Vegetative Anatomy of the New Caledonian Endemic Amborella trichopoda: Relationships with the Illiciales and Implications for Vessel Origin

Abstract

Light microscopy was used to study leaf hypodermis, vein sclerenchyma, stomatal subsidiary cell types, and stem and root xylem in liquid-preserved material of Amborella trichopoda; oblique borders on tracheid pits, scalariform end walls on tracheids, and porosities in end-wall pit membranes were studied with scanning electron microscopy. Amborella shares stomatal configurations, nodal type (in part), ray types, and porose pit membranes in tracheary elements with Illiciales s.l., but differs from that order in lacking oil cells, vessels, and grouped axial parenchyma cells. These data are consistent with a basal position in angiosperms for Amborella, and for a close relationship with, but not inclusion in, Illiciales; inclusion in a monofamilial order is conceivable. Both loss of pit membranes or pit membrane portions on end walls and increase in cell diameter are requisites for origin of vessels. Sarcandra and Illiciaceae show these early stages in origin of vessels; Amborella shows development of porosities in pit membranes. Vessel presence or absence may not be strictly bipolar, because some primitive vessel elements exhibit at least some tracheidlike characteristics and are thus transitional, and because changes in at least two characters define vessel origin.

The single species of Amborellaceae (Amborella trichopoda Baill., New Caledonia) is claimed to be the sister group to the remainder of angiosperms according to recent studies (Mathews and Donoghue 1999, Parkinson et al. 1999, Qiu et al. 1999, Soltis et al. 1999). These studies each analyzed more than a single gene site, and this expanded data base as well as the similarity of the cladistic results yielded by these studies have commanded attention by phylogenists. Branching from the cladogram just above Amborella are Nymphaeales (excluding Nelumbonaceae), and then an expanded Illiciales (Illiciaceae, Schisandraceae, Austrobaileyaceae, Trimeniaceae). This treatment was foreshadowed by the results of the Angiosperm Phylogeny Group (1998), who placed a similar roster of families in an unnamed grouping cited first (and thus basal) in their ordering of angiosperms. The phylogenetic significance of anatomical features of Amborella potentially becomes very considerable.

In terms of vegetative anatomy, Amborella had already attracted attention because of the vesselless nature of its wood (Tieghem 1900, Bailey and Swamy 1948, Bailey 1957). Bailey regarded vessellessness as a primitive feature in woody dicotyledons, whereas recent cladists, beginning with Young (1981), regarded vessellessness as a derived condition in woody dicotyledons (for a discussion, see Baas and Wheeler 1996). The more recent cladistic work, cited above, by placing Amborella in a basal position in angiosperms, reopens the possibility that vessellessness is a primitive feature. If this possibility is valid, the nature of tracheids in Amborella becomes worthy of consideration.

By means of scanning electron microscopy (SEM), we are attempting to show whether tracheids of Amborella are transitional to vessels in any respect, and, by inference, whether vessels of Illiciales are essentially relatively little-modified versions of tracheids, as hypothesized by Bailey (1944) and Carlquist (1988). If vessel origin is a matter of degrees of intermediacy and change in character state in several characteristics, one can call into question the bipolarity of the coding of vessel presence in cladistic work.

Our materials differ from those available to earlier authors. Bailey and Swamy (1948) had only dried materials and therefore were unable to illustrate and identify some histological features completely. Bailey (1957) had wood of a relatively large stem, but was unable to present SEM data. We were able to study liquid-preserved material of roots, stems, and leaves of Amborella. These materials permit us to answer whether Amborella has oil or mucilage cells, the presence of which was denied by Bailey and Swamy (1948), although claimed by Perkins (1898), and to offer reports on other histological features hitherto undescribed. A useful summary of vegetative anatomy of Amborella was offered by Metcalfe (1987). If Amborella is the sister group to the remainder of dicotyledons, the character state of each feature in this plant takes on greater potential significance and aids in finding the best taxonomic and phylogenetic treatment for the genus.

Materials and Methods

Data on wood are derived from...