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ISSN OOOI-6799 ActaPhytotax,Geobot. 50(1):75-79(1999)

lntegumentary Studies in Menyanthaceae (Campanulales sensu lato)

' NOBUHIKO INOUE and HIROSHI TOBE2

'Sagano 2FZicudy High School, K),oto, KYoto 616-8226; qrintegrated Human Studies, K>roto Uitiversity, kyoto 606- 8501

Abstraet. On the basis of three species in three genera (Menyanthes, Nqphrophyllidium and N)Jnrphoides) of Menyanthaceae we found that the family has a thick, 10- to 25-cell-layered

integument as in Asteraceae and Goodeniaceae, and not a thin, 3- to 6-cell-layered integument as in Pentaphragmataceae and Campanulaceae sensu lato, In the light of a molecular phylogenetic tree of Campanulales sensu lato published elsewhere, the result suggests that the evolution from the thin to the thick integument occurred in a common ancestor with A$teraceae, Goodeniaceae, and Calyceraceae although the last family is not known yet with respect to integumentary thickness.

Key words: Astera]es, Campanulales, integument, Menyanthaceae, ovule

Received Febrt`ary 12, 1999; acceptedApril 26, J999

Menyanthaceae, comprising five genera and 40 species distributed worldwide as aquatic plants, had been placed in various plant groups such as Gentianales (e.g., Wagenitz, 1964; Goldberg, 1986), Solanales (Cronquist, 1981), Cornales (Dahlgren, 1989), Campanulales (with [Lammers, 1992] or without Asteraceae [TIhorne, 1992]), or its own order Menyanthales (rlakhtajan, 1992). Currently, however, there is an ample eyidence for placing it in Campanulales sens" lato (Asterales sensu lato). In fact a cladistic analysis (Gustafsson and Bremer, 1995) and molecular phylogenetic analyses Chase et al., 1993; Olmstead et al., 1993; Cosner et al., 1994; Gustafsson et al., 1996) both have showed that Menyanathaceae are closeiy related to campanulalean families and should be assigned to Campanulales sensu lato. Ibbe and Morin (1996) reviewed literatures on embryological studies in Campanulaies sens" lato and tried to show how embryological characters have evolved within the order (`EAsterid II" [Chase et al., 1993]) in the light of results of molecular phylogenetic analyses. One of the embryological characters that have evolved and thus are diversified within the order is the thickness of the sole integument. [[he families, like Pentadiplandraceae, Donatiaceae, Carnpanulaceae sensu lato, and Stylidiaceae, which are basally positioned in the phylogeny of Campanulales sensu lato have a thin, 3- to 6-cell-layered integument. On the other hand, advanced families like Asteraceae and Goodeniaceae have a much thicker, 12- to 25-cell-layered integument. Therefore there is no doubt that ovules have evolved toward those haying a thick integument within the order. However, since none of the earlier studies have referred to the thickness of the integument in Menyanthaceae (and Calyceraceae), it has remained unclear where an increase of the thickness of the integument exactly occurred, i.e., in an

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ancestor common to Asteraceae and Goodeniaceae as supposed by Tbbe and Morin (1996, p. 432, Fig. 1) or in a more basal ancestor common not only to Asteraceae and Goodeniaceae but also to Calyceraceae and Menyanthaceae. A few literatures of embryological studies, which were published befbre 1950 and concerned only with Menyanthes and Nymphoides, are available for Menyanthaceae but they have never referred to the development and thickness of mtegument. The purpose of this paper is to clarify whether Menyanthaceae have the thin or the thick integument,･ and thereby to show more exactly where the increase of the thickness of the integument had occurred in the evolution of Campanulales sensu lato.

Materials and Methods

The following three species in three genera of Menyanthaceae were investigated in this study: Menyanthes trijrbliata L. (Tbbe 312, Kyo), Nephrophyllidium crista-galli (Hook.) Gilg (Sugawara 970910, sHiN), and Alymphoides indica (L.) O. Kuntze (Kadono, no voucher). Flowers nearly at anthesis were fixed in FAA (5 parts formalin, 5 parts acetic acid, 90 parts 50% ethanol) and sectioned with a rotary microtome following standard paraffin methods. The thickness of the integument was measured on the basis of transverse sections of 14 (Menyanthes trijbliata), 8 (IVlephmphyllidium crista- galti), and 12 ovules (A6,mphoides indica), respectively.

Resulbs and Discussion

In all the three species examined their ovules have a single, multiplicative integument. In Menyanthes trijbliata (Figs. 1, 2) and ACymphoides indica (Figs. 5, 6) the ovules are more or less bilaterally flattened with the integument thicker on antiraphal side than on lateral side, while in AJephmphytlidium crista-galli (Figs. 3, 4) the ovules have no significant difference in thickness between antiraphal and lateral side. In Menyanthes trijbliata the integument is 13-18 cells thick on lateral side and 18-25 cells thick on antiraphal side, and in A71ymphoides indica it is 10-14 cells thick on lateral side and 15-20 cells thick on antiraphal side. These two genera are also similar in having not only the bilaterally flattened ovules but also a single (occasionally two) vascular bundle on antiraphal side. On the other hand, in Naphrqphyllidi"m crista-galli the integument is 1 O-14 cells thick. Now that Menyanthaceae were fOund to have a thick integument as in Asteraceae and Goodeniaceae, the evolution from the thin to the thick integument has evidently occurred early in the evolution of the Carirpanulales sensu lato, that is, in a cornmon ancestor to Asteraceae, Goodeniaceae, Menyanthaceae, and Calyceraceae. Fig. 7 presents the molecular phylogenetic tree illustrating the evolution of embryological characters in Campanulales sens" lato, which was presented by Tbbe and Morin (1996) but now is revised with respect to where the evolution from the thin to the thick integument occurred.

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August 1999 INOUE & TOBE: Integuments of Menyanthaceae 77 geL3 ng.Fi'i'':t

tt,/E,:lttlt//

"t t l/

r, #li.g} l[ "'I,Y'l

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-rtr.-r-r.,:･,:'f?,;k'1''i'"lI?:: - / ltl/tg//t-t//"t'll

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FIGs. 1-6, Microtome sectiens of mature ovules of Menyanthaceae. 1, 3, S. Longitudinal sections of ovules. 2, 4, 6. Transverse sections of ovules. 1 and 2. Menyanthes lriji)liata, 3 and 4. IVephrophyllidium crista-galli. S and 6, IV},imphoides indica, Arrows indicate vascular bundles running in the antiraphal side of ovule. Scales equal 100 "m in Figs. 1-5 and 50 "m in Fig. 6.

Whether Calyceraceae have a thin or a thick integument is however still unknown; in this respect therefore, the ovules of the members of Calyceraceae rnust be exarnined.

We are gratefu1 to Yasuro Kadono and Takashi Sugawara fbr their assistance in collecting materials used in the study.

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Asterid V Unitegmicovute Tenuinucelttzteavule Endothelium abinin'eCetlularendosperm

Asterid IV Endospermhaicstorium Asterid III

Asterid I Pentaphragmataceae Argophyllaceae Alseousmiaceae nsgE-.om: Stylidiaceae Campan"laceaes.t. Donatiaceae Lossofendospermhaustorium ff --AS-qQ-ig

-gs8yptv. 71tiekintegument Menyanthaceae

Ca]yceraceae

1i Scantyendesperm Goodeniaceae

NuclearAmoeboldtapetumendosperm Asteraceae(Mutisieae)

FIG. 7. Phylogenetic tree of an expunded Asteridae, showing an evolution of a few significant embryological characters particularly in Campanulales sensu Iato, The original figure was presented by Tobe and Morin (1996, p. 432), but it is llow revised with respect to the position at which the eyDlutien from the thin to the thick integument eccurred. An arrow indicates a transfer of the position where the thick integument (synapomorphy) was acquired, from the positiQn presented in Tobe and Morin (1996) to a more basal clade cornmon to Menyanthaceae, Calyceraceae, Goodeniaceae, ancl Asteraceae.

References

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. Clafk, M, Herdren, B. S, Gaut, R, K, Jansen, K,-J. Kim, C, F, Wimpee, J, F. Smith, G. R. Fumier, 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,

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Bomtraeger Berlin 、405 −424 ． GebrUder ， ， pp

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