Summary Here, the coevolution of mycorrhizal fungi and roots is assessed in the light of evidence now available, from palaeobotanical and morphological studies and the analysis of DNA-based phylogenies. The first bryophyte-like land plants, in the early Devonian (400 million years ago), had endophytic associations resembling vesicular‐ arbuscular mycorrhizas (VAM) even before roots evolved. Mycorrhizal evolution would have progressed from endophytic hyphae towards balanced associations where partners were interdependent due to the exchange of limiting energy and nutrient resources. Most mycorrhizas are mutualistic, but in some cases the trend for increasing plant control of fungi culminates in the exploitative mycorrhizas of achlorophyllous, mycoheterotrophic plants. Ectomycorrhizal, ericoid and orchid mycorrhizas, as well as nonmycorrhizal roots, evolved during the period of rapid angiosperm radiation in the Cretaceous. It is hypothesised that roots gradually evolved from rhizomes to provide more suitable habitats for mycorrhizal fungi and provide plants with complex branching and leaves with water and nutrients. Selection pressures have caused the morphological divergence of roots with different types of mycorrizas. Root cortex thickness and exodermis suberization are greatest in obligately mycorrhizal plants, while nonmycorrhizal plants tend to have fine roots, with more roots hairs and relatively advanced chemical defences. Major coevolutionary trends and the relative success of plants with different root types are discussed.

Coevolution of roots and mycorrhizas of land plants

The origin and early evolution of land plants in the mid-Palaeozoic era, between about 480 and 360 million years ago, was an important event in the history of life, with far-reaching consequences for the evolution of terrestrial organisms and global environments. A recent surge of interest, catalysed by palaeobotanical discoveries and advances in the systematics of living plants, provides a revised perspective on the evolution of early land plants and suggests new directions for future research.

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The origin and early evolution of plants on land

Reconstructing the origin and evolution of land plants and their algal relatives is a fundamental problem in plant phylogenetics, and is essential for understanding how critical adaptations arose, including the embryo, vascular tissue, seeds, and flowers. Despite advances in molecular systematics, some hypotheses of relationships remain weakly resolved. Inferring deep phylogenies with bouts of rapid diversification can be problematic; however, genome-scale data should significantly increase the number of informative characters for analyses. Recent phylogenomic reconstructions focused on the major divergences of plants have resulted in promising but inconsistent results. One limitation is sparse taxon sampling, likely resulting from the difficulty and cost of data generation. To address this limitation, transcriptome data for 92 streptophyte taxa were generated and analyzed along with 11 published plant genome sequences. Phylogenetic reconstructions were conducted using up to 852 nuclear genes and 1,701,170 aligned sites. Sixty-nine analyses were performed to test the robustness of phylogenetic inferences to permutations of the data matrix or to phylogenetic method, including supermatrix, supertree, and coalescent-based approaches, maximum-likelihood and Bayesian methods, partitioned and unpartitioned analyses, and amino acid versus DNA alignments. Among other results, we find robust support for a sister-group relationship between land plants and one group of streptophyte green algae, the Zygnematophyceae. Strong and robust support for a clade comprising liverworts and mosses is inconsistent with a widely accepted view of early land plant evolution, and suggests that phylogenetic hypotheses used to understand the evolution of fundamental plant traits should be reevaluated.

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Phylotranscriptomic analysis of the origin and early diversification of land plants

The beneficial effects of arbuscular mycorrhizal (AM) fungi on plant performance and soil health are essential for the sustainable management of agricultural ecosystems. Nevertheless, since the ‘first green revolution’, less attention has been given to beneficial soil microorganisms in general and to AM fungi in particular. Human society benefits from a multitude of resources and processes from natural and managed ecosystems, to which AM make a crucial contribution. These resources and processes, which are called ecosystem services, include products like food and processes like nutrient transfer. Many people have been under the illusion that these ecosystem services are free, invulnerable and infinitely available; taken for granted as public benefits, they lack a formal market and are traditionally absent from society’s balance sheet. In 1997, a team of researchers from the USA, Argentina and the Netherlands put an average price tag of US $33 trillion a year on these fundamental ecosystem services. The present review highlights the key role that the AM symbiosis can play as an ecosystem service provider to guarantee plant productivity and quality in emerging systems of sustainable agriculture. The appropriate management of ecosystem services rendered by AM will impact on natural resource conservation and utilisation with an obvious net gain for human society.

Agroecology: the key role of arbuscular mycorrhizas in ecosystem services.

Phosphorites of the late Neoproterozoic (570 ± 20 Myr BP) Doushantuo Formation, southern China, preserve an exceptional record of multicellular life from just before the Ediacaran radiation of macroscopic animals. Abundant thalli with cellular structures preserved in three-dimensional detail show that latest-Proterozoic algae already possessed many of the anatomical and reproductive features seen in the modern marine flora. Embryos preserved in early cleavage stages indicate that the divergence of lineages leading to bilaterians may have occurred well before their macroscopic traces or body fossils appear in the geological record. Discovery of these fossils shows that the early evolution of multicellular organisms is amenable to direct palaeontological inquiry.

Three-dimensional preservation of algae and animal embryos in a Neoproterozoic phosphorite

Plant life in the Devonian

What do we now know about the origins of plants on land, from an evolutionary and an environmental perspective? The essays in this collection present a synthesis of our present state of knowledge, integrating current information in paleobotany with physical, chemical, and geological data.

Plants invade the land : evolutionary and environmental perspectives

Considerable progress has been made in documenting evidence of very early plants starting in the basal Ordovician employing dispersed spore, phytodebris, and mesofossil data. Macrofossil evidence is sparse until Late Silurian, but recent new data are improving our understanding of aspects of earliest plants. The considerable information about the possible source of cryptospores and trilete spores especially from the well-preserved mesofossils of the Late Silurian and Early Devonian is summarized. Promising avenues of research are the study of spore ultrastructure, and neo-paleo comparisons between newly discovered resistant components of extant bryophytes and fragmentary fossil remains. Recent macrofossil discoveries in the Late Silurian advance our understanding of early events in plant evolution and raise new questions about the timing of evolution or relationships among earliest (mostly vascular) plants.

The Earliest Land Plants

We summarize the current information on gametophytic plants from the Lower Devonian that are represented by three types based on permineralizations in the Rhynie Chert, two of which are antheridial (Lyonophyton and Kidstonophyton) and one that is archegoniate (Langiophyton). Impression and compression remains attributed to Sciadophyton and Calyculiphyton also are interpreted as gametophytic, based on their similarity to the permineralized forms. All are axial structures, with some axes terminating in cup-shaped gametangiophores on or in which gametangia occur, and all exhibit preserved cuticles with stomata and conducting tissue. Similarity in epidermal and conducting cell characters serves as a basis for postulating sporophyte relationships for the Rhynie Chert gametophytes as follows (N-2N): Lyonophyton-Aglaophyton, Kidstonophyton-Nothia, and Langiophyton-Horneophyton. Comparison with bryophytes and tracheophytes shows that these forms exhibit unique combinations of characters. They are more advanced th...

The Gametophyte Generation of Some Early Devonian Land Plants

Available data on the stratigraphic ranges of latest Silurian and Devonian vascular plant macro-fossils (sporophytes) and spores provide insights into the tempo and mode of early tracheophyte evolution. Patterns of diversification, origination, and extinction conform in general to the predictions of Sepkoski's kinetic model of diversification. Rates of generic origination and extinction vary not only through time but also between organ systems for a single time interval. This fact, coupled with data on longevity and turnover and comparative morphological observations, can be used to document mosaic evolution in early vascular plant history. Mosaic evolution is an important theme in plant evolution; indeed, what we recognize as macroevolutionary events often correlate with brief periods of pronounced mosaicism. Such evolutionary patterns reflect the developmental biology of tracheophytes in which individual organs often have life spans that are considerably shorter than the life of the whole plant. Under these conditions, individual organs or organ systems can respond to different sets of evolutionary pressures.The major period of early vascular plant diversification occurred during the late Early and early Middle Devonian Period, 30 Myr or more after the origin of the group. Such lags in diversification are not uncommon in the fossil record. Sometimes they reflect extrinsic controls on diversification, but in other cases they appear to be a consequence of intrinsic rates of origination and extinction.

Patricia G. Gensel

Papers

Plant life in the Devonian

Plants invade the land : evolutionary and environmental perspectives

The Earliest Land Plants

The Gametophyte Generation of Some Early Devonian Land Plants

Character diversification and patterns of evolution in early vascular plants