scholarly journals Evolutionary dynamics of mycorrhizal symbiosis in land plant diversification

2017 ◽  
Author(s):  
Frida A.A. Feijen ◽  
Rutger A. Vos ◽  
Jorinde Nuytinck ◽  
Vincent S.F.T. Merckx
Keyword(s):  
Soil Fungi ◽  
Evolutionary Dynamics ◽  
State Transition ◽  
Land Plant ◽  
Land Plants ◽  
Mycorrhizal Symbiosis ◽  
Large Species ◽  
Mycorrhizal Associations ◽  
Colonization Of Land ◽  
Early Land

Mycorrhizal symbiosis between soil fungi and land plants is one of the most widespread and ecologically important mutualisms on earth. It has long been hypothesized that the Glomeromycotina, the mycorrhizal symbionts of the majority of plants, facilitated colonization of land by plants in the Ordovician. This view was recently challenged by the discovery of mycorrhizal associations with Mucoromycotina in several early diverging lineages of land plants. Utilizing a large, species-level database of plants’ mycorrhizal associations and a Bayesian approach to state transition dynamics we here show that the recruitment of Mucoromycotina is the best supported transition from a non-mycorrhizal state. We further found that transitions between different combinations of either or both of Mucoromycotina and Glomeromycotina occur at high rates and found similar promiscuity among combinations that include either or both of Glomeromycotina and Ascomycota with a nearly fixed association with Basidiomycota. Our results demonstrate that under the most likely scenario symbiosis with Mucoromycotina enabled the establishment of early land plants.

scholarly journals Algal ancestor of land plants was preadapted for symbiosis

2015 ◽  
Vol 112 (43) ◽  
pp. 13390-13395 ◽  
Author(s):  
Pierre-Marc Delaux ◽  
Guru V. Radhakrishnan ◽  
Dhileepkumar Jayaraman ◽  
Jitender Cheema ◽  
Mathilde Malbreil ◽  
...  
Keyword(s):  
Root Colonization ◽  
Land Plant ◽  
Land Plants ◽  
Recent Common Ancestor ◽  
Mycorrhizal Symbiosis ◽  
Specific Expression ◽  
Symbiotic Associations ◽  
Most Recent Common Ancestor ◽  
Green Algal ◽  
Colonization Of Land

Colonization of land by plants was a major transition on Earth, but the developmental and genetic innovations required for this transition remain unknown. Physiological studies and the fossil record strongly suggest that the ability of the first land plants to form symbiotic associations with beneficial fungi was one of these critical innovations. In angiosperms, genes required for the perception and transduction of diffusible fungal signals for root colonization and for nutrient exchange have been characterized. However, the origin of these genes and their potential correlation with land colonization remain elusive. A comprehensive phylogenetic analysis of 259 transcriptomes and 10 green algal and basal land plant genomes, coupled with the characterization of the evolutionary path leading to the appearance of a key regulator, a calcium- and calmodulin-dependent protein kinase, showed that the symbiotic signaling pathway predated the first land plants. In contrast, downstream genes required for root colonization and their specific expression pattern probably appeared subsequent to the colonization of land. We conclude that the most recent common ancestor of extant land plants and green algae was preadapted for symbiotic associations. Subsequent improvement of this precursor stage in early land plants through rounds of gene duplication led to the acquisition of additional pathways and the ability to form a fully functional arbuscular mycorrhizal symbiosis.

Age of the Cedarberg Formation, South Africa and early land plant evolution

1986 ◽  
Vol 123 (4) ◽  
pp. 445-454 ◽  
Author(s):  
J. Gray ◽  
J. N. Theron ◽  
A. J. Boucot
Keyword(s):  
South Africa ◽  
Land Plant ◽  
Plant Evolution ◽  
Marine Phytoplankton ◽  
Land Plants ◽  
Table Mountain ◽  
Plant Remains ◽  
First Occurrence ◽  
Land Plant Evolution ◽  
Early Land

AbstractThe first occurrence of Early Paleozoic land plants is reported from South Africa. The plant remains are small, compact tetrahedral spore tetrads. They occur abundantly in the Soom Shale Member of the Cedarberg Formation, Table Mountain Group. Marine? phytoplankton (sphaeromorphs or leiospheres) occur with the spore tetrads in all samples. Rare chitinozoans are found in half the samples. Together with similar spore tetrads from the Paraná Basin (Gray et al. 1985) these are the first well-documented records of Ashgill and/or earlier Llandovery land plants from the Malvinokaffric Realm, and from the African continent south of Libya. These spore tetrads have botanical, evolutionary, and biogeographic significance. Their size in comparison with spore tetrads from stratigraphic sections throughout eastern North America, suggests that an earliest Llandovery age is more probable for the Soom Shale Member, although a latest Ordovician age cannot be discounted. The age of the brachiopods in the overlying Disa Siltstone Member has been in contention for over a decade. Both Ashgillian and Early Llandovery ages have been proposed. The age of the underlying Soom Shale Member based on plant spores and trilobites (earliest Llandovery or latest Ashgillian) suggests that the Disa Siltstone Member is also likely to be of Early Llandovery age, although the distance between the Soom Shale Member spore-bearing locality and rocks to the south yielding abundant invertebrate body fossils at one locality is great enough to permit diachroneity.

scholarly journals Vegetative and reproductive innovations of early land plants: implications for a unified phylogeny

2000 ◽  
Vol 355 (1398) ◽  
pp. 769-793 ◽  
Author(s):  
Karen Sue Renzaglia ◽  
R. Joel Duff ◽  
Daniel L. Nickrent ◽  
David J. Garbary
Keyword(s):  
Phylogenetic Signal ◽  
Phenotypic Variability ◽  
Land Plant ◽  
Land Plants ◽  
Total Evidence ◽  
Data Sets ◽  
Data Set ◽  
Plant Phylogeny ◽  
Male Gametes ◽  
Early Land

As the oldest extant lineages of land plants, bryophytes provide a living laboratory in which to evaluate morphological adaptations associated with early land existence. In this paper we examine reproductive and structural innovations in the gametophyte and sporophyte generations of hornworts, liverworts, mosses and basal pteridophytes. Reproductive features relating to spermatogenesis and the architecture of motile male gametes are overviewed and evaluated from an evolutionary perspective. Phylogenetic analyses of a data set derived from spermatogenesis and one derived from comprehensive morphogenetic data are compared with a molecular analysis of nuclear and mitochondrial small subunit rDNA sequences. Although relatively small because of a reliance on water for sexual reproduction, gametophytes of bryophytes are the most elaborate of those produced by any land plant. Phenotypic variability in gametophytic habit ranges from leafy to thalloid forms with the greatest diversity exhibited by hepatics. Appendages, including leaves, slime papillae and hairs, predominate in liverworts and mosses, while hornwort gametophytes are strictly thalloid with no organized external structures. Internalization of reproductive and vegetative structures within mucilage–filled spaces is an adaptive strategy exhibited by hornworts. The formative stages of gametangial development are similar in the three bryophyte groups, with the exception that in mosses apical growth is intercalated into early organogenesis, a feature echoed in moss sporophyte ontogeny. A monosporangiate, unbranched sporophyte typifies bryophytes, but developmental and structural innovations suggest the three bryophyte groups diverged prior to elaboration of this generation. Sporophyte morphogenesis in hornworts involves non–synchronized sporogenesis and the continued elongation of the single sporangium, features unique among archegoniates. In hepatics, elongation of the sporophyte seta and archegoniophore is rapid and requires instantaneous wall expandability and hydrostatic support. Unicellular, spiralled elaters and capsule dehiscence through the formation of four regular valves are autapomorphies of liverworts. Sporophytic sophistications in the moss clade include conducting tissue, stomata, an assimilative layer and an elaborate peristome for extended spore dispersal. Characters such as stomata and conducting cells that are shared among sporophytes of mosses, hornworts and pteridophytes are interpreted as parallelisms and not homologies. Our phylogenetic analysis of three different data sets is the most comprehensive to date and points to a single phylogenetic solution for the evolution of basal embryophytes. Hornworts are supported as the earliest divergent embryophyte clade with a moss/liverwort clade sister to tracheophytes. Among pteridophytes, lycophytes are monophyletic and an assemblage containing ferns, Equisetum and psilophytes is sister to seed plants. Congruence between morphological and molecular hypotheses indicates that these data sets are tracking the same phylogenetic signal and reinforces our phylogenetic conclusions. It appears that total evidence approaches are valuable in resolving ancient radiations such as those characterizing the evolution of early embryophytes. More information on land plant phylogeny can be found at: http://www.science.siu.edu/landplants/index.html.

scholarly journals The dawn of symbiosis between plants and fungi

2011 ◽  
Vol 7 (4) ◽  
pp. 574-577 ◽  
Author(s):  
Martin I. Bidartondo ◽  
David J. Read ◽  
James M. Trappe ◽  
Vincent Merckx ◽  
Roberto Ligrone ◽  
...  
Keyword(s):  
Vascular Plant ◽  
Land Plants ◽  
Evolutionary Trees ◽  
Early Devonian ◽  
Present Evidence ◽  
Plant Fossils ◽  
Biological Innovations ◽  
New Hypothesis ◽  
Colonization Of Land ◽  
Early Land

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.

scholarly journals The timescale of early land plant evolution

2018 ◽  
Vol 115 (10) ◽  
pp. E2274-E2283 ◽  
Author(s):  
Jennifer L. Morris ◽  
Mark N. Puttick ◽  
James W. Clark ◽  
Dianne Edwards ◽  
Paul Kenrick ◽  
...  
Keyword(s):  
Molecular Clock ◽  
Fossil Record ◽  
Land Plant ◽  
Plant Evolution ◽  
Land Plants ◽  
Early Land Plant ◽  
Land Plant Evolution ◽  
The Impact ◽  
Earth’S System ◽  
Early Land

Establishing the timescale of early land plant evolution is essential for testing hypotheses on the coevolution of land plants and Earth’s System. The sparseness of early land plant megafossils and stratigraphic controls on their distribution make the fossil record an unreliable guide, leaving only the molecular clock. However, the application of molecular clock methodology is challenged by the current impasse in attempts to resolve the evolutionary relationships among the living bryophytes and tracheophytes. Here, we establish a timescale for early land plant evolution that integrates over topological uncertainty by exploring the impact of competing hypotheses on bryophyte−tracheophyte relationships, among other variables, on divergence time estimation. We codify 37 fossil calibrations for Viridiplantae following best practice. We apply these calibrations in a Bayesian relaxed molecular clock analysis of a phylogenomic dataset encompassing the diversity of Embryophyta and their relatives within Viridiplantae. Topology and dataset sizes have little impact on age estimates, with greater differences among alternative clock models and calibration strategies. For all analyses, a Cambrian origin of Embryophyta is recovered with highest probability. The estimated ages for crown tracheophytes range from Late Ordovician to late Silurian. This timescale implies an early establishment of terrestrial ecosystems by land plants that is in close accord with recent estimates for the origin of terrestrial animal lineages. Biogeochemical models that are constrained by the fossil record of early land plants, or attempt to explain their impact, must consider the implications of a much earlier, middle Cambrian–Early Ordovician, origin.

scholarly journals Evolutionary dynamics of mycorrhizal symbiosis in land plant diversification

2018 ◽  
Vol 8 (1) ◽  
Author(s):  
Frida A. A. Feijen ◽  
Rutger A. Vos ◽  
Jorinde Nuytinck ◽  
Vincent S. F. T. Merckx
Keyword(s):  
Evolutionary Dynamics ◽  
Land Plant ◽  
Mycorrhizal Symbiosis ◽  
Plant Diversification

scholarly journals The microfossil record of early land plants

2000 ◽  
Vol 355 (1398) ◽  
pp. 717-732 ◽  
Author(s):  
Charles H. Wellman ◽  
Jane Gray
Keyword(s):  
Fossil Record ◽  
Vascular Plants ◽  
Major Change ◽  
Land Plant ◽  
Land Plants ◽  
Early Land Plant ◽  
Early Late ◽  
Early Land ◽  
Lines Of Evidence ◽  
Plant Microfossil

Dispersed microfossils (spores and phytodebris) provide the earliest evidence for land plants. They are first reported from the Llanvirn (Mid–Ordovician). More or less identical assemblages occur from the Llanvirn (Mid–Ordovician) to the late Llandovery (Early Silurian), suggesting a period of relative stasis some 40 Myr in duration. Various lines of evidence suggest that these early dispersed microfossils derive from parent plants that were bryophyte–like if not in fact bryophytes. In the late Llandovery (late Early Silurian) there was a major change in the nature of dispersed spore assemblages as the separated products of dyads (hilate monads) and tetrads (trilete spores) became relatively abundant. The inception of trilete spores probably represents the appearance of vascular plants or their immediate progenitors. A little later in time, in the Wenlock (early Late Silurian), the earliest unequivocal land plant megafossils occur. They are represented by rhyniophytoids. It is only from the Late Silurian onwards that the microfossil / megafossil record can be integrated and utilized in interpretation of the flora. Dispersed microfossils are preserved in vast numbers, in a variety of environments, and have a reasonable spatial and temporal fossil record. The fossil record of plant megafossils by comparison is poor and biased, with only a dozen or so known pre–Devonian assemblages. In this paper, the early land plant microfossil record, and its interpretation, are reviewed. New discoveries, novel techniques and fresh lines of inquiry are outlined and discussed.

Morphometric analysis of Rhynia and Asteroxylon: testing functional aspects of early land plant evolution

Paleobiology ◽  
2000 ◽  
Vol 26 (3) ◽  
pp. 405-418 ◽  
Author(s):  
A. Roth-Nebelsick ◽  
G. Grimm ◽  
V. Mosbrugger ◽  
H. Hass ◽  
H. Kerp
Keyword(s):  
Water Transport ◽  
Land Plant ◽  
Plant Evolution ◽  
Cross Sectional Area ◽  
Land Plants ◽  
Limiting Factor ◽  
Vascular Bundles ◽  
Sectional Area ◽  
Cross Sectional ◽  
Early Land

New morphometric data gathered from cross-sections of two Lower Devonian land plants (Rhynia gwynne-vaughanii and Asteroxylon mackiei) are interpreted in terms of the evolution of the function of vascular bundles in early land plants. The following conclusions can be drawn from these new data: (1) The ratio of the cross-sectional area of the xylem (representing the conducting volume supplying the axis with water) to the xylem perimeter (representing the “contact area” between xylem and parenchyma through which water leaves the xylem and enters the parenchyma) is not constant for Rhynia axes, almost constant for Asteroxylon axes, and different between Rhynia and Asteroxylon. Thus, Bowers hypothesis that the ratio of cross-sectional area of the xylem to xylem perimeter is constant during ontogenetic development is true for Asteroxylon. That this ratio is constant during phylogeny, however, is not supported by our data. (2) The ratio between cross-sectional area of xylem to parenchyma is higher in Asteroxylon than in Rhynia. (3) As predicted by previous computer simulations, the ratio of the xylem perimeter to the axis perimeter plays a major role in determining water transport performance of the transpiring axis. This ratio is constant within ontogeny but is different in Asteroxylon and Rhynia. In Asteroxylon axes, this ratio is about twice as large as in Rhynia axes. (4) Contrary to the expectations, the distance between the outermost layer of the xylem and the transpiring surface, which represents the low-conductivity pathway through the parenchyma, appears not to be a limiting factor for the water transport in axes of Rhynia and Asteroxylon. (5) From the analysis of the geometric parameters, it is evident that Rhynia and Asteroxylon with their distinct stelar geometries represent two different constructional types for which no transitional stages are known.

Computer simulations of early land plant branching morphologies: canalization of patterns during evolution?

Paleobiology ◽  
1982 ◽  
Vol 8 (3) ◽  
pp. 196-210 ◽  
Author(s):  
Karl J. Niklas
Keyword(s):  
Computer Simulations ◽  
Mechanical Design ◽  
Vegetative Reproduction ◽  
Land Plant ◽  
Land Plants ◽  
Fossil Plants ◽  
Early Land Plant ◽  
Plant Groups ◽  
Branching Patterns ◽  
Early Land

Using computer simulations and a quantitative method for describing bifurcating structures, the morphology of branching patterns seen in early land plants is analyzed. Four types or models of random branching (regular, geometric, binomial, and poisson) are shown to adequately describe the range of observed branching in most early land plants. Approximately 57% of all randomly generated computer patterns show reiterative branching events (=three successive identical modes of branching). Artificial canalization of reiterative events results in branching patterns structurally analogous with that of ancient fossil plants. Simulated phylogenetic changes among early land plant lineages, based on parsimonious transitions in branching patterns, indicate that most observed trends can be related directly to those seen in randomly generating branching patterns in which “size” is increased. The trimerophyte to progymnosperm trend in changing branching patterns is an exception, since the binomial model describing the progymnosperms has not been simulated by random processes.While the apparent phylogenetic changes among early land plant groups do not require deterministic explanations, the transition from regular to geometric branching and the “canalization” of reiterative branching patterns may represent a grade level response to selective pressures related to mechanical design and vegetative reproduction.

scholarly journals Constraining the role of early land plants in Palaeozoic weathering and global cooling

2015 ◽  
Vol 282 (1813) ◽  
pp. 20151115 ◽  
Author(s):  
Joe Quirk ◽  
Jonathan R. Leake ◽  
David A. Johnson ◽  
Lyla L. Taylor ◽  
Loredana Saccone ◽  
...  
Keyword(s):  
Arbuscular Mycorrhizal ◽  
Am Fungi ◽  
Land Plant ◽  
Network Size ◽  
Mineral Weathering ◽  
Land Plants ◽  
Tree Roots ◽  
Plant Fossils ◽  
Terrestrial Environments ◽  
Early Land

How the colonization of terrestrial environments by early land plants over 400 Ma influenced rock weathering, the biogeochemical cycling of carbon and phosphorus, and climate in the Palaeozoic is uncertain. Here we show experimentally that mineral weathering by liverworts—an extant lineage of early land plants—partnering arbuscular mycorrhizal (AM) fungi, like those in 410 Ma-old early land plant fossils, amplified calcium weathering from basalt grains threefold to sevenfold, relative to plant-free controls. Phosphate weathering by mycorrhizal liverworts was amplified 9–13-fold over plant-free controls, compared with fivefold to sevenfold amplification by liverworts lacking fungal symbionts. Etching and trenching of phyllosilicate minerals increased with AM fungal network size and atmospheric CO 2 concentration. Integration of grain-scale weathering rates over the depths of liverwort rhizoids and mycelia (0.1 m), or tree roots and mycelia (0.75 m), indicate early land plants with shallow anchorage systems were probably at least 10-fold less effective at enhancing the total weathering flux than later-evolving trees. This work challenges the suggestion that early land plants significantly enhanced total weathering and land-to-ocean fluxes of calcium and phosphorus, which have been proposed as a trigger for transient dramatic atmospheric CO 2 sequestration and glaciations in the Ordovician.

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