Jeffrey G. Duckett

The dawn of symbiosis between plants and fungi

The colonization of land by plants relied on fundamental biological innovations, among which was symbiosis with fungi to enhance nutrient uptake. Here we present evidence that several species representing the earliest groups of land plants are symbiotic with fungi of the Mucoromycotina. This finding brings up the possibility that terrestrialization was facilitated by these fungi rather than, as conventionally proposed, by members of the Glomeromycota. Since the 1970s it has been assumed, largely from the observation that vascular plant fossils of the early Devonian (400 Ma) show arbuscule-like structures, that fungi of the Glomeromycota were the earliest to form mycorrhizas, and evolutionary trees have, until now, placed Glomeromycota as the oldest known lineage of endomycorrhizal fungi. Our observation that Endogone-like fungi are widely associated with the earliest branching land plants, and give way to glomeromycotan fungi in later lineages, raises the new hypothesis that members of the Mucoromycotina rather than the Glomeromycota enabled the establishment and growth of early land colonists.

The phylogeny of land plants: A cladistic analysis based on male gametogenesis

A cladistic analysis was carried out to resolve phylogenetic pattern among bryophytes and other land plants. The analysis used 22 taxa of land plants and 90 characters relating to male gametogenesis.Coleochaete orChara/Nitella were the outgroups in various analyses using HENNIG86, PAUP, and MacClade, and the land plant phylogeny was unchanged regardless of outgroup utilized. The most parsimonious cladograms from HENNIG86 (7 trees) have treelengths of 243 (C.I. = 0.58, R.I. = 0.82). Bryophytes are monophyletic as are hornworts, liverworts, and mosses, with hornworts identified as the sister group of a liverwort/moss assemblage. In vascular plants, lycophytes are polyphyletic andSelaginella is close to the bryophytes.Lycopodium is the sister group of the remaining vascular plants (minusSelaginella). Longer treelengths (over 250) are required to produce tree topologies in which either lycophytes are monophyletic or to reconstruct the paraphyletic bryophyte phylogeny of recent authors. This analysis challenges existing concepts of bryophyte phylogeny based on more classical data and interpretations, and provides new insight into land plant evolution.

Evolution of the major moss lineages: phylogenetic analyses based on multiple gene sequences and morphology

Abstract Evolutionary relationships of mosses are still poorly understood, with family, order, and subclass circumscription and relationships remaining especially obscure. Over the past decade, a considerable body of data has accumulated, including information on morphological, developmental, anatomical, and ultrastructural characteristics, as well as nucleotide sequences for a number of nuclear and plastid genes. We have combined data from these different sources to provide an overview of the relationships of the major lineages of mosses. We analyzed a data set that includes 33 moss species and ten outgroup taxa drawn from the liverworts, hornworts, and vascular plants. Molecular data consisted of nucleotide sequences from four DNA regions, (rbcL, trnL-trnF, rps4 and 18S). Morphological data included 41 characters of which many were derived from published anatomical and ultra-structural studies. Combining morphological and molecular data in the analyses showed that mosses, including Sphagnum, Takakia, Andreaea and Andreaeobryum, form a monophyletic group, provided improved resolution of higher level relationships, and further insight into evolutionary patterns in morphology.

Bryophyte phylogeny: Advancing the molecular and morphological frontiers

Abstract Revolutionary new concepts of bryophyte relationships have emerged from molecular phylogenetic analyses conducted since the onset of the 21st century. For example, sequence data contradict the historical notion that isophylly in leafy liverworts is plesiomorphic and that simple thalloid liverworts are monophyletic. Also contrary to traditional views are the concepts that Leiosporoceros is genetically distinct from other hornworts and that Oedipodium is sister to the peristomate mosses. Substantial increases in ultrastructural and anatomical data likewise have provided new insights on interrelationships. Because of this recent deluge in evolutionary studies on bryophytes, it is an opportune time to co-examine contemporary morphological knowledge and novel molecular hypotheses. An understanding of bryophyte evolution and biology is essential to identify structural innovations that accompanied early land colonization and to illuminate the evolution of more complicated body plans in tracheophytes. In this review, we examine the progress that has been made since the 1999 International Botanical Congress in clarifying the evolutionary history of the three groups of bryophytes. The state of our knowledge on interrelationships is discussed, with poorly-known, genetically divergent taxa illustrated for each group. Our review of bryophyte evolution includes a reëvaluation of the evolution of sperm cells, sporogenesis, stomata, symbioses, conducting cells and chloroplast ultrastructure in hornworts. We explore the prospects for future discoveries and advances with an emphasis on fundamental evolutionary problems that remain and the challenges that must be met to resolve them.

An X-ray Microanalytical Study of the Distribution of Cadmium in Roots of Zea mays L.

X-ray microanalysis of roots of Zea mays L. grown in the presence of cadmium, revealed that the absorbed metal is removed by normal electron microscope preparative procedures. Following pretreatment with either phosphate or sulphide to immobilize cadmium, the metal was detected in the walls of the sieve elements and in the middle lamella separating the endodermis from the pericycle. These findings suggest that cadmium is principally bound to ion exchange sites on pectic residues in the cell wall.

Glomeromycotean associations in liverworts: a molecular, cellular, and taxonomic analysis

Liverworts form endophytic associations with fungi that mirror mycorrhizal associations in tracheophytes. Here we report a worldwide survey of liverwort associations with glomeromycotean fungi (GAs), together with a comparative molecular and cellular analysis in representative species. Liverwort GAs are circumscribed by a basal assemblage embracing the Haplomitriopsida, the Marchantiopsida (except a few mostly derived clades), and part of the Metzgeriidae. Fungal endophytes from Haplomitrium, Conocephalum, Fossombronia, and Pellia were related to Glomus Group A, while the endophyte from Monoclea was related to Acaulospora. An isolate of G. mosseae colonized axenic thalli of Conocephalum, producing an association similar to that in the wild. Fungal colonization in marchantialean liverworts suppressed cell wall autofluorescence and elicited the deposition of a new wall layer that specifically bound the monoclonal antibody CCRC-M1 against fucosylated side groups associated with xyloglucan and rhamnogalacturonan I. The interfacial material covering the intracellular fungus contained the same epitopes present in host cell walls. The taxonomic distribution and cytology of liverwort GAs suggest an ancient origin and multiple more recent losses, but the occurence in widely separated liverwort taxa of fungi related to glomeromycotean lineages that form arbuscular mycorrhizas in tracheophytes, notably the Glomus Group A, is better explained by host shifting from tracheophytes to liverworts.

First evidence of mutualism between ancient plant lineages (Haplomitriopsida liverworts) and Mucoromycotina fungi and its response to simulated Palaeozoic changes in atmospheric CO2

The discovery that Mucoromycotina, an ancient and partially saprotrophic fungal lineage, associates with the basal liverwort lineage Haplomitriopsida casts doubt on the widely held view that Glomeromycota formed the sole ancestral plant–fungus symbiosis. Whether this association is mutualistic, and how its functioning was affected by the fall in atmospheric CO2 concentration that followed plant terrestrialization in the Palaeozoic, remains unknown. We measured carbon-for-nutrient exchanges between Haplomitriopsida liverworts and Mucoromycotina fungi under simulated mid-Palaeozoic (1500 ppm) and near-contemporary (440 ppm) CO2 concentrations using isotope tracers, and analysed cytological differences in plant–fungal interactions. Concomitantly, we cultured both partners axenically, resynthesized the associations in vitro, and characterized their cytology. We demonstrate that liverwort–Mucoromycotina symbiosis is mutualistic and mycorrhiza-like, but differs from liverwort–Glomeromycota symbiosis in maintaining functional efficiency of carbon-for-nutrient exchange between partners across CO2 concentrations. Inoculation of axenic plants with Mucoromycotina caused major cytological changes affecting the anatomy of plant tissues, similar to that observed in wild-collected plants colonized by Mucoromycotina fungi. By demonstrating reciprocal exchange of carbon for nutrients between partners, our results provide support for Mucoromycotina establishing the earliest mutualistic symbiosis with land plants. As symbiotic functional efficiency was not compromised by reduced CO2, we suggest that other factors led to the modern predominance of the Glomeromycota symbiosis.

The Gametophyte-Sporophyte Junction in Land Plants

Publisher Summary The chapter presents a comparative analysis of the placenta in land plants. The gametophyte–sporophyte junction is termed as the placental region. Systematic survey of bryophytes, pteridophytes, and placental analogues in seed plants are also explained. The gametophyte–sporophyte junctions in bryophyte groups are distinguished by the presence or absence of cell wall labyrinths in the placental cells, cell wall structure, shape, and arrangement of wall ingrowths and plastid morphology. Two stages of sporophyte development, the pre–meiotic stage and post–meiotic stage are discussed. Studies carried out by using the representatives of bryophyte groups namely mosses, liverworts, and anthocerotes are explained. The chapter also explains characteristic features of placenta like the distribution of transfer cells, distribution of wall ingrowth and time of ingrowth for different organisms belonging to mosses and liverworts. Cytoplasmic features of placental cells like shape, membrane system, plastoglobuli, and starch for sporophyte and gametophyte in mosses and liverworts are described. The anthocerotes are distinguished based on cytological, anatomical, and developmental characteristics. The taxonomic significance of placenta in bryophytes and the implications on phylogeny are also discussed. Differences in the placental regions, cell wall ingrowths, and intercellular spaces between bryophytes and pteridophytes are explained. These differences are related to the transient nature of sporophytic dependence on the gametophyte in pteridophytes. Transfer cell morphology has been described at every site of solute exchange via the apoplast of angiosperms.

Symbiotic options for the conquest of land

The domination of the landmasses of Earth by plants starting during the Ordovician Period drastically altered the development of the biosphere and the composition of the atmosphere, with far-reaching consequences for all life ever since. It is widely thought that symbiotic soil fungi facilitated the colonization of the terrestrial environment by plants. However, recent discoveries in molecular ecology, physiology, cytology, and paleontology have brought into question the hitherto-assumed identity and biology of the fungi engaged in symbiosis with the earliest-diverging lineages of extant land plants. Here, we reconsider the existing paradigm and show that the symbiotic options available to the first plants emerging onto the land were more varied than previously thought.

Exploding a myth: the capsule dehiscence mechanism and the function of pseudostomata in Sphagnum

The nineteenth century air-gun explanation for explosive spore discharge in Sphagnum has never been tested experimentally. Similarly, the function of the numerous stomata ubiquitous in the capsule walls has never been investigated. Both intact and pricked Sphagnum capsules, that were allowed to dry out, all dehisced over an 8-12 h period during which time the stomatal guard cells gradually collapsed and their potassium content, measured by X-ray microanalysis in a cryoscanning electron microscope, gradually increased. By contrast, guard cell potassium fell in water-stressed Arabidopsis. The pricking experiments demonstrate that the air-gun notion for explosive spore discharge in Sphagnum is inaccurate; differential shrinkage of the capsule walls causes popping off the rigid operculum. The absence of evidence for a potassium-regulating mechanism in the stomatal guard cells and their gradual collapse before spore discharge indicates that their sole role is facilitation of sporophyte desiccation that ultimately leads to capsule dehiscence. Our novel functional data on Sphagnum, when considered in relation to bryophyte phylogeny, suggest the possibility that stomata first appeared in land plants as structures that facilitated sporophyte drying out before spore discharge and only subsequently acquired their role in the regulation of gaseous exchange.