellary margins in the style; (7) flower with the median outer tepal on the abaxial side; (8) flower with moniliform hairs; and (9) flower with weak monosymmetry. We further found that, as the flowers developed, the ovary shifted its position from inferior to superior. As a whole, their structure changes suggest that the Nartheciaceae flowers have evolved in close association with pollination and seed dispersal. By considering inferior ovaries and the presence of septal nectaries as plesiomorphies of Nartheciaceae, we discussed evolution of the ovary position and septal nectaries in all the monocots.

Keywords

Dioscoreales Flower evolution Monocots Nartheciaceae Ovary position Septal nectary 

Introduction

Nartheciaceae, a small family of monocots, are considered as the first diverging lineage in Dioscoreales (Caddick et al. 2002; Merckx et al. 2006). The family comprises five genera: Aletris (40 spp.), Lophiola (one sp.), Metanarthecium (one sp.), Narthecium (six spp.), and Nietneria (one sp.). They are distributed patchily in the North temperate zone, Venezuela and Guiana and scattered in West Malesia (Stevens 2001 onwards). Until recently, these genera were never treated together as members of the family (for taxonomic history see Merckx et al. 2008). However, recent molecular analyses have revealed that the five genera constitute a distinct family Nartheciaceae (Fuse et al. 2012; Merckx et al. 2008). Among the five genera, Metanarthecium (M. luteo-viride Maxim.) has sometimes been placed in the largest genus Aletris (Hara 1967; Takhtajan 2009; Tamura 1998; Zomlefer 1999). Molecular analyses by Merckx et al. (2008) indicated that M. luteo-viride is embedded in a clade of Aletris, while those by Fuse et al. (2012) showed that M. luteo-viride is a sister group to the rest of the family. Metanarthecium was followed by Aletris which is sister to Lophiola, Nietneria and Narthecium, whereas Lophiola is sister to Nietneria and Narthecium.

Morphologically the genera of Nartheciaceae are relatively well understood. Utech (1978) examined the floral vascular anatomy of Metanarthecium luteo-viride; Sterling (1979) reported the floral vascular anatomy, particularly the gynoecial vasculature of Narthecium californicum Baker and Nietneria corymbosa Klotzsch & Rich. Schomb. Simpson and Dickison (1981) described the floral anatomy and vascular anatomy of Lophiola aurea Ker Gawl. Rudall (2002) described the ovary position and presence or absence of septal nectaries in Aletris, Lophiola, Narthecium, and Nietneria, and presented a few micrographs of the microtome sections of the flowers of A. glabra Bureau & Franch. and Narthecium ossifragum (L.) Huds. Remizowa et al. (2006) also reported the ovary position in N. ossifragum and N. balansae Briq. and showed the development of gynoecium in N. balansae with a few micrographs of the microtome sections and scanning electron micrographs of N. balansae. Remizowa et al. (2008) further reported the floral development in M. luteo-viride (and briefly in N. balansae); they confirmed that the postgenital fusion of carpels is associated with the presence of septal nectaries in Metanarthecium.

Consequently, the previous studies of Nartheciaceae (e.g. Fuse et al. 2012; Remizowa et al. 2006; Tamura 1998) showed that the flowers are diverse in their morphology, particularly in the ovary position and presence or absence of septal nectaries within the family. In fact, the ovary is almost superior in Metanarthecium and Narthecium ossifragum, slightly semi-inferior in N. balansae, semi-inferior in Aletris glabra and Lophiola, and inferior in Nietneria (e.g. Fuse et al. 2012; Remizowa et al. 2006; Rudall 2002; Tamura 1998). Septal nectaries are present in Aletris and Metanarthecium, while they are absent in Lophiola, Narthecium, and Nietneria. However, these floral traits of the individual genera are not always shown with explicit evidence, such as micrographs showing floral structure and development. Thus far, the micrographs of microtome sections and/or scanning electron micrographs are limited to part of the family as mentioned above. In particular, the evolution of ovary position and septal nectaries needs re-examination based on the morphological and anatomical studies of flowers across the whole range of nartheciaceous taxa (Fuse et al. 2012). Furthermore, the presence or absence of the floral tube and moniliform hairs have been reported (for review see Remizowa et al. 2008 and references cited therein).

In the present study, we present an extensive comparison of the floral structure among all the five genera to understand the floral evolution in Nartheciaceae. We document the floral development of individual genera except Nietneria, because flowers in early developmental stages may reveal essential structures which might disappear during the late developmental stages (for one of the most recent examples see Tobe 2012: Cardiopteris). We focus on the shift of ovary position during the development of flower which has never been documented in previous studies. A part of our data, particularly in relation to the flowers of Metanarthecium and Narthecium, has been published already (Remizowa et al. 2008; Rudall 2002). However, in contrast to any published data, the flowers in the micrographs presented in this paper are consistently arranged with their adaxial side above. This enabled exact comparisons throughout the family. Finally, the evolution of floral characters in Nartheciaceae, as well as of the ovary position and septal nectaries in all monocots, will be discussed in light of phylogenetic context.

Materials and methods

Six species of the five genera Aletris foliata (Maxim.) Makino et Nemoto, A. spicata (Thunb.) Franch., Lophiola aurea Ker Gawl., Metanarthecium luteo­viride Maxim., Narthecium asiaticum Maxim., and Nietneria corymbosa Kl. Et Rich. were investigated in the present study. Their collection data are presented in Table 1. Except for those of Nietneria, flower buds at various stages of development were collected from their natural habitats and fixed with FAA (five parts stock formalin; five parts glacial acetic acid; 90 parts 50% ethanol). Several flowers of Nietneria were collected from the herbarium specimens for anatomical study. They were rehydrated in a 2% ammonia solution for six hours before being transferred to FAA.

Table 1

Species studied of Nartheciaceae and collection information

Aletris foliata (Maxim.) Makino et Nemoto

Japan. Niigata Pref., Mt. Amakazari. M.N. Tamura et al. 14341 (KYO)

A. spicata (Thunb.) Franch.

Japan. Mie Pref., Seki-cho. S. Fuse 8021 (Bot. Gard., Osaka City Univ.)

Lophiola aurea Ker Gawl.

USA. Florida, Liberty city, Brushy Island. No voucher.

Metanarthecium luteo-viride Maxim

Japan: Shiga Pref., Mt. Mikuni M. N. Tamura et al. 8009 (Bot. Gard., Osaka City Univ.)

Narthecium asiaticum Maxim.

Japan: Shiga Pref., Mt. Mikuni M. N. Tamura et al. 8012 (Bot. Gard., Osaka City Univ.)

Nietneria corymbosa Kl. Et Rich.

Venezuela. Bolivar, Ptari-tepui. B.K. Holst 3592 (MO)

Some flower buds and nearly mature flowers were dehydrated through an ethanol series and then embedded in Technovit 7100 (Kulzer, Wehrheim, Germany) for microtoming. Serial resin sections cut at a thickness of 5 µm using a rotary microtome equipped with a steel blade were stained with Heidenhain’s hematoxylin and mounted in Entellan® new (Merck, Darmstadt, Germany). They were observed with an Olympus BX­51 microscope.

Character state construction of floral characters was made for Nartheciaceae using other Dioscoreales as outgroup as shown in Table 2. The data of the other Dioscoreales were obtained from Dioscoreaceae and Taccaceae, which are relatively well understood with respect to the floral morphology and structure (Dahlgren et al. 1985; Stevens 2001 onward). Figure 9 shows apomorphies of the floral characters mapped on a phylogenetic tree from Fuse et al. (2012). Further, the distribution of inferior ovaries and septal nectaries on a phylogenetic tree of monocots are presented in Figs. 10 and 11, respectively, and they were obtained using parsimony in Mesquite version 3.3 (Maddison and Maddison 2015). A tree topology of the monocots was obtained by combining a tree of orders in APG IV (2016) with the trees of families in individual orders from Stevens (2001 onwards).

The terminology used for the structure of gynoecium (i.e. synascidiate, symplicate) followed Leinfellner (1950).

Results

General morphology of the flowers

Flowers are borne on racemes. Each flower is pedicellate and subtended by a bract with a single relatively small bracteole on the pedicel. The flowers are bisexual and trimerous, each comprising six tepals in two whorls (three outer and three inner), six stamens in two whorls (three outer and three inner), and three carpels forming a gynoecium. The floral elements are arranged alternately. The inner tepals are similar both in size and shape to the outer tepals. The inner tepals or tepal lobes are imbricate in aestivation. Both the outer and inner tepals, like the stamens, are supplied by a single vascular trace at their bases. Each vascular trace trifurcates upward, so that each outer and inner tepal (or lobe) has three veins.

Metanarthecium

Mature flowers

Before anthesis, flowers of Metanarthecium luteo-viride appear lanceolate in the longitudinal section (Fig. 1a), with an adaxial outer tepal and an adaxial carpel (see bract position in Fig. 1b). Six tepals are connate to form the perianth tube (free from the gynoecium) in the lower part of the flower (Fig. 1a–e), and have free lobes above the perianth tube (Fig. 1f, g, i). The outer stamens are attached to the outer tepal lobes at a slightly higher position than that of the inner stamens attached to the inner tepal lobes (Fig. 1f). No trichomes are formed on the stamen filaments.

Fig. 1

Anatomy of flowers of Metanarthecium luteo-viride. a Longitudinal section of a mature flower, with the adaxial side on the right, obtained by sectioning through line a in e. bi Transverse sections of flower at levels marked bi in a, showing the floral structure and septal nectaries. All figures are presented with the adaxial side above. br bract, bt bracteole, itl inner tepal, otl outer tepal, ne nectary, ov ovule, pt floral tube, sg stigma, st stamen, sty style. Scale bars are 500 µm in a and b. Scale bar in b applies to ci

The gynoecium is composed of two zones: a synascidiate zone from its base to the upper part of the ovary (Fig. 1b–f), and a symplicate zone from the upper part of the ovary to the stigma (Fig. 1g–i). However, the early development of carpels revealed that the gynoecium is largely symplicate as will be described below. The ovary is trilocular throughout its length (Fig. 1b–g). The style is also trilocular in the lower part (Fig. 1h), but the locules are closed in the upper part (Fig. 1i). Ventral sutures of the three carpels remain unfused in the upper part of the ovary (Fig. 1g) and the style (Fig. 1h, i) and are continuous with one another in the center. A compitum is formed in the style (Fig. 1h, i). Septal nectaries are present between the locules in the lower half of the ovary (Fig. 1a, d, e) but absent in the upper half (Fig. 1f, g).

Gynoecial development

During the early developmental stages, three carpels of the gynoecium are free and separate on the adaxial side (Fig. 2a–c, e). Future placental regions are deeply embedded in the receptacle. In the gynoecium prior to initiation of the ovule primordia, about half of the ovary is inferior; thus, the ovary is semi-inferior (Fig. 2b). However, as the ovule primordia are initiated from the placenta, the ovary becomes almost superior (Fig. 2c) as seen in the mature flower (Fig. 1a). Thus, the ovary shifted its position from semi-inferior to almost superior during development (compare the levels indicated by arrows showing the junction between the carpel periphery and stamen base in Fig. 2b, c). Further, the short synascidiate zone occurs in addition to a long plicate zone (Fig. 2c).

Fig. 2

Development of flowers in Metanarthecium luteo-viride. ac Longitudinal sections of flower buds. a Flower bud prior to ovule initiation. b Flower bud with ovule primordia that are just initiated in an ovary locule. c Flower bud with ovule primordia. di Transverse sections (TS) of flower buds, presented with the adaxial side above. d TS at an inferior part, showing ovule initiation. e TS at a superior part, showing that three carpels are free. f TS at a superior part, showing postgenital carpel fusion. g Magnified view of f, showing the initiation of fusion of the lateral carpellary margins. h TS at a lower level of the gynoecium, showing the initiation of the septal nectary. i TS at an upper level of the gynoecium, showing the lateral fusion of the carpels. ca carpel, itl inner tepal, otl outer tepal, ne nectary, ov ovule (primodium), st stamen. Scale bars are 100 µm in ac, e, f, h, i, and 50 µm in d, g

During development, the gynoecium demonstrates postgenital carpel fusion. We document the developmental processes of carpel fusion again as details were not clearly presented in previous studies. In a young gynoecium where the ovule primordia were just initiated, the transverse sections through the inferior part of the ovary show that the carpels are united in the periphery, but are free on both the adaxial and lateral sides (Fig. 2d). In the superior part of the ovary, the carpels are free, although their respective lateral and adaxial margins closely border one another (Fig. 2e). Thereafter, the three carpels begin to fuse at their lateral and ventral margins (Fig. 2f, g). By the time the integument is initiated on the ovule primordia, carpel fusion proceeds on the lateral and/or ventral sides (Fig. 2h, i). However, fusion of the lateral margins of the carpel is incomplete in the lower half of the ovary, where the septal nectaries are formed by the epidermal cells on the lateral margins of the carpels (Fig. 2h). The septal nectary has the lowest end at the base of the superior part of the ovary, where an orifice is present to exude nectar.

In the flowers at anthesis, postgenital carpel fusion of the lateral margins is completed above the level of the sterile synascidiate zone except in the region of septal nectaries. Thus, no carpellary boundary exists in the septum of the style. Each carpel has three vascular bundles, one on the dorsal (abaxial) side and two on the ventral (adaxial) side (Fig. 2f, i).

Aletris

Mature flowers

Flowers of the two Aletris species (A. foliata and A. spicata) showed no differences in the floral structure and development, except in the ovary position. A. spicata has an inferior ovary (Fig. 3a), while A. foliata has a semi-inferior ovary (Fig. 3b). Before anthesis, they appear elliptical in the longitudinal section (Fig. 3a, b). They have an adaxial outer tepal and an adaxial carpel (see bract position in Fig. 3c–h, j). Six tepals connate to form a floral tube with six free tepal lobes above the perianth tube (Fig. 3a–h). The outer stamens are attached to the perianth tube at a slightly higher position than that of the inner stamens. No trichomes are formed on the stamen filaments.

Fig. 3

Anatomy of flowers of Aletris. a Longitudinal section (LS) of mature flower of A. spicata, with the adaxial side on the right. b LS of a mature flower of A. foliata, with the adaxial side on the right side, obtained by sectioning through line b in h. cj Transverse sections of a flower of A. foliata at levels marked cj in b, showing floral structure and septal nectaries. All figures are presented with the adaxial side above. br bract, bt bracteole, itl inner tepal, otl outer tepal, ne nectary, ov ovule, pt perianth tube, sg stigma, st stamen, sty style. Scale bars are 500 µm in ac. Scale bar in c applies to dj

The gynoecium is composed of two zones: a synascidiate zone (Fig. 3c–e), and a symplicate zone (Fig. 3f–j). The ovary is trilocular throughout its length (Fig. 3c–h). The style is also trilocular in the lower part (Fig. 3i). The septal nectaries are present between the locules in the upper half (Fig. 3a: A. spicata) or middle (Fig. 3b: A. foliata) of the ovary.

Gynoecial development

During the early developmental stages, the ovary of Aletris foliata, which has a semi-inferior ovary in their mature flowers (Fig. 3b), is almost inferior (Fig. 4a, b). Thus, the superior position of the ovary shifts slightly upward as the flowers develop. In the flowers at anthesis the ovary appears almost superior (Fig. 4c). Thus, in A. foliata the ovary shifts its position from inferior to semi-inferior during development. Further, the synascidiate zone decreases in the lower part of the gynoecium.

Fig. 4

Development of flowers in Aletris. ac Longitudinal sections of flower buds and open flower of A. foliata. a Flower bud with the ovule primordia in an ovary locule. Note that the ovary is inferior. b Flower bud with the ovule primordia. c Open flower with a semi-inferior ovary. dh Transverse sections (TS) of flower buds of A. foliata, presented with the adaxial side above. d TS at a superior region, showing that the three carpels are separate. eg Three selected successive TSs at an inferior region, presented from top (e) downward (f, g), showing postgenital carpellary fusion. h TS at a lower level of the gynoecium, showing the septal nectary. i TS of a flower bud of A. spicata, showing the septal nectary. ne nectary, ov ovule, pt perianth tube. Scale bars are 500 µm in c, 200 µm in a, b, and d, and 100µ m in ei

The gynoecium shows a postgenital carpel fusion. In a young gynoecium where the ovule primordia are initiated, the three carpels are entirely free in the superior part of the ovary and in the style (Fig. 4d). If we look at the serial microtome sections from the uppermost part of the inferior part of the gynoecium downward, the carpels are free on the adaxial and lateral sides (Fig. 4e, f). Below such a symplicate zone, the carpels are completely fused (Fig. 4g). The fusion of the lateral margins is incomplete at the upper part of the symplicate zone, where septal nectaries are formed by the epidermal cells of the lateral margins (Fig. 4h: A. foliata, Fig. 4i: A. spicata). The upper part of the nectary extends to the base of the superior part of the ovary (Fig. 4h) and is located opposite to an orifice for exuding nectar. In the flowers at anthesis, postgenital fusion of the lateral margins is complete above the level of the sterile synascidiate zone except in the septal nectaries. No carpellary boundary exists in the septum of the style, either. Each carpel has three vascular bundles, one on the dorsal (abaxial) side and two on the ventral (adaxial) side.

Lophiola

Mature flowers

Before anthesis, the flowers of Lophiola aurea appear narrowly elliptical in the longitudinal section (Fig. 5a). Each flower has an adaxial outer tepal and an adaxial carpel (see bract position in Fig. 5b). Their ovary is semi-inferior (Fig. 5a, c–e). A perianth tube (free from the gynoecium) is barely formed. The outer and inner tepals are free in the superior part of the ovary, although fusion between tepals is observed for a very short distance in the transverse sections (Fig. 5e). There are no septal nectaries throughout the ovary (Fig. 5c–e). Long moniliform hairs, which are not seen in flower buds (Fig. 5i), occur abundantly from the inner side of the basal parts of the outer and inner tepals (Fig. 5e–g, j). They are composed of a few elongate cells (Fig. 5j).

Fig. 5

Anatomy and development of flowers of Lophiola aurea. a, i Longitudinal sections (LS) of a mature flower (a) and flower bud (i). bh Transverse sections (TS) of a flower bud (b) and mature flower (c–h), presented with the adaxial side above. ch TSs at levels marked ch in a. j LS of a mature flower, showing the moniliform hairs on adaxial side of tepals. br bract, bt bracteole, itl inner tepal, mh moniliform hairs, otl outer tepal, ov ovule, sg stigma, st stamen, sty style. Scale bars are 500 µm in c, 200 µm in a, b and i, and 100 µm in h and j. Scale bar in c applies to dg

The gynoecium is composed of three zones: a trilocular synascidiate zone (Fig. 5c) approximately at the lower one-third of the ovary, a unilocular symplicate zone (Fig. 5d–f) in the upper two-third of the ovary and in the lower part of the style, and the plicate zone (Fig. 5g) in the upper part of the style. In the unilocular zone, an adaxial edge of each septum forms a thick placenta, where many ovules develop (Fig. 5d, e). In the style, the three carpels are entirely free with free lateral margins, and their respective ventral margins are open to form a common stylar canal or an internal compitum (Fig. 5g, h).

Gynoecial development

During the early developmental stage, the ovary appears almost inferior (Fig. 5i). In a more or less mature flower bud, the upper one-fourth of the ovary is superior with the remaining three-fourths inferior. The difference in the ovary position between young and mature flower buds indicates that the ovary shifts its position from inferior to semi-inferior during development.

Carpel fusion in the ovary is congenital. If the structure of a young gynoecium prior to initiation of the ovule primordia in the ovary is pursued from the top downward using its transverse sections, we can see that the three constituting carpels are free only in the upper part of the style. There is no sign that the three carpels are initially free in the ovary.

Nietneria

Mature flowers

Flowers have a semi-inferior ovary immediately before anthesis, and have no perianth tube around the superior part of the ovary (Fig. 6a). The outer and inner tepals are free above the inferior part of the ovary.

Fig. 6

Anatomy of the flowers of Nietneria corymbosa. a Longitudinal section of a mature flower. be Transverse sections of a mature flower at levels marked be in a. f Magnified view of style in e. itl inner tepal, otl outer tepal, ov ovule, st stamen, sty style. Scale bars are 500 µm in ae and f, and 50 µm in d

The gynoecium is composed of a short synascidiate zone in the lower half of the ovary and a long symplicate zone in the remaining upper part. The ovary is unilocular in its upper half and trilocular in the lower half (Fig. 6b, c). Both the lower and upper parts of the style (Fig. 6d, e) are also unilocular. In the style, the three carpels are not fused at their lateral margins (Fig. 6d), and their respective ventral margins are open to form a common stylar canal and a compitum (Fig. 6f). If available, younger buds should have three separate carpels in the style. There are no septal nectaries throughout the ovary. No particular hairs are present on the filaments.

The development of the flowers was not investigated.

Narthecium

Mature flowers

Before anthesis, the flowers of Narthecium asiaticum appear more or less lanceolate in the longitudinal section (Fig. 7a). Median longitudinal sections of mature flowers indicate that the style is slightly recurved in the abaxial direction (Fig. 7a), indicating that the flowers are weakly monosymmetric. Unlike the flowers of the other genera, the flowers of Narthecium have an abaxial outer tepal and an abaxial carpel with a subtending bract on the abaxial side of the pedicel. The innermost tepal is present on the adaxial side. They have a nearly superior ovary, and no perianth tube around the superior part of the ovary (Fig. 7a–f). The stamens appear to be inserted almost at the same level as the free tepals (Fig. 7d). The microtome sections of the flowers show that the outer stamens are attached to the outer tepals, and the inner stamens to the ovary (Fig. 7d).

Fig. 7

Anatomy and development of the flowers of Narthecium asiaticum. a Longitudinal section (LS) of a mature flower, with the adaxial side on the right, obtained by sectioning through line a in d. bg Transverse sections (TS) of a mature flower at levels marked bg in a, presented with the adaxial side above. h LS of a mature flower, showing the moniliform hairs on filaments. i LS of a flower bud prior to ovule initiation. j LS of a flower bud with ovule primordia that are just initiated in an ovary locule. br bract, bt bracteole, itl inner tepal, mh moniliform hairs, otl outer tepal, ov ovule, sg stigma, st stamen, sty style. Scale bars are 500 µm in a and b, and 100 µm in gj. Scale bar in b applies to cf

The gynoecium is composed of trilocular synascidiate zone (Fig. 7b–d), trilocular symplicate (Fig. 7e), and unilocular symplicate (Fig. 7f, g) zones. The placenta and ovules are mainly present in the superior part of the synascidiate zone. In contrast to those of the four other genera, the three carpels of Narthecium are completely fused with the lateral margins in the style (Fig. 7b–g). Their respective ventral margins are open forming a common stylar canal or an internal compitum (Fig. 7f, g). There are no septal nectaries in the ovary. Moniliform hairs are abundant on the filaments, and each hair is composed of more than 10 small bead­like cells (Fig. 7h).

Gynoecial development

During the early stages of development, carpels are free at least on the adaxial side, and their future placental region is deeply embedded (Fig. 7i). In the gynoecium where the ovule primordia are initiated, the ovary appears semi-inferior with about one-third of the ovary embedded in the receptacle (Fig. 7j). This indicates that the ovary has shifted its position slightly upward from a semi-inferior to an almost superior position during development.

Irrespective of their developmental stages, the three carpels are completely fused with one another throughout the whole gynoecium. Even in young flower buds, a style is observed with a single canal in the center. The style is not composed of three separate carpels as observed in Lophiola, indicating that the carpel fusion in the ovary is congenital.

Discussion

Comparisons within Nartheciaceae, and evolution of floral characters

Extensive observations have confirmed diversity among the genera in the following nine characters: (1) the presence or absence of a perianth tube (free from the gynoecium); (2) the level of stamen insertion; (3) the mode of carpel fusion (i.e., postgenital or congenital); (4) the presence or absence of septal nectaries; (5) whether the style is trilocular or unilocular; (6) the presence or absence of fusion of the lateral margins of carpels in the style (i.e., symplicate or asymplicate); (7) the disposition of floral elements in relation to the inflorescence axis; (8) the presence or absence of moniliform hairs; and (9) whether flowers are polysymmetric or weakly monosymmetric. Their respective character states in Nartheciaceae and other Dioscoreales (as outgroup) are tabulated (Table 2), and the distribution of apomorphies of the nine characters is mapped on a phylogenetic tree (Fig. 8).

Table 2

Comparisons of nine floral charactrs in Nartheciaceae. Character state polarities were determined using Taccaceae and Dioscoreaceae as outgroup

Character

Metanarthecium

Aletris

Lophiola

Nietneria

Narthecium

Taccaceae/Dioscoreacea

1. Presence or absence of a perianth tube

Present (0)

Present (0)

Absent (1)

Absent (1)

Absent (1)

Present

2. Level of stamen insertion

On the perianth tube (0)

On the perianth tube (0)

At the base of tepal (1)

At the base of tepal (1)

At the base of tepal (1)

On the perianth tube

3. Mode of carpel fusion

Post-genital (0)

Post-genital (0)

Congenital (1)

Congenital (1)

Congenital (1)

?

4. Presence or absence of septal nectaries

Present (0)

Present (0)

Absent (1)

Absent (1)

Absent (1)

Present

5. Number of locules in the style

3 (0)

3 (0)

1 (1)

1 (1)

1 (1)

1

6. Fusion of the lateral carpellary margings in the style

Present (0)

Present (0)

Absent (1)

Absent (1)

Present (0)

?

7. Disposition of the median outer tepal in relation to the inflorescence axis

Adaxial (0)

Adaxial (0)

Adaxial (0)

Adaxial (0)

Abaxial (0)

Adaxial

8. Presence or absence of moniliform hairs

Absent (0)

Absent (0)

Present on inside of tepals (2)

Absent (0)

Present on filaments (1)

Absent

9. Symmetry

Polysymmetric (0)

Polysymmetric (0)

Polysymmetric (0)

Polysymmetric (0)

Weakly monosymmetric (1)

Polysymmetric

The data of Taccaceae and Dioscoreaceae are based on Dahlgren et al. (1985) and Stevens (2001 onward). Plesiomorphy is scored 0, and apomorphy 1. The numbers (1–9) that precede the characters correspond to the numbers appearing on the phylogenetic tree in Fig. 9

Fig. 8

Nartheciaceae tree, based on Fuse et al. (2012), showing the distribution of apomorphies in the nine floral characters. The nine characters (numbered 1–9) and character states are presented in Table 2. A black bar indicates a synapomorphy or autapomorphy, and a white bar indicates a reversal

In Metanarthecium and Aletris, a perianth tube is formed by the fusion of outer and inner tepals, where the outer and inner stamens are inserted. The presence of the perianth tube in Metanarthecium was already reported by Utech (1978) and Remizowa et al. (2008). However, in Lophiola, Nietneria and Narthecium, no perianth tube is formed (character 1) and the six stamens are inserted at the base of the free tepals (character 2). In addition, in Metanarthecium and Aletris the three carpels are fused postgenitally and form the septal nectaries, as reported by Remizowa et al. (2008) for Metanarthecium. In both Metanarthecium and Aletris, the gynoecium is trilocular throughout. The observations made in the flowers of Metanarthecium agreed with those of Remizowa et al. (2008), but did not coincide with the observations of Utech (1978), who reported a unilocular style. Although Remizowa et al. (2008) suggested that there might be intraspecific variation in M. luteo-viride, it seems likely that the drawings of the transverse sections of the Metanarthecium flowers by Utech (1978) were erroneous. Utech (1978) did not present micrographs to show the unilocular style in M. luteo-viride. On the other hand, in Lophiola, Nietneria and Narthecium the three carpels are fused congenitally (character 3) and do not form (or lost) the septal nectaries (character 4), and the style is unilocular (character 5). The fusion of carpellary lateral margins in the style is observed in Metanarthecium and Aletris. Loss of this feature is basal for the Lophiola, Nietneria and Narthecium clade, where the styles of most taxa have unfused lateral carpellary margins. However, in Narthecium, fusion of lateral margins reoccurs as a reversal (character 6).

As for the disposition of floral elements, all the genera, except for Narthecium, exhibited the median outer tepal on the adaxial side. In Narthecium, the median outer tepal is positioned on the abaxial side (character 7). Narthecium further differs from the four other genera in having weakly monosymmetric flowers (character 8). This monosymmetry is represented by the pistil that is slightly recurved in the abaxial direction. The moniliform hairs are formed on the inner side of the perianth tube (Lophiola) and filaments (Narthecium) (character 9).

Based on the aforementioned comparisons among the five genera of Nartheciaceae, three floral diagrams are obtained (Fig. 9). The first is the floral diagram of Metanarthecium and Aletris (Fig. 9a); the second is that of Lophiola and Nietneria (Fig. 9b), and the third is that of Narthecium (Fig. 9c). The loss of the perianth tube (Fig. 9b, c), as well as of the septal nectaries (Fig. 8), in the clade of Lophiola, Nietneria and Narthecium apparently reflects a change in pollinators; the evolutionary loss of septal nectaries indicating a change in the reward offered by the flowers to the pollinators from nectar (Metanarthecium and Aletris) to pollen (Lophiola, Nietneria and Narthecium). The formation of the moniliform hairs inside the perianth in Lophipla or on the filaments in Narthecium, and the weak monosymmetry of flowers (Narthecium) suggest that the flowers of Nartheciaceae have evolved in close association with pollination. The flowers of Narthecium asiaticum are known to be pollinated mainly by the shyrphid flies that collect pollen grains (Ishii and Sakai 2001). Furthermore, the change in the disposition of floral elements in Narthecium, where the median outer tepal is positioned on the abaxial side (Fig. 9c), might be associated with the monosymmetry, thus with pollination.

Fig. 9

Floral diagrams of Nartheciaceae. a Aletris and Metanarthecium. b Nietneria and Lophiola. c Narthecium. Note the differences among the three diagrams in the presence or absence of a perianth tube, the level of stamen insertion, the presence or absence of fusion of the lateral margins of carpels, and the disposition of floral elements in relation to the inflorescence axis

Since Metanarthecium was published as a new genus in Melanthiaceae (Maximowicz 1867), there has been controversy as to whether Metanarthecium should be placed within Aletris (for reviews see Hara 1967; Merckx et al. 2008, and literature cited therein). Hara (1967) compared the floral morphology of Metanarthecium and Aletris, concluding that no essential differences exist between the two genera, thus treating M. luteo-virde as “A. luteo-viridis” (Maxim.) Franchet. Recent molecular analyses indicate that M. luteo-virde is nested within the clade of Aletris (Caddick et al. 2002; Merckx et al. 2008), while Fuse and Tamura (2000) and Fuse et al. (2012) supported the distinctness of Metanarthecium from Aletris. Metanarthecium is sister to the rest of Nartheciaceae (Fig. 9). However, in the present study no synapomorphies were found for the clade of Aletris, Lophiola, Nietneria, and Narthecium. Thus, finding a synapomorphy for Aletris, Lophiola, Nietneria, and Nartheciuman is still an unresolved subject. Likewise, a synapomorphy is also uncertain for a clade of Nietneria and Narthecium.

Evolution of ovary position

Ovary position was one of the floral characters that was highlighted in the present study, because it has been described variously for the genera of Nartheciaceae as explained in the Introduction. The observations confirmed that the position of the ovary is highly diverse within the family. The ovaries can be almost superior (Metanarthecium and Narthecium), semi-inferior (Aletris foliata, Lophiola, and Nietneria) and inferior (A. spicata). However, earlier stages of flower development of Metanarthecium, Narthecium and A. foliata show an inferior placed ovary that shifts its position during ontogeny. Even at the mature stages of Metanarthecium and Narthecium, short inferior ovary-parts can be recognized. These facts indicate that, like the other Dioscoreales, Nartheciaceae originally had an inferior ovary as a plesiomorphy. However, during the evolution of the family, the ovary shifted its position from inferior to semi-inferior (Aletris foliata, Nietneria, and Lophiola) or almost superior (Metanarthecium, Narthecium). Remizowa et al. (2008) also suggested the possibility that “the almost completely superior ovary position in Metanarthecium is a secondary condition”.

Such an evolutionary change from inferior to semi-inferior or almost superior ovary position is probably associated with the change in seed dispersal pattern, because it raises the position of the capsule which loculicidally dehisces to disperse seeds at maturity (for capsule dehiscence modes see Tamura 1998). Therefore, during seed dispersal, nearly the whole fruit is exposed to the air in both Metanarthecium and Narthecium; half or more of the fruit is exposed to the air in Aletris foliata, Lophiola, and Nietneria; and only the top of the fruit is exposed to the air in A. spicata. Our preliminary observations show that in Metanarthecium and Narthecium the seeds are dispersed almost simultaneously from the whole fruit, whereas in A. spicata they are dispersed little by little only from the top of the fruit. In A. foliata, Lophiola, and Nietneria, the seeds will be dispersed in an intermediate proportion of effect between the seeds of Metanarthecium/Narthecium and those of A. foliata/Lophiola/Nietneria. The idea that the evolutionary change of ovary position from inferior to superior occurred in association with seed dispersal in Nartheciaceae may contradict the fact that some other families such as Alstroemeriaceae (Bayer 1998) and Iridaceae (Goldblatt et al. 1998) have genera with perfectly functional pseudo-luculicidal capsules derived from inferior ovaries. However, in Nartheciaceae the fruit wall derived from the superior ovary-part is much thinner in thickness than a pseudo-fruit wall derived from the inferior ovary-part, allowing easier wall dehiscence.

Once the inferior ovary position in Nartheciaceae is established to be a plesiomorphy, then we can look at the evolution of ovary position in the whole monocots in better shape than before. Evolution of ovary position in monocots has been discussed by Rudall (2002), Soltis et al. (2006), and Endress (2011). Rudall (2002) and Soltis et al. (2006) regarded the ovaries of Nartheciaceae to be equivocal, while Endress (2011) rather treated the ovaries of the whole Dioscoreales to be inferior and showed that inferior ovaries occurred as homoplasies in a few monocot orders including Dioscoreales. If the ovaries of Nartheciaceae are regarded as inferior, it provides a clear evolutionary scenario of ovary position in monocots (Fig. 10).

Fig. 10

Evolution of ovary position in monocots. An arrow indicates a major evolutionary change in the ovary position from superior to inferior that occurred in a clade leading to Dioscoreales/Pandanales, Liliales, and Asparagales, with reversals within each order. An arrowhead indicates another major evolutionary change in the ovary position from superior to inferior in Zingiberales

A major evolutionary change of the ovary position from superior to inferior occurs in a clade of Dioscoreales/Pandanales (Vellozialceae, Stemonaceae, etc.) and within several groups of Liliales (Alstroemeriaceae, Campynemataceae, Corsiaceae, etc.) and Asparagales (Orchidaceae, Iridaceae, etc.) (see arrow in Fig. 10). Reversals in the ovary position from inferior to superior occur not only within every order, that is, Dioscoreales (Nartheciaceae), Pandanales, Liliales, and Asparagales, but also in a clade of Arecales (Arecaceae and Dasypogonaceae), Poales (Typhaceae, Poaceae, etc.), and Commelinales (Commelinaceae, Pontederiaceae, etc.). The change in ovary position from superior to inferior occurs again in a clade of Zingiberales (Musaceae, Zingiberaceae, etc.) (see arrowhead in Fig. 10).

This evolutionary scenario might raise questions in some families and orders. For instance, Melanthiaceae have the superior ovary as a reversal from an inferior ovary (Fig. 10). In some members of Melanthiaceae (e.g. Veratrum), the superior ovary is composed of shortly fused carpels (nearly apocarpous). This was used as one of the bases to consider that Melanthiaceae (Melanthioideae in Liliaceae sensu Melchior 1964) are morphologically primitive among the monocots (e.g. Thorne 1992). Melanthiaceae and some other families in the orders, where both superior and inferior ovaries are known to occur, need future developmental studies to confirm an ancestral ovary position. Indeed, in the case of Haemodoraceae (Commelinales) which have both superior and inferior ovaries (Fig. 10), floral developmental studies provide evidence for reversals in ovary position from inferior to superior (Simpson 1998).

Thus, in most of the major groups (orders), the evolution in the ovary position from superior to inferior or reversals from inferior to superior are found. In other words, flowers have evolved in association with pollen vectors (Endress 2011) and possibly also with seed dispersal, as in Nartheciaceae.

Evolution of septal nectaries

The presence of septal nectaries is one of characteristic features of monocots. Their morphology, distribution and evolution have been discussed often (e.g. Endress 2011; Rudall 2002; Smets et al. 2000). In the present study, it was confirmed that, like Metanarthecium, Aletris exhibits postgenital carpel fusion and has septal nectaries. In both Metanarthecium and Aletris the three carpels were separate (free) during the early stage of development. These observations support the conclusion of van Heel (1988) that the occurrence of septal nectaries is associated with free or partly free carpels. The basal distribution of the septal nectaries in the phylogenetic tree of Nartheciaceae suggests that their presence is a plesiomorphy in Nartheciaceae. Since septal nectaries are known to be present in other Dioscoreales (Burmanniaceae, Dioscoreaceae, and Taccaceae) (Dahlgren et al. 1985), their presence is a plesiomorphy of Dioscoreales (Fig. 11).

Fig. 11

Evolution of septal netaries in monocots. Note that septal nectaries evolved early in monocot evolution (arrow); however, they were lost due to the changes in the pollination pattern (arrowheads)

Although it is equivocal whether the presence of septal nectaries is a plesiomorphy or apomorphy in Alismatales, where some families, such as Tofieldiaceae and Alismataceae, have septal nectaries, while others, such as Scheuchzeriaceae and Aponogetonaceae, do not have them, it seems that septal nectaries appeared early in the monocot evolution. Remizowa et al. (2010) stated that “A possible explanation of the fact that postgenital fusion is always present in gynoecia with septal nectaries is that septal nectaries evolved only once, and their correlation with postgenital fusion in extant monocots is inherited from their common ancestor.” However, it is unclear from where the septal nectaries first evolved, whether it is from a clade leading to the whole monocots or from a basal clade except Acoraceae (see arrow in Fig. 11). In most studies Acoraceae are sister to all other monocots (e.g. Chase et al. 2000; Duvall et al. 1993; Hertweck et al. 2015; Soltis et al. 2007), whereas in some studies Acoraceae are often combined with Alismatales (e.g., Davis et al. 2006; Petersen et al. 2015; Stevenson et al. 2000) (for more information see Stevens 2001 onwards). Considering their unique development as well as their distribution throughout monocots, the presence of septal nectaries can be viewed as one of key innovations in the origin of the entire monocots. This hypothesis agrees with that of Remizowa et al. (2010) that “the ancestral monocot conditions were postgenital fusion between carpels and presence of septal nectaries.” Due to the changes in the mode of pollination, septal nectaries are now lost not only in Acoraceae/Alismatales pro parte but also in Liliales and most of Poales. Alismatalean families lacking septal nectaries are aquatic and water-pollinated; lilialean families lacking septal nectaries alternatively have nectaries on the perianth bases; and poalean families lacking septal nectaries are anemophilous (for details in individual families see Endress 1995).

In addition to being lost in major monocot groups, septal nectaries are lost even within small families such as Nartheciaceae probably due to the change in pollinators. The presence or absence of the septal nectaries, combined with the aforementioned evolutionary change in the ovary position, shows how individual monocot families and orders have evolved and are characterized in terms of pollination and seed dispersal patterns.

Notes

Acknowledgements

The study was supported by a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science (No. 16H05763, 17K07530).

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Copyright information

© The Botanical Society of Japan and Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  • Hiroshi Tobe
    • 1
  • Yu-Ling Huang
    • 1
    • 2
  • Tomoki Kadokawa
    • 1
  • Minoru N. Tamura
    • 1
  1. 1.Department of Botany, Graduate School of ScienceKyoto UniversityKyotoJapan
  2. 2.National Museum of Natural ScienceTaichungTaiwan

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