Printer Friendly

Sieve-element plastids and evolution of monocotyledons, with emphasis on melanthiaceae sensu lato and Aristolochiaceae-Asaroideae, a putative dicotyledon sister group.

II. Introduction

The origin and evolution of monocotyledons has been a subject to which systematists have given increased attention at least since Engler's 1892 treatise. Although Engler's classification and family concepts partly survived through the next century (e.g., Cronquist, 1981, 1988), the position of monocotyledons preceding dicotyledons was early on questioned and in phylogenetic concepts replaced by their ranalean ancestry (Bessey, 1893; Hallier, 1905).

An intensified study of an increasingly greater number of angiosperms and of novel, in part rather sophisticated, features, which commenced in the second half of the last century, revealed several character states present in both monocotyledons and Annonaceae, Aristolochiaceae, Piperaceae, and other dicotyledon families belonging to the ranalean complex. This punctual harmony led Huber (1977) to propose a single natural unit for monocotyledons and basic Ranales (in 1982 and 1991 expanded to include Caryophyllales, but see Dahlgren & Bremer, 1985) and to separate them from the main body of dicotyledons.

At the family level and above, the results from the new characters combined with the main body of morphological and anatomical details, their cladistic compilation, and phylogenetic estimation (Dahlgren & Rasmussen, 1983), resulted in the new monocotyledon classification by Dahlgren et al. (1985) and definitely marked the end of the Englerian influence, most clearly visible in the fragmentation of Liliaceae s.l. (proposed by Huber, 1969).

Intimately connected with the efforts toward a phylogenetic classification were attempts to identify the putatively most basal monocotyledon. While Dahlgren et al. (1985) and Dahlgren and Bremer (1985) favored Dioscoreales (see also Huber, 1969), new studies by Tillich (1985), Grayum (1987), and Duvall et al. (1 993a) pushed Acorus into this position. Duvall et al. (1993a, 1993b) were the first to apply molecular data to the phylogeny of monocotyledons, and, together with new morphological studies, their data proved to be the nucleus of the renewed interest and active research in monocotyledons, impressively documented by the proceedings of the Kew and Sydney conferences (Rudall et al., 1995; Wilson & Morrison, 2000).

As a result of more intensive sampling and analysis of a larger data set, both in molecular and combined molecular-morphological studies, additional groups, most prominently Tofieldiaceae, Araceae, and other families of Alismatales sensu Angiosperm Phylogeny Group (APG, 1998), came into focus as comparatively basal taxa and separated as the next clade (after Acorus) from the remainder of monocots (Chase et al., 1995a, 1995b; Savolainen et al. 2000). Tofieldia was first named by Walker (1986) as being among the most primitive extant monocotyledons, together with Narthecium (both are former members of Melanthiaceae s.l.), Acoraceae, Scheuchzeriaceae, and Butomaceae.

The sieve-element plastids of monocotyledons, early on found to be very distinct from those of dicotyledons (Behnke, 1972) and later classified as subtype P2 (Behnke, 1981a), are characterized by cuneate protein crystals detected with the transmission electron microscope in all species studied. The two aristolochiid genera Asarum and Saruma are the only dicotyledon taxa to also contain cuneate crystals (Behnke, 1971, 1988); however, no particular monocotyledon taxon could be named as their putative link.

When, for a comprehensive survey of the distribution of monocotyledon sieve-element plastids (Behnke, 2000), the number of investigated species was raised to (now) more than 750, representing all families and most of its segregates, some were found to contain 1) polygonal, orthogonal, or other crystals in addition to cuneate crystals and/or 2) less-distinct, angular crystals instead of the cuneate ones. The most typical example of the latter configuration are Velloziaceae (Behnke et al., 2000), while a number of diverse taxa, among them Tofieldiaceae, have plastids with the one or another, additional crystal shape.

In the present study the sieve-element plastids of putative basal taxa of monocotyledons and their (formerly) related families are described and compared with those of Asarum, Saruma, and other basal dicotyledons.

III. Material and Methods

Living material is a prerequisite for fixation of sieve elements and the eventual investigation of their plastids with the transmission electron microscope. Therefore, the majority of species were prepared for fixation by the author in botanical gardens, while other samples were air mailed to me within a few days under special care for further processing at Heidelberg (see Table I). Whenever possible, sieve-element plastid vouchers containing a sample of the specimen used, an electron micrograph of its typical plastid, and an embedded block of the respective fixation were prepared and placed in TEX.

Stem material (vegetative or generative), petioles, or leaf veins were selected, cut with a razor blade into thin, longitudinal sections, and immediately immersed in the fixation mixture. Fixation was for three or more hours at room temperature in a sodium cacodylate--buffered solution containing 4% formaldehyde and 5% glutaraldehyde adjusted to pH 7.2. Postfixation in buffered 1% 0504, stepwise dehydration with acetone, and embedding and polymerization in epon-araldite or low-viscosity epoxy mixtures were according to standard procedures. Semithin sections were cut from embedded material and inspected for phloem parts, before ultrathin sections were cut with a diamond knife using a Reichert Ultracut microtome and subsequently stained with aqueous uranyl acetate and lead citrate. Sections were viewed and photographed with Philips CM 10 and Philips EM 400 transmission electron microscopes at 100 kV.

IV. Results


Cuneate protein crystals are the synapomorphic feature of all monocot sieve-element plastids (subtype P2) and are present solely or in addition to other crystals and/or starch grains and! or protein filaments (Fig. 1, upper part); rarely are they replaced by angular crystals (e.g., subform [] in Velloziaceae; see Fig. 46) or entirely lost (form Ss, with Pistia, Araceae, as the only example). If present in dicotyledon sieve-element plastids, protein crystals have different shapes (e.g., globular, polygonal, rectangular), but the majority of taxa have only starch (S-type plastids; see Behnke, 1981 b). In basal dicotyledons (Fig. 1, lower part), starch grains are present in almost all sieve-element plastids, either exclusively (form Ss) or, equally often, together with polygonal crystals (form P1 cs) and, less frequently, with protein crystals and filaments (form Plcfs).

I. Sieve-Element Plastids of Basal Dicotyledons

The sieve-element plastids of Amborella (Fig. 2) and all the other basal angiosperms in the ANITA grade (sensu Qiu et al., 2000) of Chloranthaceae and Ceratophyllum (Fig. 3) are S-type, containing starch only. P-type plastids of different forms prevail in the other eumagnoliid orders; namely, Laurales, Magnoliales, and Piperales (see Behnke, 1988).

a. Piperales

Lactoris (Fig. 4) and the species studied in Piperaceae and Saururaceae contain S-type sieve-element plastids; most species of Aristolochiaceae, P-type. In Aristolochia, Holostylis, Isotrema, and Pararistolochia, form Plcs (Fig. 6) or form Plcfs plastids are most common, whereas in Thottea, S-type plastids prevail. The sieve-element plastids of Aristolochia clematitis (Fig. 5), of two more Aristolochia species, and of Asaroideae are distinguishable from all other members in the order by their lack of starch.

b. Asarum and Saruma

The sieve-element plastids of the two asaroid genera (7 species studied; see Table I) were comparatively early shown to contain cuneate crystals (Behnke, 1971), but only now, with the enormous amount of plastid data available, can an explanation of their ontogeny, together with arguments supporting their position between dicotyledon and monocotyledon forms, be offered.

With their single, large polygonal and many cuneate crystals, subform [PI/2c.sub.cp] plastids Asarurn (Fig. 9) and Saruma (Fig. 10) display typical character states of both basal dicotyledon and monocotyledon sieve-element plastids. An ontogenetic study of phloem in Saruma, comparing differentiating and mature sieve elements (Fig. 7), repeatedly disclosed sieve-element plastids at a very early stage of differentiation (Fig. 7, arrows). Their shape is still amoeboid; i.e., they have not yet reached their final globular outline. Each plastid contains one large polygonal crystal (Fig. 8); cuneate crystals are still missing. This picture is almost identical to those found in young sieve elements of Aristolochia clematitis (Behnke, 1988; Fig. 1), but whereas sieve-element plastids of Saruma continue their development to subform [p1/2c.sub.cp]' showing then polygonal and cuneate crystals (Fig. 10), those of A. clematitis stay as subform [p1/2c.sub.p] (Fig. 5).


1. Acorus

Acorus calamus (Fig. 19) and A. gramineus (Fig. 20) have sieve-element plastids with only cuneate crystals--i.e., subform [P2c.sub.c] plastids--as do about 80% of the extant monocotyledons (Behnke, 2000). Sizes and number of crystals differ between the two species, but no other inclusions were detected (some 50 plastids were screened).

2. Japonoliriaceae and Tofleldiaceae

The sieve-element plastids of Japonolirion osense match those of Asarurn and Saruma, in both size and composition: they contain a dense polygonal and several equally dense cuneate crystals (Fig. 11), the two criteria that define subform [p1/2c.sub.cp] plastids. In Japonolirion, crystals seem to be larger and more closely centered (compare Figs. 9 and 10 with Fig. 11), but surveying the more than 300 plastids documented from the three genera, their similarity is striking.

Our studies in Tofieldiaceae (7 specimens from 6 species; see Table I) revealed subform [P1/2c.sub.cp] sieve-element plastids identical to those of Japonolirion (Figs. 12-16). Although not always stained as dark, the polygonal crystal is composed of nearly as tightly packed subunits (Fig. 14) as depicted earlier for cuneate crystals (Behnke, 1971) and is clearly distinct from the wider spacing in the small crystals of Narthecium (see Fig. 28).

3. Araceae and Traditional Alismatales

With a few exceptions, Araceae contain very large subform [P2c.sub.c]S plastids (Figs. 23, 24); the numbers and sizes of their cuneate crystals and starch grains vary considerably in the family (see Behnke, 1995). Opposed to this, all families traditionally included in Alismales are pure subform [P2c.sub.c] taxa. Their plastids are much larger (Fig. 21: Potamogeton; Fig. 22: Alisma) but have the same characters as found in Acorus.


1. Triuridaceae and Pandanales

In Pandanales as circumscribed by Chase et al. (2000) subform [P2c.sub.c] and subform [P2c.sub.c]f plastids prevail, but nearly all Velloziaceae differ by including in their sieve-element plastids small, angular crystals instead of cuneate ones (Fig. 46; cf. Behnke et al., 2000). The subform [P2c.sub.a-c] plastids of Sciaphila purpurea (Triuridaceae) also contain angular crystals in both young (Fig. 17) and mature sieve elements (Fig. 18), with rarely a few cuneate ones in addition.

2. Nartheciaceae, Burmanniaceae, and Dioscoreales

Subform [P2c.sub.c] sieve-element plastids are present in almost all families belonging to Dioscoreales (Figs. 25-31), with only some Dioscorea species having subform [P2c.sub.c]s. This also includes the investigated species of Burmanniaceae (Fig. 31) and Nartheciaceae (Figs. 26, 27), two families only recently incorporated into the order, but exempts Narthecium. The sieve-element plastids of Narthecium ossifragum contain cuneate crystals, as do all other taxa in the order, but also a number of smaller, not uniformly shaped crystals with a wider spacing of subunits (Figs. 28, 29). Sieve-element plastids with this combination of crystals are assigned to subform [P2c.sub.el] and known from Poales (Fig. 32), Bromeliaceae and other taxa (see Behnke, 2000; Behnke et al., 2000).


The 15 species investigated in the newly defined family (now including Trilliaceae; Rudall et al., 2000) have subform [P2c.sub.c] sieve-element plastids with comparatively large, cuneate crystals (Figs. 33-41), the only exception being Veratrum formosanum, which has an additional, nearly orthogonal crystal (Fig. 37). However, neither V. formosanum nor any of the species investigated (see Table I) contain large, polygonal or small, loosely packed crystals, as found in Tofieldiaceae and Narthecium, respectively. Also the size of sieve-element plastids is significantly larger in Melanthiaceae s.str. than in Tofieldiaceae and Nartheciaceae.


For about 10% of the more than 750 monocotyledons investigated for sieve-element plastids, results were obtained from at least two different specimens. Among these we found only three species--Acanthochlamys bracteata (Fig. 43), Barbaceniopsis vargasiana (Figs. 44, 46), and a not-further-determined Dioscorea from Ethiopia (Figs. 42, 45)--in which the plastids of the different samples did not match each other. In one specimen the sieve-element plastids contained cuneate, respectively angular crystals and conformed to the (sub-)form generally recorded in the genus or family; those of the other had only a single large, polygonal crystal.

The situation in Dioscorea sp. is of additional interest. In the one sample, and in other Dioscorea species investigated, the plastids of anastomosal sieve elements located in the node of stems are distinguished by cuneate crystals that are much smaller than those of all other sieve elements: see figure 8.16 in Behnke (1990), taken from the same plant (then named D. cf. ethiopica). In the other specimen there is no structural difference between sieve-element plastids in nodal (Fig. 42) and internodal (Fig. 45) phloem; that is, the average size of the lone polygonal crystal is the same in all sieve elements.

V. Discussion

The heterogeneity of the sieve-element plastids recorded in the Melanthiaceae s.l. confirms the dismemberment of the family into several different taxa, as previously proposed according to results obtained with morphological and molecular characters and their singular or combined cladistic analysis (e.g., Ambrose, 1980; Chase et al., 1993, 1995a, 1995b; Goldblatt, 1995; Zomlefer, 1999; Fuse & Tamura, 2000).

Japonofirion osense, the latest addition to the former Melanthiaceae s.l., is singular in its form P1/2[c.sub.cp] plastids, which, among all angiosperms, match only and are hardly distinguishable from those of Asarum and Saruma. The second closest are Tofieldiaceae, which also contain P1/2[c.sub.cp] plastids, but with their polygonal crystals often stained less dark as a result of slightly wider spacing of the subunits. Subform P2[] sieve-element plastids of Narthecium ossifragum (Nartheciaceae s.str.), with cuneate and small, loosely packed crystals, may be interpreted as 1) bridging subform P2[c.sub.cp] of Tofieldiaceae to subform P2[c.sub.c] plastids found in Aletris and other Nartheciaceae, in Melanthiaceae s.str. and most monocotyledon families, or 2) leading up to members of Asparagales and Poales with the same subform P2[].

Nakai (1930), who first described Japonolirion, included the new genus in the tribe Helonieae (Melanthiaceae), but, after a detailed study of its floral vascular anatomy, Utech (1984) transferred it to Tofieldieae. Tamura (1998) treats Japonolirion as a monotypic tribe placed together with Tofieldieae and Petrosavieae in the subfamily Tofieldioideae, which he combines with Narthecioideae in his Nartheciaceae. Takhtajan (1997) raised Japonolirion to family status and includes it with Tofieldiaceae, Nartheciaceae, Xerophyllaceae, and more families split from Melanthiaceae in his Melanthiales.

Phylogenetic trees using DNA data to demonstrate relationships among angiosperms 1) support Japonolirion (together with Petrosavia, now treated as Petrosaviaceae) in a dade branching after Acorus and after Alismatales sensu APG (1998) as sister to the main body of monocotyledons, 2) include Tofieldiaceae, together with Araceae in the latter, second-most basal dade ofmonocotyledons, and 3) associate Nartheciaceac s.str. with Dioscoreales branching next after Petrosaviaceae (Chase et aL, 1995a, 2000; Kubitzki et al., 1998; Caddick et aL, 2000; Savolainen et aL, 2000; Soltis et al., 2000).

Ultrastructural characters of angiosperm sieve-element plastids (Behnke, 1988, 1991,2000) suggest a slightly different evolution of the monocotyledons: The probably most basal angiosperms (Qiu et al., 2000), the ANITA grade (Amborellaceae, Nymphaeales, Austrobaileyaceae, Trimeniaceae, and Illiciales) plus Chloranthaceae and Ceratophyllaceae, exclusively contain S-type plastids. In angiosperms (for gymnosperms, see Behnke, 1974), P-type plastids first appear in eumagnoliids (Winterales, Piperales, Magnoliales, Laurales), where, with the exception of Himantandraceae, Lactoridaceae, Piperaceae, and Saururacene, one or several different forms (Plc, Pics, Plcfs, Plfs) are found in at least some species (Behnke, 1988). Aristolochiaceae, the only family of Piperales with P-type plastids, is of special interest, because it is also the single known eumagnoliid taxon that contains species with form Plc plastids; i.e., missing additional starch grains. The loss of starch in sieve-element plastids of some paleoherbs is h eld to be a prerequisite for the development of the monocotyledon subtype P2, which, in only a minority of taxa, has starch-containing forms (P2cs, P2cfs), most likely acquired secondarily. Of the two subforms--P1/2[c.sub.p] in a few Aristolochia species, and P1/2[c.sub.cp] in Asarum and Saruma--the latter shares characters of both eumagnoliids and monocotyledons (see Fig. 1, P1/2c).

Our ontogenetic studies have documented that, in sieve-element plastids of Saruma, the first inclusion to appear is a large, polygonal crystal, followed subsequently by cuneate crystals. This suggests the addition of the typical monocot crystals rather than a partial particulation of the polygonal one. Also in favor are previous ontogenetic studies of form P2c sieve-element plastids, which clearly demonstrated the formation of cuneate crystals, not preceded by any large crystal (e.g., Behnke, 1981a). Consequently, P1/2[c.sub.cp] plastids of Japonolirion would have retained the polygonal crystal, while all other monocotyledons had lost it; e.g., through steps of gradual disintegration and as putatively initiated in Tofieldiaceae. Monocotyledon sieveelement plastids that lack cuneate crystals but contain a single polygonal one instead, found so far in mutations of three taxa, are in turn explained as the result of a complex genetic block that retains the polygonal crystal as their eumagnoliid ancestry and repre sses the formation of their monocotytedon identity (cuneate crystals).

Therefore, summarizing the structural evidence from sieve-element plastids, Japonolirion and the Tofieldiaceae are identified as basal monocotyledons that share a common ancestry with aristolochiid eumagnoliids. In phylogenetic studies based on molecular data, and using Acorus as the most basal monocotyledon, a single dicotyledon sister group of the monocotyledons has so far not been found, but Aristolochiaceae is among the candidates (see e.g., Duvall, 2000).
Table I

Forms of sieve-element plastids and origin of investigated species

 Forms of Plant
 sieve-element parts
Investigated taxa (a) plastids (b) used (c)

 Amborella trichopoda Bail. Ss S

 Ceratophyllum demersum L. Ss S
 Aristolochia clematitis L. P1/[2c.sub.p] S
 Aristolochia ringens Vaht non [P1c.sub.p]s S
 Link & Otto
 Asarum arifolium Michx. P1/[2c.sub.cp] S
 Asarum canadense L. P1/[2c.sub.cp] P
 Asarum caudatum Lindl. P1/[2c.sub.cp] P
 Asarum chingchengense. C.Y. P1/[2c.sub.cp] S
 Cheng & C.S. Yang
 Asarum europaeum L. P1/[2c.sub.cp] P
 Asarum shuttleworthii Britten P1/[2c.sub.cp] S, P
 & Baker f.

 Saruma henryi Oliv. P1/[2c.sub.cp] S, P
 Lactoris fernandezianus Phil. Ss S

 Japonolirion osense Nakai P1/[2c.sub.cp] B, S, V

 Acorus Calamus L. [P2c.sub.c] V
 Acorus gramineus Ait. [P2c.sub.c] V
 Alisma plantago-aquatica L. [P2c.sub.c] S
 Gymnostachys anceps R. Br. [P2c.sub.s] S, V
 Spathiphyllum wallisii Regel [P2c.sub.s] P
 Potamogeton natans L. [P2c.sub.c] S
 Harperocallis flava McDaniel P1/[2c.sub.p] V

 Pleea tenuifolia Michx. P1/[2c.sub.cp] S, V

 Pleea tenuifolia Michx. P1/[2c.sub.cp] V

 Tofieldia calyculata (L.) Wah- P1/[2c.sub.cp] B
 Tofieldia coccinea Richards P1/[2c.sub.cp] V
 Tofieldia pusilla (Michx.) Pers. P1/[2c.sub.cp] B, V
 Tofieldia racemosa (Walter) P1/[2c.sub.cp] S, V
 Britton, Stems & Poggenb.

 Burmannia madagascariensis [P2c.sub.c] B
 Burmannia wallichii Hook. f. [P2c.sub.c] S

 Dioscorca batatas Decne. [P2c.sub.cp.sup.c] S
 Dioscorea oppositifolia L. [P2c.sub.c] S
 Dioscorea sp. [P2c.sub.c] S
 Dioscorea sp. P1/[2c.sub.p] S
 Aletris glabra Bur. & Franch. [P2c.sub.c] V
 Lophiola americana (Pursh) [P2c.sub.c] B, V

 Narthecium assifragum (L.) [P2c.sub.d] B
Melanthiaceae s.str.
 Chamaelirium luteum (L.) Gray [P2c.sub.c] S

 Chinographis japonica Maxim [P2c.sub.c] V
 Helonias bullata L. [P2c.sub.c] V
 Heloniopsis orientalis (Thunb.) [P2c.sub.c] B, V
 Paris quadrifolia [P2c.sub.c] S
 Stenanthium gramineum (Ker.- [P2c.sub.c] V
 Gawl.) Morong
 Trillium cernuum L. [P2c.sub.c] S
 Trillium grandiflorum (Michx.) [P2c.sub.c] S
 Trillium sessile L. [P2c.sub.c] S
 Veratrum album L. [P2c.sub.c] S
 Veratrum formosanum Loes. [] V
 Veratrum nigrum L. [P2c.sub.c] V
 Xerophyllum temax (Pursh) Nutt. [P2c.sub.c] V

 Zigadenus elegans Pursh [P2c.sub.c] B, V
 Zigadenus glaberrimus Michx. [P2c.sub.c] V
 Sciaphila purpurea Benth. [P2c.sub.a-c] S

 Barbaceniopsis vargasiana P1/[] S, V
 (L. B. Sm.) L. B. Sm.
 Barbaceniopsis vargasiana [] S, V
 (L. B. Sm.) L. B. Sm.
 Acanthochlamys bracteata [P2c.sub.c] S, V
 P. C. Kao

 Acanthachlamys bracteata P1/[2c.sub.p] S, V
 P. C. Kao

 Hygroryza aristata (Retz.) Nees [] S, V
 ex Wight & Arn.

Investigated taxa (a) Origin of material (d)

 Amborella trichopoda Bail. Steep, forested slope leading
 to the Plateau de Dogny, near
 Sanamea, NEW CALEDONIA; leg.
 G. McPherson 2357
 Ceratophyllum demersum L. BG-BONN
 Aristolochia clematitis L. BG-HEID
 Aristolochia ringens Vaht non BG-HEID
 Link & Otto
 Asarum arifolium Michx. BG-MJG
 Asarum canadense L. BG-BONN
 Asarum caudatum Lindl. BG-BONN
 Asarum chingchengense. C.Y. BG-HEID
 Cheng & C.S. Yang
 Asarum europaeum L. BG-BONN
 Asarum shuttleworthii Britten Garden grown at Piccadilly Farm,
 & Baker f. Oconee Co., GA; originally
 collected near Fort Payne, De Kalb
 Co., AL; S. B. Jones 24970
 Saruma henryi Oliv. BG-HEID
 Lactoris fernandezianus Phil. Maratierra, Juan Fernandez Is.,
 CHILE; leg. Stuessy, Matthei,
 Sanders & Valdebenitos 5425
 Japonolirion osense Nakai Teshio Region Exper. Forest, Prov.
 Rumoi, Hokkaido, JAPAN; leg.
 M. N. Tamura
 Acorus Calamus L. BG-HEID
 Acorus gramineus Ait. BG-HEID
 Alisma plantago-aquatica L. BG-HEID
 Gymnostachys anceps R. Br. BG-M
 Spathiphyllum wallisii Regel BG-HEID
 Potamogeton natans L. BG-HEID
 Harperocallis flava McDaniel Apakachicola National Forest,
 Liberty Co., FL; leg.
 A. F. Johnson sent by L.G. Chafin
 Pleea tenuifolia Michx. Onslow co., Nc, U.S.A.; leg B. A.
 Pleea tenuifolia Michx. New Home Bogs, Eglin Air Force
 Base, Walton Co., FL; leg. L. G.
 Tofieldia calyculata (L.) Wah- BG-MJG
 Tofieldia coccinea Richards BG-E 19310065
 Tofieldia pusilla (Michx.) Pers. BG-K
 Tofieldia racemosa (Walter) New Home Bogs, Eglin Air Force
 Britton, Stems & Poggenb. Base, Walton Co., FL; leg. L. G.
 Burmannia madagascariensis Mount Niangbo, IVORY COAST;
 Mart. leg. S. Porembski 3841
 Burmannia wallichii Hook. f. Tai Po Kau Natural Reserve, HONG
 KONG; leg. D. X. Zhang, sent by
 R. Saunders
 Dioscorca batatas Decne. 80-BONN
 Dioscorea oppositifolia L. BG-HEID
 Dioscorea sp. BG-HEID ex BG-L
 Dioscorea sp. BG-HEID ex BG-L
 Aletris glabra Bur. & Franch. BG-E 19892198
 Lophiola americana (Pursh) Along Highway 71 at White City
 Wood Fire Tower, Gulf Co., FL; leg.
 L. G. Chafin
 Narthecium assifragum (L.) BG-BONN
Melanthiaceae s.str.
 Chamaelirium luteum (L.) Gray Stephens Co., GA; leg. Davis &
 Spangler 30 (GH), sent by D. E.
 Chinographis japonica Maxim BG-E 19761879
 Helonias bullata L. BG-K
 Heloniopsis orientalis (Thunb.) BG-HEID
 Paris quadrifolia BG-HEID
 Stenanthium gramineum (Ker.- BG-E 19740350
 Gawl.) Morong
 Trillium cernuum L. BG-HEID
 Trillium grandiflorum (Michx.) BG-M
 Trillium sessile L. BG-HEID
 Veratrum album L. BG-HEID
 Veratrum formosanum Loes. BG-BAS 489/97
 Veratrum nigrum L. BG-BAS 77/97
 Xerophyllum temax (Pursh) Nutt. BG-UC (Berkeley); sent by H. C.
 Zigadenus elegans Pursh BG-BONN
 Zigadenus glaberrimus Michx. BG-M
 Sciaphila purpurea Benth. Depto. Loreto, PERU; leg. J.
 Skrabal & T. Franke 98/127 (M),
 sent by H.-J. Tillich
 Barbaceniopsis vargasiana BG-HEID
 (L. B. Sm.) L. B. Sm.
 Barbaceniopsis vargasiana BG-HEID
 (L. B. Sm.) L. B. Sm.
 Acanthochlamys bracteata Chengduan Mountains, W-Sichuan,
 CHINA; sent by P. C. Kao
 Acanthachlamys bracteata Chengduan Mountains, W-Sichuan,
 CHINA; sent by P. C. Kao
 Hygroryza aristata (Retz.) Nees BG-HEID
 ex Wight & Arn.

(a)Monocotyledon families arranged after Chase et al. (2000).

(b)See Fig. 1.

(c)pedicel or peduncle P = petiole S = stem V = leaf vein.

(d)For cultivated material, the acronyms of botanical gardens (BG)
follow Holmgren et al. (1990).

(e)Previously (Behnke, 2000) erroneously reported to have form-P2cs

VI. Acknowledgments

I thank all those who have over the years generously helped collect specimens in the wild for me, especially D. G. Boufford (Cambridge,

MA), L. G. Chafin (Tallahassee, FL), S. B. Jones (Athens, GA), P.-C. Kao (Chengdu, People's Republic of China), C. McPherson (Saint Louis, MO), S. Porembski (Rostok, Germany), R. Saunders (Hong Kong), B. A. Sorrie (Southern Pines, NC), T. F. Stuessy (Vienna, Austria), M. N. Tamura (Osaka, Japan), and H.-J. Tillich (Munich, Germany), and all those who helped to select or send specimens from the living collections of their institutions, especially R. Andrews (Kew, England), P. O. Ashby (Edinburgh, Scotland), J. Bogner (Munich, Germany), H. C. Forbes (Berkeley, CA), U. Hecker (Mainz, Germany), K. Kramer (Heidelberg, Germany), and B. Matter (Basel, Switzerland).

VII. Literature Cited

Ambrose, J. D. 1980. A re-evaluation of the Melanthioideae (Liliaceae) using numerical analyses. Pp. 65-81 in C. D. Brickell, D. F. Cutler & M. Gregory (eds.), Petaloid monocotyledons: Horticultural and botanical research. Linn. Soc. Symposium Ser., 8. Academic Press, London, New York.

APG (Angiosperm Phylogeny Group). 1998. An ordinal classification for the families of flowering plants. Ann. Missouri Bot. Gard. 85: 53 1-553.

Behnke, H.-D. 1971. Zum Feinbau der Siebrohren-Plastiden von Aristolochia und Asarum (Aristolochiaceae). Planta 97: 62-69.

-----. 1972. Sieve-tube plastids in relation to angiosperm systematics: An attempt towards a classification by ultrastructural analysis. Bot. Rev. (Lancaster) 38: 155-197.

-----. 1974. Sieve-element plastids of Gymnospermae: Their ultrastructure in relation to systematics. Pl. Syst. Evol. 123: 1-12.

-----. 1981a. Siebelement-Plastiden Phloem-Protein und Evolution der Blutenpflanzen, II. Monokotyledonen Ber. Deutsch. Bot. Ges. 94: 647-662.

-----. 198lb. Sieve-element characters. Nord. J. Bot. 1: 381-400.

-----. 1988. Sieve-element plastids, phloem protein and evolution of flowering plants, III. Magnoliidae. Taxon 37, 699-732.

-----. 1990. Sieve elements of internodal and nodal anastomoses of the monocotyledon liana Dioscorea. Pp. 161-178 in H.-D. Behnke & R. D. Sjolund (eds.), Sieve elements: Comparative structure, induction and development. Springer-Verlag, Berlin, Heidelberg, New York.

-----. 1991. Distribution and evolution of forms and types of sieve-element plastids in the dicotyledons. Aliso 13: 167-182.

-----. 1995. P-type sieve-element plastids and the systematics of the Arales (sensu Cronquist 1988), with S-type plastids in Pistia. Pl. Syst. Evol. 195: 87-119.

-----. 2000. Forms and sizes of sieve-element plastids and evolution of the monocotyledons. Pp. 163-188 in K. L. Wilson & D. A. Morrison (eds.), Monocots: Systematics and evolution. CSIRO, Melbourne, Australia.

-----, J. Treutlein, M. Wink, K. Kramer, C. Schneider & P. C. Kao. 2000. Systematics and evolution of the Velloziaceae, with special reference to sieve-element plastids and rbcL sequence data. Bot. J, Linn. Soc. 134: 93-129.

Bessey, C. E. 1893. Evolution and classification. Bot. Gaz. 18: 329-333.

Caddick, L. R., P. J. Rudall, P. Wilkin & M. W. Chase. 2000. Yams and their allies: Systematics of Dioscoreales. Pp. 475-487 in K. L. Wilson & D. A. Morrison (eds.), Monocots: Systematics and evolution. CSIRO, Melbourne, Australia.

Chase, M. W., D. E. Soltis, R. G. Olmstead, D. Morgan, D. H. Les, B. D. Mishler, M. R. Duvall, R. A. Price, H. G. Hills, Y.-L. Qiu, K. A. Kron, J. H. Rettig, E. Conti, J. D. Palmer, J. R. Manhart, K. J. Sytsma, H. J. Michaels, W. J. Kress, K. G. Karol, W. D. Clark, M. Heden, B. S. Gaut, R. K. Jansen, K.-J. Kim, C. F. Wimpee, J. F. Smith, G. R. Furnier, S. H. Strauss, Q.-Y. Xiang, G. M. Plunkett, P. S. Soltis, S. M. Swensen, S. E. Williams, P. A. Gadek, C. J. Quinn, L. E. Eguiarte, E. Golenberg, G. H. Learn Jr., S. W. Graham, S. C. H. Barrett, S. Dayanandan & V. A. Albert. 1993. Phylogenetics of seed plants: An analysis of nucleotide sequences from the plastid gene rbcL. Ann. Missouri Bot. Gard. 80: 528-580.

-----, M. R. Duvall, H. G. Hills, J. G. Conran, A. V. Cox, L. E. Eguiarte, J. Hartwell, M. F. Fay, L. R. Caddick, K. M. Cameron & S. Hoot. 1995a. Molecular phylogenetics of Lilianae. Pp. 109-137 in P. J. Rudall, P. J. Cribb, D. F. Cutler & C. J. Humphries (eds.), Monocotyledons: Systematics and evolution. 2 vols. Roy. Bot. Gard., Kew.

-----, D. W. Stevenson, P. Wilkin & P. J. Rudall. 1995b. Monocot systematics: A combined analysis. Pp. 685-730 in P. J. Rudall, P. J. Cribb, D. F. Cutler & C. J. Humphries (eds.), Monocotyledons: Systematics and evolution. 2 vols. Roy. Bot. Gard., Kew.

-----, D. E. Soltis, P. S. Soltis, P. J. Rudall, M. F. Fay, W. H. Hahn, S. Sullivan, J. Joseph, M. Molvray, P. J. Kores, T. J. Givnish, K. J. Sytsma & J. C. Pires. 2000. Higher-level systematics of the monocotyledons: An assessment of current knowledge and a new classification. Pp. 3-16 in K. L. Wilson & D. A. Morrison (eds.), Monocots: Systematics and evolution. CSIRO, Melbourne, Australia.

Cronquist, A. 1981. An Integrated System of Classification of Flowering Plants. Columbia Univ. Press, New York.

-----, 1988. The Evolution and Classification of Flowering Plants. Ed. 2. New York Bot. Gard., Bronx. Dahlgren, R. & K. Bremer. 1985. Major clades of the angiosperms. Cladistics 1: 349-368.

-----, & F. N. Rasmussen. 1983. Monocotyledon evolution. Characters and phylogenetic estimation. Evol. Biol. 16: 255-395.

-----, H. T. Clifford & P. F. Yeo. 1985. The families of the monocotyledons: Structure, evolution, and taxonomy. Springer-Verlag, Berlin.

Duvall, M. R. 2000. Seeking the sister group of the monocots. Pp. 25-32 in K. L. Wilson & D. A. Morrison (eds.), Monocots: Systematics and evolution. CSIRO, Melbourne, Australia.

-----, G. H. Learn, L. E. Eguiarte & M.T. Clegg. 1993a. Phylogenetic analysis of rbcL sequences identifies Acorus calamus as the primal extant monocotyledon. Proc. Natl. Acad. U.S.A. 90: 4641-4644.

-----, M. T. Clegg, M. W. Chase, W. D. Clark, W. J. Kress, H. G. Hills, L. E. Eguiarte, J. F. Smith, B. S. Gant & E. Zimmer. 1993b. Phylogenetic hypotheses for the monocotyledons constructed from rbcL sequence data. Ann. Missouri Bot. Gard. 80: 607-619.

Engler, A. 1892. Die systematische Anordnung der monokotyledonen Angiospermen. Abh. Preuss. Akad. Wiss. Fuse, S. & M. N. Tamura. 2000. A phylogenetic analysis of the plastid matK gene with emphasis on Melanthiaceae sensu lato. Pl. Biol. 2: 415-427.

Goldblatt, P. 1995. The status of R. Dahlgren's orders Liliales and Melanthiales. Pp. 181-200 in P. J. Rudall, P. J. Cribb, D. F. Cutler & C. J. Humphries (eds.), Monocotyledons: Systematics and evolution. 2 vols. Roy. Bot. Gard., Kew.

Grayum, M. H. 1987. A summary of evidence and arguments supporting the removal of Acorus from the Araceae. Taxon 36: 723-729.

Hallier, H. 1905. Em zweiter Entwurf des naturlichen (phylogenetischen) Systems der Blutenpflanzen. Vorlaufige Mitteilung. Ber. Deutsch. Bot. Ges. 23: 85-91.

Holmgren, P. K., N. H. Holmgren & L. C. Barnett (eds.). 1990. Index herbariorum, I. The herbaria of the world. Ed. 8. New York Hot. Gard., Bronx.

Huber, H. 1969. Die Samenmerkmale und Verwandtschaftsverhaltnisse der Liliifloren. Mitt. Bot. Staatssamml. Munchen 8: 219-538.

-----, 1977. The treatment of the monocotyledons in an evolutionary system of classification. P1. Syst. Evol., Suppl. 1: 285-296.

-----. 1982. Die zweikeimblattrigen Geholze im System der Angiospermen. Mitt. Bot. Staatssamml. Munchen 18: 59-78.

-----. 1991. Angiospermen: Leitfaden durch die Ordnungen and Familien der Bedecktsamer. Fischer-Verlag, Stuttgart, New York.

Kubitzki, K., P. J. Rudall & M. W. Chase. 1998. Systematics and Evolution. Pp. 23-33 in K. Kubitzki (ed.), The families and genera of vascular plants. Vol.3. Flowering plants: Monocotyledons: Lilianae (except Orchidaceae). Springer-Verlag, Berlin.

Nakai, T. 1930. Plantae Japonicae and Koreanae. Bot. Mag. (Tokyo) 44: 22-23.

Qiu, Y.-L. J. Lee, F. Bernasconi-Quadroni, D. E. Soltis, P. S. Soltis, M. Zanis, E. A. Zimmer, Z. Chen, V. Savolainen & M. W. Chase. 2000. Phylogeny of basal angiosperms: analyses of five genes from three genomes. Int. J. PI. Sci. 161 (6 Suppl.): S3-S27.

Rudall, P. J., P. J. Cribb, D. F. Cutler & C. J. Humphries (eds.). 1995. Monocotyledons: Systematics and evolution. 2 vols. Roy. Bot. Gard., Kew.

-----, K. L. Stobart, W.-P. Hong, J. G. Conran, C. A. Furness, G. C. Kite & M. W. Chase. 2000. Consider the lilies: Systematics of the Liliales. Pp. 347-359 in K. L. Wilson & D. A. Morrison (eds.), Monocots: Systematics and evolution. CSIRO, Melbourne, Australia.

Savolainen, V., M. F. Fay, D. C. Albach, A. Backlund, M. van der Bank, K. M. Cameron, S. A. Johnson, M. D. Liedo, J.-C. Pintaud, M. Powell, M. C. Sheahan, D. E. Soltis, P. S. Soltis, P. Weston, W. M. Whitten, K. J. Wurdack & M. W. Chase. 2000. Phylogeny of the eudicots: A nearly complete familial analysis based on rbcL gene sequences. Kew Bull. 55: 257-309.

Soltis, D. E., P. 5. Soltis, M. W. Chase, M. E. Mart, D. C. Albach, M. Zanis, V. Savolainen, W. H. Hahn, S. B. Hoot, M. F. Fay, M. Axtell, S. M. Swensen, L. M. Prince, W. J. Kress, K. C. Nixon & J. S. Farris. 2000. Angiosperm phylogeny inferred from 18S rDNA, rbcL and atpB sequences. Bot. J. Linn. Soc. 133: 381-461.

Takhtajan, A. 1997. Diversity and classification of flowering plants. Columbia Univ. Press, New York.

Tamura, M. N. 1998. Nartheciaceae. Pp. 381-392 in K. Kubitzki (ed.), The families and genera of vascular plants. Vol. 3. Flowering plants: Monocotyledons: Lilianae (except Orchidaceae). Springer-Verlag, Berlin.

Tillich, H.-J. 1985. Keimlingsbau und verwandtsehaftliche Beziehungen der Araceae. Gleditschia 13: 63-73.

Utech, F. H. 1984. Floral vascular anatomy of Japonolirion osense Nakai (Liliaceae) and its tribal relationship. Ann. Carnegie Mus. 53: 447-461.

Walker, J. W. 1986. Classification and evolution of the monocotyledons. Amer. J. Bot. 73: 746.

Wilson, K. L. & D. A. Morrison (eds.). 2000. Monocots: Systematics and evolution. CSIRO, Melbourne, Australia.

Zomlefer, W. B. 1999. Advances in angiosperm systematics: Examples from the Liliales and Asparagales. J. Torrey Bot. Soc. 125: 58-62.
COPYRIGHT 2002 New York Botanical Garden
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2002 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Author:Behnke, H. Dietmar
Publication:The Botanical Review
Date:Oct 1, 2002
Previous Article:Leaf anatomical characters and their value in understanding morphoclines in the Araceae.
Next Article:Morphology and angiosperm systematics in the Molecular era.

Terms of use | Copyright © 2018 Farlex, Inc. | Feedback | For webmasters