Plants (land plants, embryophytes) are of monophyletic origin from a freshwater ancestor that, if still extant, would be classified among the charophycean green algae. Plants, but not charophyceans, possess a life history involving alternation of two morphologically distinct developmentally associated bodies, sporophyte and gametophyte. Body plan evolution in plants has involved fundamental changes in the forms of both gametophyte and sporophyte and the evolutionary origin of regulatory systems that generate different body plans in sporophytes and gametophytes of the same species. Comparative analysis, based on molecular phylogenetic information, identifies fundamental body plan features that originated during radiation of charophycean algae and were inherited by plants. These include, in probable evolutionary order: cellulosic cell wall, multicellular body, cytokinetic phragmoplast, plasmodesmata, apical meristematic cell, apical cell proliferation (branching), threedimensional tissues, asymmetric cell division, cell specialization capacity, zygote retention, and placenta. Body plan features whose origin is linked to the dawn of plants include: multicellular sporophyte body, histogenetic apical meristem in the gametophyte body, and capacity for tissue differentiation in both sporophyte and gametophyte. Origin of a well-defined sporophytic apical stem cell and a system for its proliferation, correlated with capacity for organ production and branching, occurred sometime between the divergence of modern bryophytes and vascular plant lineages. Roots and their meristem and a multilayered tunica-corpus shoot apical meristem arose later. Regulatory genes affecting shoot meristems, which have been detected by analysis of higher plant mutants, may be relevant to understanding early plant body plan transitions.Fundamental aspects of the plant body plan are remarkably consistent within the plant kingdom and are different from metazoans. All plants exhibit at least one form of apical meristem consisting of one or more cells that are functionally analogous to metazoan stem cells because they are histogenetic, i.e., able to generate specialized tissues. Plants differ from animals in that the plant apical meristem has the additional capability to generate organs (leaves and stem) and reproductive organ systems (cones or flowers) throughout the life of the plant, whereas the number and form of metazoan organs are embryonically determined. Plants are often described as having a ''modular construction'' that allows flexibility in organ production in response to changes in environmental conditions. Plants also differ from animals in that the plant sexual life history involves an alternation of two multicellular bodies (sporophyte and gametophyte) that are morphologically different and have changed differently through time. Thus the body plans of these two life history phases have taken separate evolutionary pathways (Fig. 1).That a simple single-celled histogenetic apical meristem (Fig. 2) appeared very early in plant evolution ...
Premise of research. The origin of land plants catalyzed key changes in Earth's atmosphere and biota. Microbial associations likely nurtured earliest plants and influenced their biogeochemical roles. Because angiosperm and animal microbiomes-bacteria, archaea, microbial eukaryotes, and genes that promote host survival-are known to display lineage effects, we hypothesized that microbiomes of early-diverging modern bryophytes and phylogenetically closely related green algae might likewise reveal commonalities reflecting ancestral traits.Methodology. New metagenomic sequence data were obtained for the late-diverging streptophyte algae Chaetosphaeridium globosum and Coleochaete pulvinata and the liverwort Conocephalum conicum, representing early-diverging land plants. New 16S rDNA amplicon sequences were acquired for the charalean Nitella tenuissima. Sequence data were used to infer bacterial genera and fungi for comparisons among streptophyte microbiota and with our published microbiome data for the outgroup chlorophyte Cladophora. To enhance evolutionary signal, taxa were sampled in the same time frame and from geographically close locales. Streptophyte metagenomic data were also probed for protein markers of significant physiological and biogeochemical functions: NifH indicating nitrogen fixation, particulate MMo indicating methane oxidation, and vitamin B 12 (cobalamin) indicating biosynthetic pathway enzymes.Pivotal results. Microbiota of studied streptophytes consistently included diverse N-fixing cyanobacteria and/or Rhizobiales, as well as methanotrophs and early-diverging fungi, and were more similar to each other than to Cladophora microbiota. Streptophyte metagenomic data indicated diverse nifH (nitrogen fixation) and pMMo (methane oxidation) marker sequences and vitamin B 12 pathway genes. Glomalean fungi occurred with Conocephalum, consistent with field studies of modern liverworts and microfossil evidence for cooccurrence of glomaleans and early land plants. Conclusions.A suite of N fixers, methanotrophs, cobalamin producers, and early-diverging fungi was consistently associated with modern streptophyte algae and bryophytes studied, suggesting features of early land plants that have played significant, previously unrecognized roles in global nitrogen and carbon cycling for hundreds of millions of years.
We have used transmission electron microscopy to examine plasmodesmata of the charophycean green alga Chara zeylanica, and of the putatively early divergent bryophytes Monoclea gottschei (liverwort), Notothylas orbicularis (hornwort), and Sphagnum fimbriatum (moss), in an attempt to learn when seed plant plasmodesmata may have originated. The three bryophytes examined have desmotubules. In addition, Monoclea was found to have branched plasmodesmata, and plasmodesmata of Sphagnum displayed densely staining regions around the neck region, as well as ring-like wall specializations. In Chara, longitudinal sections revealed endoplasmic reticulum (ER) that sometimes appeared to be associated with plasmodesmata, but this was rare, despite abundant ER at the cell periphery. Across all three fixation methods, cross-sectional views showed an internal central structure, which in some cases appeared to be connected to the plasma membrane via spoke-like structures. Plasmodesmata were present even in the incompletely formed reticulum of forming cell plates, from which we conclude that primary plasmodesmata are formed at cytokinesis in Chara zeylanica. Based on these results it appears that plasmodesmata of Chara may be less specialized than those of seed plants, and that complex plasmodesmata probably evolved in the ancestor of land plants before extant lineages of bryophytes diverged.
Although there is clear evidence for the establishment of terrestrial plant life by the end of the Ordovician, the fossil record indicates that land plants remained extremely small and structurally simple until the Late Silurian. Among the events associated with this first major radiation of land plants is the evolution of tracheids, complex water-conducting cells defined by the presence of lignified secondary cell wall thickenings. Recent palaeobotanical analyses indicate that Early Devonian tracheids appear to possess secondary cell wall thickenings composed of two distinct layers: a degradation-prone layer adjacent to the primary cell wall and a degradation-resistant (possibly lignified) layer next to the cell lumen. In order to understand better the early evolution of tracheids, developmental and comparative studies of key basal (and potentially plesiomorphic) extant vascular plants have been initiated. Ultrastructural analysis and enzyme degradation studies of wall structure (to approximate diagenetic alterations of fossil tracheid structure) have been conducted on basal members of each of the two major clades of extant vascular plants: Huperzia (Lycophytina) and Equisetum (Euphyllophytina. This research demonstrates that secondary cell walls of extant basal vascular plants include a degradation-prone layer ('template layer') and a degradation-resistant layer ('resistant layer'). This pattern of secondary cell wall formation in the water-conducting cells of extant vascular plants matches the pattern of wall thickenings in the tracheids of early fossil vascular plants and provides a key evolutionary link between tracheids of living vascular plants and those of their earliest fossil ancestors. Further studies of tracheid development and structure among basal extant vascular plants will lead to a more precise reconstruction of the early evolution of water-conducting tissues in land plants, and will add to the current limited knowledge of spatial, temporal and cytochemical aspects of cell wall formation in tracheary elements of vascular plants.
Microbialites are mineral formations formed by microbial communities that are often dominated by cyanobacteria. Carbonate microbialites, known from Proterozoic times through the present, are recognized for sequestering globally significant amounts of inorganic carbon. Recent ecological work has focused on microbial communities dominated by cyanobacteria that produce microbial mats and laminate microbialites (stromatolites). However, the taxonomic composition and functions of microbial communities that generate distinctive clotted microbialites (thrombolites) are less well understood. Here, microscopy and deep shotgun sequencing were used to characterize the microbiome (microbial taxa and their genomes) associated with a single cyanobacterial host linked by 16S sequences to Nostoc commune Vaucher ex Bornet & Flahault, which dominates abundant littoral clotted microbialites in shallow, subpolar, freshwater Laguna Larga in southern Chile. Microscopy and energy‐dispersive X‐ray spectroscopy suggested the hypothesis that adherent hollow carbonate spheres typical of the clotted microbialite begin development on the rigid curved outer surfaces of the Nostoc balls. A surface biofilm included >50 nonoxygenic bacterial genera (taxa other than Nostoc) that indicate diverse ecological functions. The Laguna Larga Nostoc microbiome included the sulfate reducers Desulfomicrobium and Sulfospirillum and genes encoding all known proteins specific to sulfate reduction, a process known to facilitate carbonate deposition by increasing pH. Sequences indicating presence of nostocalean and other types of nifH, nostocalean sulfide:ferredoxin oxidoreductase (indicating anoxygenic photosynthesis), and biosynthetic pathways for the secondary products scytonemin, mycosporine, and microviridin toxin were identified. These results allow comparisons with microbiota and microbiomes of other algae and illuminate biogeochemical roles of ancient microbialites.
Features of modern aeroterrestrial Coleochaete suggest that ancient complex streptophyte algae could grow and reproduce in moist subaerial habitats, persist through periods of desiccation, and leave behind distinctive microfossil remains.
New structural, nutritional, and stable carbon isotope data may resolve a long-standing mystery-the biological affinities of the fossil Prototaxites, the largest organism on land during the Late Silurian to Late Devonian (420-370 Ma). The tree trunk-shaped specimens, of varying dimensions but consistent tubular anatomy, first formed prior to vascular plant dominance. Hence, Prototaxites has been proposed to represent giant algae, fungi, or lichens, despite incompatible biochemical and anatomical observations. Our comparative analyses instead indicate that Prototaxites formed from partially degraded, wind-, gravity-, or water-rolled mats of mixotrophic liverworts having fungal and cyanobacterial associates, much like the modern liverwort genus Marchantia. We propose that the fossil body is largely derived from abundant, highly degradation-resistant, tubular rhizoids of marchantioid liverworts, intermixed with tubular microbial elements. Our concept explains previously puzzling fossil features and is consistent with evidence for liverworts and microbial associates in Ordovician-Devonian deposits, extensive ancient and modern marchantioid mats, and modern associations of liverworts with cyanobacteria and diverse types of fungi. Our interpretation indicates that liverworts were important components of Devonian ecosystems, that some macrofossils and microfossils previously attributed to "nematophytes" actually represent remains of ancient liverworts, and that mixotrophy and microbial associations were features of early land plants.
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