Evidence of land plant affinity for the Devonian fossil Protosalvinia (Foerstia)

The Devonian plant fossil Protosalvinia (Foerstia) has been examined by solid-state ¹³C nuclear magnetic resonance spectroscopy (NMR) and pyrolysis-gas chromatography-mass spectrometry (PY-GC-MS). Results of these studies reveal that the chemical structure of Protosalvinia is remarkably similar to that of coalified wood. A well-defined phenolic carbon peak in the NMR spectra and the appearance of phenol and alkylated phenols in pyrolysis products are clearly indicative of lignin-like compounds. These data represent significant new information on the chemical nature of Protosalvinia and provide the first substantial organic geochemical evidence for land plant affinity. ▭ Protosalvinia, Foerstia, Upper Devonian, biostratigraphy, carbon-13 NMR, PY-GC-MS, lignin.     

Orestovia and the origin of vascular plants

The enigmatic Orestovia from the Lower Devonian of Siberia has a vascular cylinder of spiral and annular tracheids, external and internal cuticles in the cortex, and stomata. Abundant spores are occasionally preserved between the cortex cuticles. The 'reticulate structures' are thyriothecia of a hemisphaeriacean fungus. Spores of several types are found sticking to the cuticle. Orestovia can be conceived as a transitional form between the alga-like Protosalvinia and the sporangiate vascular plants. The origin of land plants is discussed.     

Multigene phylogeny of land plants with special reference to bryophytes and the earliest land plants

A widely held view of land plant relationships places liverworts as the first branch of the land plant tree, whereas some molecular analyses and a cladistic study of morphological characters indicate that hornworts are the earliest land plants. To help resolve this conflict, we used parsimony and likelihood methods to analyze a 6, 095-character data set composed of four genes (chloroplast rbcL and small-subunit rDNA from all three plant genomes) from all major land plant lineages. In all analyses, significant support was obtained for the monophyly of vascular plants, lycophytes, ferns (including PSILOTUM: and EQUISETUM:), seed plants, and angiosperms. Relationships among the three bryophyte lineages were unresolved in parsimony analyses in which all positions were included and weighted equally. However, in parsimony and likelihood analyses in which rbcL third-codon-position transitions were either excluded or downweighted (due to apparent saturation), hornworts were placed as sister to all other land plants, with mosses and liverworts jointly forming the second deepest lineage. Decay analyses and Kishino-Hasegawa tests of the third-position-excluded data set showed significant support for the hornwort-basal topology over several alternative topologies, including the commonly cited liverwort-basal topology. Among the four genes used, mitochondrial small-subunit rDNA showed the lowest homoplasy and alone recovered essentially the same topology as the multigene tree. This molecular phylogeny presents new opportunities to assess paleontological evidence and morphological innovations that occurred during the early evolution of terrestrial plants.     

Phylogeny of early land plants: insights from genes and genomes

A large body of evidence from molecular systematic studies has confirmed the charophytic origin of land plants, and clarified monophyly of many lineages in charophytes and land plants. These studies have also identified liverworts as the earliest land plants, and the lycopods as the extant sister group to all other vascular plants. Two traditionally defined groups-bryophytes and pteridophytes-are now recognized as early grades of land plant evolution. However, several problems that complicate the use of sequence data in reconstructing plant phylogeny have become apparent; reconstruction of an accurate land plant phylogeny will require analysis of sequences of multiple genes and genomic structural characters of all three genomes.     

Early vascular land plants: proof and conjecture

Megafossil evidence does not fill the 'evolutionary gap' between land plants and their hypothetical green algal ancestors. Rare Late Silurian vascular plant megafossils provide little information about the morphological, physiological, biochemical, and ecological steps that preceded their evolution. Dissociated trilete spores, spore tetrads, cuticle- and tracheid-like structures far exceed the abundance and diversity of Silurian vascular plant megafossils, and appear millions of years before them. In reference to whole-bodied organisms, these or analogous structures belong to land plants or emergent aquatics; they may represent plants evolutionarily intermediate between green algae and descendent vascular plants at the bryophyte or pre-bryophyte stages. Changes in the cellular biochemistry of pre-Devonian land plants in response to the selective pressures of terrestrial life may have led to the origin of lignin and cutin, neither of which has any counterpart among the algae, and to the evolutionary surge of the vascular plants in the Early Devonian represented by the plant megafossil record. Positive correlation between abundance and diversity of trilete spores and shallow-water, nearshore sites reinforces conclusions based on morphology that a terrestrial flora existed well prior to the appearance of vascular plant megafossils.     

A feeling for the superorganism: expression of plant form in the lichen thallus

The composite thalli produced by lichen fungi in symbiosis with algae often show structural convergences with plants. Similar overall thallus forms and branching patterns may arise in lichens with very different anatomical construction, indicating the autonomy of the morphological level of organization. Fungal and algal growth and division may be highly integrated within meristem-like morphogenetic zones in many lichens, whereas in others the symbionts may contribute in a less synchronized fashion to the construction of the thallus. Although thallus-level morphology and morphogenesis may be compared with those of plants, ontogeny of the lichen thallus differs fundamentally. Observations of lichen ontogeny illustrate the formation of the thallus by unification of autonomous, primary cellular elements in co-ordinated growth. In land plants and many algae, by contrast, the plant body is the primary structure, the cellular elements of which represent secondary subdivisions. The convergences in form are based on a common mode of nutrition in combination with cell-wall building materials that impart similar structural potential. The photosynthetic apparatus forming the basis of this mode of nutrition is not a convergent feature, however, but a homologous structure that originated in the cyanobacteria and subsequently passed laterally into diverse biological lineages by repeated endosymbioses. With consolidation of these symbioses as eukaryotic algae and plants, the organismal level of organization was repeatedly re-established with increasing degrees of complexity, and morphological convergences were expressed at these new levels. In lichens, by contrast, the symbiosis is not organismally consolidated; morphological expression instead emerges at the superorganismal level.  © 2006 The Linnean Society of London, Botanical Journal of the Linnean Society , 2006, 150 , 89–99.     

How plants conquered land: evolution of terrestrial adaptation

The transition of plants from water to land is considered one of the most significant events in the evolution of life on Earth. The colonization of land by plants, accompanied by their morphological, physiological and developmental changes, resulted in plant biodiversity. Besides significantly influencing oxygen levels in the air and on land, plants manufacture organic matter from CO₂ and water with the help of sunlight, paving the way for the diversification of nonplant lineages ranging from microscopic organisms to animals. Land plants regulate the climate by adjusting total biomass and energy flow. At the genetic level, these innovations are achieved through the rearrangement of pre-existing genetic information. Advances in genome sequencing technology are revamping our understanding of plant evolution. This study highlights the morphological and genomic innovations that allow plants to integrate life on Earth.     

Chemotaxonomy of some Paleozoic vascular plants. Part I: Chemical compositions and preliminary cluster analyses

The chemical compositions of plant fossils having trimerophyte (Pertica,Psilophyton princeps, P. cf.jorbesii), rhyniophyte (Taeniocrada), and zosterophyll (Sawdonia) morphological characteristics are chemically analyzed and chemotaxonomically related to vascular ( ?Eohostimella, Renalia, Chahuria) and putative non-vascular plant fossils (Botryococcus, Parka, Pachytheca, Prototaxites,Nematothallus, Spongiophyton, Protosalvinia, Orestovia) whose taxonomic affinities are unknown or speculative. Separation of the material examined into clusters representing higher taxa (i.e., algal, nonalgal, trimerophyte, rhyniophyte, zosterophyll plant groupings) is effected by the weighting of chemical data during cluster analyses. The weighting of phenolic and monohydroxycarboxylic acid constituents is shown to cluster vascular plant material, while the criteria of carbon chainlength ranges and maxima separate vascular from non-vascular plant fossils. Multivariate analysis of the data, using chemical and geological factors, results in the clustering of four groups: (1)Botryococcus, Parka, Pachytheca, (2)Spongiophyton, Prototaxites, Nematothallus, Orestovia, (3)Eohostimella,Taeniocrada, Renalia, and (4)Psilophyton spp.,Pertica, Chaleuria. Sawdonia andProtosalvinia appear as data points showing no observable affinity with any of the above fossils.Protosalvinia, Renalia, andChaleuria are interpreted as being chemotaxonomically intermediate. These data are interpreted as indicating taxonomic affinities on a very broad scale ; possible evolutionary trends in specific chemical compounds, as they relate to vascular and non-vascular plant geochemistry, are discussed.     

The relationships of vascular plants

Recent phylogenetic research indicates that vascular plants evolved from bryophyte-like ancestors and that this involved extensive modifications to the life cycle. These conclusions are supported by a range of systematic data, including gene sequences, as well as evidence from comparative morphology and the fossil record. Within vascular plants, there is compelling evidence for two major clades, which have been termed lycophytes (clubmosses) and euphyllophytes (seed plants, ferns, horsetails). The implications of recent phylogenetic work are discussed with reference to life cycle evolution and the interpretation of stratigraphic inconsistencies in the early fossil record of land plants. Life cycles are shown to have passed through an isomorphic phase in the early stages of vascular plant evolution. Thus, the gametophyte generation of all living vascular plants is the product of massive morphological reduction. Phylogenetic research corroborates earlier suggestions of a major representational bias in the early fossil record. Mega-fossils document a sequence of appearance of groups that is at odds with that predicted by cladogram topology. It is argued here that the pattern of appearance and diversification of plant megafossils owes more to changing geological conditions than to rapid biological diversification.     

Current range condition in relation to land management systems in semi-arid savannas of Swaziland

Rangeland condition was assessed in the lowveld of Swaziland to determine the current status with emphasis on contrasting different land management systems and soil classes in two study areas. The assessment incorporated the grass and woody plant layer. The methods employed to evaluate the grass layer were ecological condition index (ECI) and weighted palatability composition (WPC). The government ranch had significantly higher ECI (mean 714.5) and WPC (mean 61) than the communal land (mean: ECI – 533.5; WPC – 48.7) and the game reserve (mean: ECI – 578.9; WPC – 47.9). The ECI and WPC values did not differ between the soil classes in most cases (range: ECI 551.5–645.9 and WPC – 43.7–57.6). The density of all woody plants and encroaching plants alone were the highest in communal land. Basal cover ranged from poor (2–3%) to good (>5%), while bare ground was rated from low (<1%) to high (>5%). Overall results showed great variability of studied variables at site and landscape levels of resolution. Generally, the grass layer was rated between fair and good when assessed on the basis of ecological and palatability merits. There was a clear indication of advancement of bush encroachment.     

Chemotaxonomy of Prototaxites and evidence for possible terrestrial adaptation

Silicified and carbonized axes of Prototaxites are chemically analyzed by means of X-ray and organic-extraction techniques. The isolation and identification of cutin and suberin derivatives, i.e., ω-hydroxymonocarboxylic acids, suggest that Prototaxites may have been a terrestrial plant or an aquatic plant showing chemical adaptation to periods of desiccation. Normal saturated acids showing no odd or even carbon-number predominance, phenyl and naphthyl aromatic acids, and normal and aromatic dicarboxylic acids isolated from fossil material, are considered inconsistent with an algal biochemistry. The normal saturated fatty acids isolated from Parka, Pachytheca, Spongiophyton, Protosalvinia, Orestovia and Taeniocrada are compared with Prototaxites. Parka, Pachytheca, Spongiophyton and Orestovia, parallel one another in their organic chemical constituents, while Protosalvinia, Taeniocrada and Prototaxites appear to have paralleled one another in their adaptation to a terrestrial habit.     

ACTIN GENE DUPLICATION AND THE EVOLUTION OF MORPHOLOGICAL COMPLEXITY IN LAND PLANTS

Actin is a highly conserved cytoskeletal protein that is a key component of cells. Genes encoding actin occur in single copies in most green algae, in 2–3 copies in bryophytes, and in increasingly more complex gene families in ferns and seed plants. We use the well-resolved phylogenetic frameworks of the Streptophyta as a guide to reconstruct the patterns of actin gene duplication in early diverging land plants. Our working hypothesis is that the origin of novel tissues in the bryophytes (e.g. multicellular sporophyte) may be reflected in the functional diversification of duplicate actin genes in these taxa. Actin is used as a model cytoskeletal protein with the assumption that its evolutionary history represents those of other cytoskeletal elements and the coevolved binding proteins. Here we provide a phylogenetic perspective on the origin of green algal and land plant actin genes and use this information to speculate on the role of plant actin in early plant evolution.     

Microfossils and evidence of land plant evolution

Resolving the question of (1) land plant and (2) vascular land plant evolution is a complex problem. It requires a continued, multidisciplinary effort. We are all grateful to Dianne Edwards and her colleagues (Edwards et al. 1979) for pursuing one such line of research with careful attention to morphology and stratigraphy. Their efforts, however, are confined to one small part of the globe, and they perforce involve only one type of evidence effective with regard to questions of vascular plant evolution once the land estate has been reached. They do not deal with the basic question of vascular and non-vascular land plant origins. The so-called Přídolí benchmark that remained the sine qua nun for vascular plant evolution when Dianne Edwards began her studies has now been irrevocably breached. What other supposedly sacrosanct benchmarks will also crumble as the result of future discoveries, now that vascular plants have been recovered from lower Ludlovian strata? Nevertheless, pre-Devonian plant megafossils are too rare to yield definitive results with regard to the origin of land plants prior to the vascular estate, even though they could in principle (as emphasized by Edwards et al. 1979) provide the least ambiguous evidence. We must look elsewhere than to megafossils for evidence suggesting links in time between green algal ancestors, major groups of living green land Plants, and the many extinct groups of enigmatic higher land plants in the crucial Early Paleozoic time interval.     

Homologous Versus Antithetic Alternation of Generations and the Origin of Sporophytes

The late-nineteenth/early-twentieth century debate over homologous versus antithetic alternation of generations is reviewed. Supporters of both theories, at first, used Coleochaete as a model for the origin of land-plant life cycles. The early debate focused on the morphological interpretation of the sporophyte and on whether vascular cryptogams had bryophyte-like ancestors. The terms of the debate shifted after the discovery that the alternation of morphological generations was accompanied by an alternation of chromosome number. Supporters of homologous alternation now promoted a model in which land plants had been derived from an algal ancestor with an isomorphic alternation of haploid and diploid generations whereas supporters of antithetic alternation favored a model in which land plants were derived from a haploid algal ancestor with zygotic meiosis. Modern evidence that embryophytes are derived from charophycean green algae is more compatible with an updated version of the antithetic theory.     

Evolution of developmental mechanisms in plants

As our understanding of developmental mechanisms in flowering plant species has become more advanced, an appreciation of the need to understand how distinct plant morphologies are generated has grown. This has led to an awareness of the key morphological differences in distinct land plant groups and to an assessment of the major innovations that occurred during land plant evolution. Recent advances demonstrate how developmental toolkits have been recruited for related purposes in different land plant groups, but the limited number of examples highlights both the infancy of the field and the difficulty of working with non-flowering plants.     

The evolution of vegetative desiccation tolerance in land plants

Vegetative desiccation tolerance is a widespread but uncommon occurrence in the plant kingdom generally. The majority of vegetative desiccation-tolerant plants are found in the less complex clades that constitute the algae, lichens and bryophytes. However, within the larger and more complex groups of vascular land plants there are some 60 to 70 species of ferns and fern allies, and approximately 60 species of angiosperms that exhibit some degree of vegetative desiccation tolerance. In this report we analyze the evidence for the differing mechanisms of desiccation tolerance in different plants, including differences in cellular protection and cellular repair, and couple this evidence with a phylogenetic framework to generate a working hypothesis as to the evolution of desiccation tolerance in land plants. We hypothesize that the initial evolution of vegetative desiccation tolerance was a crucial step in the colonization of the land by primitive plants from an origin in fresh water. The primitive mechanism of tolerance probably involved constitutive cellular protection coupled with active cellular repair, similar to that described for modern-day desiccation-tolerant bryophytes. As plant species evolved, vegetative desiccation tolerance was lost as increased growth rates, structural and morphological complexity, and mechanisms that conserve water within the plant and maintain efficient carbon fixation were selected for. Genes that had evolved for cellular protection and repair were, in all likelihood, recruited for different but related processes such as response to water stress and the desiccation tolerance of reproductive propagules. We thus hypothesize that the mechanism of desiccation tolerance exhibited in seeds, a developmentally induced cellular protection system, evolved from the primitive form of vegetative desiccation tolerance. Once established in seeds, this system became available for induction in vegetative tissues by environmental cues related to drying. The more recent, modified vegetative desiccation tolerance mechanism in angiosperms evolved from that programmed into seed development as species spread into very arid environments. Most recently, certain desiccation-tolerant monocots evolved the strategy of poikilochlorophylly to survive and compete in marginal habitats with variability in water availability.     

Plant microtubule studies: past and present

Here, I briefly review historical and morphological aspects of plant microtubule studies in land plants. Microtubules are formed from tubulins, and the polymeric configurations appear as singlet, doublet, and triplet microtubules. Doublet microtubules occur in the axoneme of cilia and flagella, and triplet microtubules occur in the basal bodies and centrosomes. Doublet and triplet microtubules are lost in all angiosperms and some gymnosperms that do not possess flagellated sperm. In land plants with flagellated sperm, centriolar centrosomes transform into basal bodies during spermatogenesis. In flowering plants, however, most male gametes (sperm) are conveyed to eggs without the benefit of cilia or flagella; thus, higher plants lack centriolar centrosome and doublet and triplet microtubules. The loss of centriolar centrosomes from the life cycle of flowering plants may have influenced the evolution of the plant microtubule system. Comparison of mitotic apparatuses in basal land plants and flowering plants illuminates the evolutionary transition from the centriolar microtubule system to the acentriolar microtubule system.     

Evolution of land plants: insights from molecular studies on basal lineages

The invasion of the land by plants, or terrestrialization, was one of the most critical events in the history of the Earth. The evolution of land plants included significant transformations in body plans: the emergence of a multicellular diploid sporophyte, transition from gametophyte-dominant to sporophyte-dominant life histories, and development of many specialized tissues and organs, such as stomata, vascular tissues, roots, leaves, seeds, and flowers. Recent advances in molecular genetics in two model basal plants, bryophytes Physcomitrella patens and Marchantia polymorpha, have begun to provide answers to several key questions regarding land plant evolution. This paper discusses the evolution of the genes and regulatory mechanisms that helped drive such significant morphological innovations among land-based plants.