Green land: Multiple perspectives on green algal evolution and the earliest land plants.

Green plants, broadly defined as green algae and the land plants (together, Viridiplantae), constitute the primary eukaryotic lineage that successfully colonized Earth's emergent landscape. Members of various clades of green plants have independently made the transition from fully aquatic to subaerial habitats many times throughout Earth's history. The transition, from unicells or simple filaments to complex multicellular plant bodies with functionally differentiated tissues and organs, was accompanied by innovations built upon a genetic and phenotypic toolkit that have served aquatic green phototrophs successfully for at least a billion years. These innovations opened an enormous array of new, drier places to live on the planet and resulted in a huge diversity of land plants that have dominated terrestrial ecosystems over the past 500 million years. This review examines the greening of the land from several perspectives, from paleontology to phylogenomics, to water stress responses and the genetic toolkit shared by green algae and plants, to the genomic evolution of the sporophyte generation. We summarize advances on disparate fronts in elucidating this important event in the evolution of the biosphere and the lacunae in our understanding of it. We present the process not as a step-by-step advancement from primitive green cells to an inevitable success of embryophytes, but rather as a process of adaptations and exaptations that allowed multiple clades of green plants, with various combinations of morphological and physiological terrestrialized traits, to become diverse and successful inhabitants of the land habitats of Earth.

Earth's earliest non-marine eukaryotes.

The existence of a terrestrial Precambrian (more than 542 Myr ago) biota has been largely inferred from indirect chemical and geological evidence associated with palaeosols, the weathering of clay minerals and microbially induced sedimentary structures in siliciclastic sediments. Direct evidence of fossils within rocks of non-marine origin in the Precambrian is exceedingly rare. The most widely cited example comprises a single report of morphologically simple mineralized tubes and spheres interpreted as cyanobacteria, obtained from 1,200-Myr-old palaeokarst in Arizona. Organic-walled microfossils were first described from the non-marine Torridonian (1.2-1.0 Gyr ago) sequence of northwest Scotland in 1907. Subsequent studies found few distinctive taxa-a century later, the Torridonian microflora is still being characterized as primarily nondescript "leiospheres". We have comprehensively sampled grey shales and phosphatic nodules throughout the Torridonian sequence. Here we report the recovery of large populations of diverse organic-walled microfossils extracted by acid maceration, complemented by studies using thin sections of phosphatic nodules that yield exceptionally detailed three-dimensional preservation. These assemblages contain multicellular structures, complex-walled cysts, asymmetric organic structures, and dorsiventral, compressed organic thalli, some approaching one millimetre in diameter. They offer direct evidence of eukaryotes living in freshwater aquatic and subaerially exposed habitats during the Proterozoic era. The apparent dominance of eukaryotes in non-marine settings by 1 Gyr ago indicates that eukaryotic evolution on land may have commenced far earlier than previously thought.

Plant evolution: A tapetum is now effectively present in all land plant lineages.

The tapetum, a tissue that elsewhere ensures correct spore development, is missing in some bryophytes. A new study shows that, in the liverwort, Marchantia polymorpha, a gene controlling spore wall deposition is expressed in the capsule lining, so these cells essentially function as a tapetum.

Aeroterrestrial Coleochaete (Streptophyta, Coleochaetales) models early plant adaptation to land.

PREMISE OF THE STUDY: The streptophyte water-to-land transition was a pivotal, but poorly understood event in Earth history. While some early-diverging modern streptophyte algae are aeroterrestrial (living in subaerial habitats), aeroterrestrial survival had not been tested for Coleochaete, widely regarded as obligately aquatic and one of the extant green algal genera most closely related to embryophytes. This relationship motivated a comparison of aeroterrestrial Coleochaete to lower Paleozoic microfossils whose relationships have been uncertain. METHODS: We tested the ability of two species of the experimentally tractable, complex streptophyte algal genus Coleochaete Bréb. to (1) grow and reproduce when cultivated under conditions that mimic humid subaerial habitats, (2) survive desiccation for some period of time, and (3) produce degradation-resistant remains comparable to enigmatic Cambrian microfossils. KEY RESULTS: When grown on mineral agar media or on quartz sand, both species displayed bodies structurally distinct from those expressed in aquatic habitats. Aeroterrestrial Coleochaete occurred as hairless, multistratose, hemispherical bodies having unistratose lobes or irregular clusters of cells with thick, layered, and chemically resistant walls that resemble certain enigmatic lower Paleozoic microfossils. Whether grown under humid conditions or air-dried for a week, then exposed to liquid water, aeroterrestrial Coleochaete produced typical asexual zoospores and germlings. Cells that had been air-dried for periods up to several months maintained their integrity and green pigmentation. CONCLUSIONS: 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.

A fossil record of land plant origins from charophyte algae.

Molecular time trees indicating that embryophytes originated around 500 million years ago (Ma) during the Cambrian are at odds with the record of fossil plants, which first appear in the mid-Silurian almost 80 million years later. This time gap has been attributed to a missing fossil plant record, but that attribution belies the case for fossil spores. Here, we describe a Tremadocian (Early Ordovician, about 480 Ma) assemblage with elements of both Cambrian and younger embryophyte spores that provides a new level of evolutionary continuity between embryophytes and their algal ancestors. This finding suggests that the molecular phylogenetic signal retains a latent evolutionary history of the acquisition of the embryophytic developmental genome, a history that perhaps began during Ediacaran-Cambrian time but was not completed until the mid-Silurian (about 430 Ma).

A possible billion-year-old holozoan with differentiated multicellularity.

Sediments of the Torridonian sequence of the Northwest Scottish Highlands contain a wide array of microfossils, documenting life in a non-marine setting a billion years ago (1 Ga).1-4 Phosphate nodules from the Diabaig Formation at Loch Torridon preserve microorganisms with cellular-level fidelity,5,6 allowing for partial reconstruction of the developmental stages of a new organism, Bicellum brasieri gen. et sp. nov. The mature form of Bicellum consists of a solid, spherical ball of tightly packed cells (a stereoblast) of isodiametric cells enclosed in a monolayer of elongated, sausage-shaped cells. However, two populations of naked stereoblasts show mixed cell shapes, which we infer to indicate incipient development of elongated cells that were migrating to the periphery of the cell mass. These simple morphogenetic movements could be explained by differential cell-cell adhesion.7,8 In fact, the basic morphology of Bicellum is topologically similar to that of experimentally produced cell masses that were shown to spontaneously segregate into two distinct domains based on differential cadherin-based cell adhesion.9 The lack of rigid cell walls in the stereoblast renders an algal affinity for Bicellum unlikely: its overall morphology is more consistent with a holozoan origin. Unicellular holozoans are known today to form multicellular stages within complex life cycles,10-13 so the occurrence of such simple levels of transient multicellularity seen here is consistent with a holozoan affinity. Regardless of precise phylogenetic placement, these fossils demonstrate simple cell differentiation and morphogenic processes that are similar to those seen in some metazoans today.

Genomic and fossil windows into the secret lives of the most ancient fungi.

Fungi have crucial roles in modern ecosystems as decomposers and pathogens, and they engage in various mutualistic associations with other organisms, especially plants. They have a lengthy geological history, and there is an emerging understanding of their impact on the evolution of Earth systems on a large scale. In this Review, we focus on the roles of fungi in the establishment and early evolution of land and freshwater ecosystems. Today, questions of evolution over deep time are informed by discoveries of new fossils and evolutionary analysis of new genomes. Inferences can be drawn from evolutionary analysis by comparing the genes and genomes of fungi with the biochemistry and development of their plant and algal hosts. We then contrast this emerging picture against evidence from the fossil record to develop a new, integrated perspective on the origin and early evolution of fungi.

Bisnorgammacerane traces predatory pressure and the persistent rise of algal ecosystems after Snowball Earth.

Eukaryotic algae rose to ecological relevance after the Neoproterozoic Snowball Earth glaciations, but the causes for this consequential evolutionary transition remain enigmatic. Cap carbonates were globally deposited directly after these glaciations, but they are usually organic barren or thermally overprinted. Here we show that uniquely-preserved cap dolostones of the Araras Group contain exceptional abundances of a newly identified biomarker: 25,28-bisnorgammacerane. Its secular occurrence, carbon isotope systematics and co-occurrence with other demethylated terpenoids suggest a mechanistic connection to extensive microbial degradation of ciliate-derived biomass in bacterially dominated ecosystems. Declining 25,28-bisnorgammacerane concentrations, and a parallel rise of steranes over hopanes, indicate the transition from a bacterial to eukaryotic dominated ecosystem after the Marinoan deglaciation. Nutrient levels already increased during the Cryogenian and were a prerequisite, but not the ultimate driver for the algal rise. Intense predatory pressure by bacterivorous protists may have irrevocably cleared self-sustaining cyanobacterial ecosystems, thereby creating the ecological opportunity that allowed for the persistent rise of eukaryotic algae to global importance.

A Triassic-Jurassic window into the evolution of Lepidoptera.

On the basis of an assemblage of fossilized wing scales recovered from latest Triassic and earliest Jurassic sediments from northern Germany, we provide the earliest evidence for Lepidoptera (moths and butterflies). The diverse scales confirm a (Late) Triassic radiation of lepidopteran lineages, including the divergence of the Glossata, the clade that comprises the vast multitude of extant moths and butterflies that have a sucking proboscis. The microfossils extend the minimum calibrated age of glossatan moths by ca. 70 million years, refuting ancestral association of the group with flowering plants. Development of the proboscis may be regarded as an adaptive innovation to sucking free liquids for maintaining the insect's water balance under arid conditions. Pollination drops secreted by a variety of Mesozoic gymnosperms may have been non-mutualistically exploited as a high-energy liquid source. The early evolution of the Lepidoptera was probably not severely interrupted by the end-Triassic biotic crisis.

Palaeoecology of a billion-year-old non-marine cyanobacterium from the Torridon Group and Nonesuch Formation.

A new chroococcalean cyanobacterium is described from approximately 1-billion-year-old non-marine deposits of the Torridonian Group of Scotland and the Nonesuch Formation of Michigan, USA. Individual cells of the new microfossil, Eohalothece lacustrina gen. et sp. nov., are associated with benthic microbial biofilms, but the majority of samples are recovered in palynological preparations in the form of large, apparently planktonic colonies, similar to extant species of Microcystis. In the Torridonian, Eohalothece is associated with phosphatic nodules, and we have developed a novel hypothesis linking Eohalothece to phosphate deposition in ancient freshwater settings. Extant cyanobacteria can be prolific producers of extracellular microcystins, which are non-ribosomal polypeptide phosphatase inhibitors. Microcystins may have promoted the retention and concentration of sedimentary organic phosphate prior to mineralization of francolite and nodule formation. This has a further implication that the Torridonian lakes were nitrogen limited as the release of microcystins is enhanced under such conditions today. The abundance and wide distribution of Eohalothece lacustrina attests to the importance of cyanobacteria as oxygen-producing photoautotrophs in lacustrine ecosystems at the time of the Mesoproterozoic-Neoproterozoic transition.