Embryology of Phyllonoma (Phyllonomaceae, Aquifoliales): characteristics and character evolution

Abstract

Phyllonoma, the sole genus of Phyllonomaceae (Aquifoliales) consisting of four Central American species, has not been well-characterized morphologically. Following a previous study of flower and inflorescence morphology, I here report the embryology of the genus based on P. tenuidens and compare its characteristics with those of other aquifolialean families, namely, Aquifoliaceae, Cardiopteridaceae, Helwingiaceae, and Stemonuraceae. Comparisons indicate that although Phyllonoma resembles all the other families embryologically, it more closely resembles Aquifoliaceae and Helwingiaceae in lacking a vascular bundle in its integument and bearing ab initio Cellular endosperm. The genus especially resembles Helwingiaceae by possessing a tenuinucellate ovule. This result corroborates molecular and floral morphological evidence, supporting the distinctness of Phyllonoma as a family and its sister-group relationship to East‒Asian Helwingiaceae. However, Phyllonoma is clearly distinguished from Helwingiaceae by seed coat structure. In Phyllonoma, the seeds (dispersed in berries) have a thick seed coat composed of irregularly enlarged, thick-walled exotestal cells, whereas the seeds (dispersed in drupes) have a thin membranous seed coat in Helwingiaceae. Taken together with earlier information on pollination (entomophily in Phyllonoma versus ambophily in Helwingiaceae), embryological evidence shows that distinct evolution has occurred in reproductive characters relating to pollination and seed dispersal in Phyllonoma.

Embryology of Cardiopteris (Cardiopteridaceae, Aquifoliales), with emphasis on unusual ovule and seed development

“…Indeed, in Phyllonoma the integument is initiated by perclinal divisions in the epidermis of an ovule primordium ( Fig. 2b in Tobe 2015). Additionally, the integument does develop into the seed coat as in the other angiosperms (including other Aquifoliales, Table S1).…”

“…Except for Helwingiaceae and Phyllonomaceae, whose embryological features have recently been published by Ao and Tobe (2015) and Tobe (2015), the embryology of the other Cardiopteridaceae, Aquifoliaceae, and Stemonuraceae remain poorly understood. As in the papers on Helwingiaceae and Phyllonomaceae (Ao and Tobe 2015;Tobe 2015), I obtained data from Fagerlind (1945) and Mauritzon (1936) for three genera of Cardiopteridaceae (Citronella, Gonocaryum, and Leptaulus); from Brewbaker (1967), Copeland (1963), Corner (1976), Herr (1959Herr ( , 1961, Schürhoff (1921), and van Tieghem (1898) for Aquifoliaceae; and from Fagerlind (1945), Mauritzon (1936), and Padmanabhan (1961) for Stemonuraceae. Comparisons based on the available information (Table S1) showed that, Cardiopteris agrees with the other families of Aquifoliales (data not available for the other Cardiopteridaceae) in characters of the anther and microspore development.…”

“…In the ovular apex, which is considered to correspond to the nucellar apex because it is destroyed later by a growing female gametophyte as in other Aquifoliales (Ao and Tobe 2015;Tobe 2015), epidermal cells do not divide periclinally to form a nucellar cap ( Fig. 2d-g, i).…”

“…Both the position of the megaspore mother cell and its subsequent development into the seven-celled/ eight-nucleate female gametophyte agree with what we know as the mode of the Polygonum type. In addition, the apical nucellar epidermal cells are destroyed by the developing female gametophyte in Cardiopteris, a phenomenon observed at the micropylar side in the anatropous ovules of the other Aquifoliales (Ao and Tobe 2015;Tobe 2015). Accordingly, we can regard the apical side of the female gametophyte of Cardiopteris as equivalent to the micropylar side of the Polygonum type female gametophyte of the other Aquifoliales and the funicular side of the former as equivalent to the chalazal side of the latter (hereafter, the apical and funicular side of the Cardiopteris female gametophyte is referred to as the micropylar and chalazal side).…”

“…Thus, development of the ovules and female gametophytes in Cardiopteris needs confirmation (Stevens 2001 onwards). Recently I have published the embryology of other families of the Aquifoliales, i.e., Helwingiaceae (Ao and Tobe 2015) and Phyllonomaceae (Tobe 2015), but the aforementioned uncertainties of Cardiopteris species have hindered critical comparisons of these families with Cardiopteridaceae (Ao and Tobe 2015;Tobe 2015).…”