Carol A. Furness

Evolution of Microsporogenesis in Angiosperms

Microsporogenesis is highly labile in early‐branching angiosperms, i.e., those with mostly sulcate pollen, compared with the tricolpate and tricolpate‐derived eudicots. New records of microsporogenesis in basal angiosperms (19 taxa were examined), together with a review of the literature, demonstrate that the existing typology has been too strictly applied; several basal angiosperms have apparently intermediate forms and therefore do not fit easily into simultaneous or successive categories. Intermediate forms include the “modified simultaneous” type, where ephemeral cell plates are formed after the first meiotic division but then disperse, and simultaneous cleavage follows the second meiotic division. This relative diversity reflects a range of variation in number and position of pollen apertures in basal angiosperms, although both monosulcate and inaperturate pollen may occur in conjunction with either simultaneous or successive microsporogenesis. However, many taxa with inaperturate pollen have successive microsporogenesis, whereas many monosulcate taxa have the simultaneous type (although successive and monosulcate is common in monocotyledons). The predominance of simultaneous microsporogenesis in extant basal angiosperms and in land plants in general (including gymnosperms) indicates that simultaneous microsporogenesis is plesiomorphic in angiosperms, despite the occurrence of the successive type in the putative first‐branching extant angiosperm, Amborella. This conclusion contradicts earlier views on the evolutionary polarity of this character.

INAPERTURATE POLLEN IN MONOCOTYLEDONS

Inaperturate pollen is widespread in the monocotyledons, includes a diverse range of forms, and has arisen independently numerous times. Evidence for this comes from the phylogenetic distribution of inaperturate pollen and also from developmental and structural differences. There is no correlation between the production of inaperturate grains and either microsporogenesis type or tapetum type. Inaperturate pollen has phylogenetic significance within some groups, e.g., in Zingiberales, Liliales, and some Asparagales. Character states for inaperturate pollen are presented. It can broadly be divided into two types, “omniaperturate” and “functionally monoaperturate,” based on the thickening of the intine. The characters of omniaperturate pollen are adaptations that potentially increase the germination efficiency of the pollen. Both types sometimes occur in environments where pollen is not subject to desiccation and, thus, may remain viable with reduced exines.

Phylogenetic relationships in Cyperaceae subfamily Mapanioideae inferred from pollen and plastid DNA sequence data.

Cyperaceae are the third largest monocotyledon family, with considerable economic and conservation importance. In subfamily Mapanioideae there is particular specialization of the inflorescence into units termed spicoids. The structural homology of the spicoid is difficult to interpret, making determination of intrafamilial relationships problematic. To address this, pollen from eight species in Mapanioideae was investigated using light microscopy and scanning and transmission electron microscopy. Pollen development was also examined to identify the type of pollen present in these species. We also analyzed DNA sequence data using the trnL-F and rps16 regions from 25 genera and 35 species of Cyperaceae, Juncaceae, and Thurniaceae. Two types of pollen, Mapania-type and pseudomonad, were identifed. Analysis of combined DNA and pollen data resolved a clade sister to the rest of Cyperaceae, corresponding to Mapanioideae. Within this, two further clades were resolved. One comprised taxa assigned to tribe Hypolytreae, which had Mapania-type pollen. The other comprised taxa mainly assigned to tribe Chrysitricheae, but included two taxa from Hypolytreae, Capitularina and Exocarya. All taxa in this clade had pseudomonad pollen. Thus new groupings within the subfamily have been discovered based on the specialization of some taxa in terms of their pollination biology.

A Plastid Gene Phylogeny of the Yam Genus, Dioscorea: Roots, Fruits and Madagascar

Abstract Following recent phylogenetic studies of the families and genera of Dioscoreales, the identification of monophyletic infrageneric taxa in the pantropical genus Dioscorea is a priority. A phylogenetic analysis based on sequence data from the plastid genes rbcL and matK is presented, using 67 species of Dioscorea and covering all the main Old World and selected New World lineages. The analysis used 14 outgroup taxa, including Trichopus Gaertn., Tacca J.R. & G. Forster, Stenomeris Planch., Burmannia L. and Thismia Griff. The main findings are: a) that a clade of rhizomatous taxa is sister to the rest of Dioscorea; b) the main Old World groups (such as the right-twining D. sect. Enantiophyllum) are monophyletic and c) there are two distinct lineages among the endemic Malagasy taxa. The consequences of the results for infrageneric classification of Dioscorea is considered, in particular the possibility of greatly simplifying the classifications of Knuth and Burkill. The results are also used to present novel hypotheses of character evolution in selected underground storage organ, inflorescence, fruit and seed characters and to discuss the origins of diversity in Dioscorea.

The Tapetum in Basal Angiosperms: Early Diversity

The distribution of tapetal types in basal angiosperms is reviewed both from the literature and new observations in the context of recent phylogenetic analyses. Secretory tapeta predominate among land plants. The majority of basal angiosperms share a secretory tapetum with their anthophyte ancestors. Plasmodial and invasive tapeta are relatively rare in eudicots but have evolved several times among early‐branching angiosperms, especially in monocotyledons, in which they have evolved three or more times. The invasive tapetum has evolved at least four other times independently in basal angiosperms: in Nymphaeaceae, Annonaceae, Monimiaceae, and Winteraceae. Plasmodial tapeta are mostly found in monocotyledons but have evolved at least twice in basal angiosperms, in Annonaceae, and in Hernandiaceae/Lauraceae. This apparent plasticity for a relatively brief but critical time in angiosperm evolution may reflect the early evolution of highly specific pollination syndromes.

The Tapetum and Systematics in Monocotyledons

This paper critically reviews the homologies and distribution of tapetum types in monocotyledons, in relation to their systematics. Two main types of tapetum are widely recognised: secretory and plasmodial, although intermediate types occur, such as the “invasive” tapetum described inCanna. In secretory tapeta, a layer of cells remains intact around the anther locule, whereas in the plasmodial type a multinucleate tapetal plasmodium is formed in the anther locule by fusion of tapetal protoplasts. In invasive tapeta, the cell walls break down and tapetal protoplasts invade the locule without fusing to form a plasmodium. When examining tapetum type, it is often necessary to dissect several developmental stages of the anthers. Secretory and plasmodial tapeta are both widely distributed in monocotyledons and have probably evolved several times, although there may be some systematic significance within certain groups. Among early branching taxa,Acorus andTofieldia have secretory tapeta, whereas Araceae and Alismatales are uniformly plasmodial. The tapetum is most diverse within Commelinanae, with both secretory and plasmodial types, and some Zingiberales have an invasive tapetum. Lilianae (Dioscoreales, Liliales, and Asparagales) are almost uniformly secretory.

Microsporogenesis and pollen morphology in dioscoreales and allied taxa

Analyses of new morphological and molecular data have resulted in a major recircumscription of Dioscoreales. However crucial characters such as microsporogenesis type and pollen morphology are not known for some taxa, and these are investigated here, particularly in view of the revised systematics of the order. Pollen morphological characters and microsporogenesis were examined using both electron microscopy (scanning and transmission) and light microscopy (including differential interference contrast). Microsporogenesis and pollen morphology were found to provide taxonomically useful characters, particularly at the genus level. Successive microsporogenesis is plesiomorphic in monocotyledons, and simultaneous microsporogenesis in Dioscorea, Rajania, Tamus and Tacca represents a probable synapomorphy for these taxa. Simultaneous microsporogenesis also supports a close sister group relationship between Japonolirion and Petrosavia but from other characters (including molecular data), their relationship with ...

Phylogenetic comparative analysis of microsporogenesis in angiosperms with a focus on monocots

This paper presents the first broad overview of three main features of microsporogenesis (male meiosis) in angiosperms: cytokinesis (cell division), intersporal wall formation, and tetrad form. A phylogenetic comparative approach was used to test for correlated evolution among these characters and to make hypotheses about evolutionary trends in microsporogenesis. The link between features of microsporogenesis and pollen aperture type was examined. We show that the pathway associated with successive cytokinesis (cytoplasm is partitioned after each meiotic division) is restricted to wall formation mediated by centrifugally developing cell plates, and tetragonal (or decussate, T-shaped, linear) tetrads. Conversely, much more flexibility is observed when cytokinesis is simultaneous (two meiotic divisions completed before cytoplasmic partitioning). We suggest that the ancestral type of microsporogenesis for angiosperms, and perhaps for all seed plants, associated simultaneous cytokinesis with centripetal wall formation, resulting in a large diversity in tetrad forms, ranging from regular tetrahedral to tetragonal tetrads, including rhomboidal tetrads. From this ancestral pathway, switches toward successive cytokinesis occurred among basal angiosperms and monocots, generally associated with a switch toward centrifugal intersporal wall formation, whereas eudicots evolved toward an almost exclusive production of regular tetrahedral tetrads. No straightforward link is found between the type of microsporogenesis and pollen aperture type.

Apertures with Lids: Distribution and Significance of Operculate Pollen in Monocotyledons

In pollen terminology, an operculum is an area of exine covering a pollen aperture like a lid. Monosulcate‐operculate, pontoperculate, disulculate, disulcate, zonasulculate, and zonasulcate aperture types are often confused in the monocot pollen literature. Various factors contribute to this confusion, including the existence of intermediate forms. Other factors include the presence of artifacts (such as the collapse of thin‐walled pollen examined using SEM) and insufficient data, either on mature pollen (including absence of ultrastructural data using TEM) or on developmental stages, especially the critical tetrad stage. In this article, we review records of monosulcate‐operculate pollen in monocots in relation to recent phylogenetic concepts, using data both from the literature and our own observations, including new records of operculate pollen in Doryanthes and Chamaerops. The exine that forms the operculum often has a simpler structure than that of the rest of the grain and is underlain by thick, often channeled, apertural intine. With the exception of monocots, opercula are rare or absent in basal angiosperms with monosulcate pollen. Within monocots, monosulcate‐operculate pollen is absent from basal monocots (Acorus and Alismatales) and is relatively infrequent among commelinids, except for some Dasypogonaceae, Arecaceae, and Poales, in which the aperture is reduced to an ulcus. In contrast, it occurs frequently in the lilioid orders Liliales, particularly Liliaceae, Melanthiaceae, and Uvulariaceae; and Asparagales, particularly Doryanthaceae, Iridaceae, Tecophilaeaceae, and Agavaceae. Species with operculate pollen often have relatives with insulae or granules on the aperture membrane or with diaperturate pollen. In some taxa, monosulcate‐operculate pollen may represent a route in the evolution of diaperturate pollen from monoaperturate pollen, although this requires further testing. The operculum has evolved several times independently in monocots and may have a variety of related functions, such as protection of the delicate apertural area from pathogens and/or dehydration, particularly in taxa from dry habitats, and a role in harmomegathy.

The Enigmatic Tribe Whitfieldieae (Acanthaceae): Delimitation and Phylogenetic Relationships Based on Molecular and Morphological Data

Abstract Relationships of the enigmatic genera Whitfieldia, Chlamydacanthus, and Lankesteria (Acanthaceae) were examined using molecular sequence data for two chloroplast loci (ndhF gene, trnL-trnF spacer and intron) for these and a sample of taxa representing all major lineages within the family. Morphological data, including pollen structure as imaged using SEM, were also compiled for these three genera, and evaluated in a phylogenetic context. Bremekamp suggested that Whitfieldia and Chlamydacanthus belonged together as tribe Whitfieldieae, and that Lankesteria was closely related to Pseuderanthemum in Justicieae. Contra earlier classifications of Acanthaceae, this would result in tribes with multiple corolla aestivation patterns. Our results confirm that Chlamydacanthus and Whitfieldia are closely related. Unexpectedly, Lankesteria is sister to these two genera together and we propose that the three genera comprise an expanded tribe Whitfieldieae. Also unexpectedly, Whitfieldieae is sister to Barlerieae. We propose a number of morphological synapomorphies for Whitfieldieae including concentric rings of ridges on the seeds and a densely granular circular area surrounding the pores of pollen grains. Chlamydacanthus and Whitfieldia further share biporate, flattened pollen grains that are circular in outline, and seeds with glabrous surfaces. Barlerieae is a large and diverse lineage such that synapomorphies to support aspects of their relationships are difficult to identify. However, hygroscopic trichomes on the seeds may be a synapomorphy for Whitfieldieae plus Barlerieae, with subsequent loss in Chlamydacanthus, Whitfieldia, and some Barleria. As here circumscribed, Whitfieldieae includes plants with both contort and imbricate corolla aestivation seconding Bremekamps misgivings about basing classifications entirely upon this character. Communicating Editor: Richard Jensen