Christine Strullu-Derrien

The origin and early evolution of roots

Exceptionally well-preserved fossils shed light on the earliest roots and their interactions with the environment. Geological sites of exceptional fossil preservation are becoming a focus of research on root evolution because they retain edaphic and ecological context, and the remains of plant soft tissues are preserved in some. New information is emerging on the origins of rooting systems, their interactions with fungi, and their nature and diversity in the earliest forest ecosystems. Remarkably well-preserved fossils prove that mycorrhizal symbionts were diverse in simple rhizoid-based systems. Roots evolved in a piecemeal fashion and independently in several major clades through the Devonian Period (416 to 360 million years ago), rapidly extending functionality and complexity. Evidence from extinct arborescent clades indicates that polar auxin transport was recruited independently in several to regulate wood and root development. The broader impact of root evolution on the geochemical carbon cycle is a developing area and one in which the interests of the plant physiologist intersect with those of the geochemist.

A Simple Type of Wood in Two Early Devonian Plants

The earliest evolution of wood occurred in plants of surprisingly small stature. The advent of wood (secondary xylem) is a major event of the Paleozoic Era, facilitating the evolution of large perennial plants. The first steps of wood evolution are unknown. We describe two small Early Devonian (407 to 397 million years ago) plants with secondary xylem including simple rays. Their wood currently represents the earliest evidence of secondary growth in plants. The small size of the plants and the presence of thick-walled cortical cells confirm that wood early evolution was driven by hydraulic constraints rather than by the necessity of mechanical support for increasing height. The plants described here are most probably precursors of lignophytes.

Plants, fungi and oomycetes: a 400-million year affair that shapes the biosphere.

10 New Phytologist Workshop on the ‘Origin and evolution of plants and their interactions with fungi’, London, UK, September 2014 In a rare gathering, genomics met palaeontology at the 10 New Phytologist Workshop on the ‘Origin and evolution of plants and their interactions with fungi’. An eclectic group of 17 expertsmet at The Natural History Museum (London, UK) on 9–10 September 2014 to discuss the latest findings on plant interactions with fungi (Eumycota) and oomycetes (Oomycota = Peronosporomycota), with topics ranging from the fossil record and comparative genomics to symbiosis and phytopathology. The discussions were largely disseminated via socialmedia (Box 1).Highly diverse plant– fungal interactions have formed the backbone of land ecosystems and biogeochemical cycles since the Palaeozoic (see Fig. 1 for geological timeframe). As summarized by Christine StrulluDerrien andPaulKenrick (TheNaturalHistoryMuseum,London, UK) the first land plants arose c. 470 million years (Myr) ago (Kenrick et al., 2012; Edwards et al., 2014), at which time fungi and oomycetes had already colonized terrestrial ecosystems. Following their terrestrialization, these microbes began to abound within plant fossils (Taylor et al., 2014, and references therein). Ultimately, biological interactions sculpted the genomes of plants, fungi and oomycetes (e.g. Schmidt & Panstruga, 2011; Kohler et al., 2015). Here we illustrate the picture that has emerged from the discussions at the 10 New Phytologist Workshop, and point to some pending questions.

Evidence of parasitic Oomycetes (Peronosporomycetes) infecting the stem cortex of the Carboniferous seed fern Lyginopteris oldhamia

Thin sections of petrified fossils made during the latter part of the nineteenth and early twentieth centuries to investigate the internal tissue systems of plants now provide an important new source of information on associated micro-organisms. We report a new heterokont eukaryote (Combresomyces williamsonii sp. nov.) based on exquisitely preserved fossil oogonia, antheridia and hyphae from the Carboniferous (Pennsylvanian: Bashkirian stage) of UK. The structure of the oogonia and antheridia and features observed within the hyphae demonstrate a relationship with Oomycetes (Peronosporomycetes). The fossil micro-organism was documented in situ in petrified stem cortex and rootlets of the extinct seed fern Lyginopteris oldhamia (Pteridospermales). The main observed features point towards a pythiaceous Oomycete but links to biotrophic Albuginales or Peronosporaceae cannot be ruled out owing to the observation of a possible haustorium. Our study provides the earliest evidence for parasitism in Oomycetes.

Early Diverging Fungi: Diversity and Impact at the Dawn of Terrestrial Life

As decomposers or plant pathogens, fungi deploy invasive growth and powerful carbohydrate active enzymes to reduce multicellular plant tissues to humus and simple sugars. Fungi are perhaps also the most important mutualistic symbionts in modern ecosystems, transporting poorly soluble mineral nutrients to plants and thus enhancing the growth of vegetation. However, at their origin over a billion years ago, fungi, like plants and animals, were unicellular marine microbes. Like the other multicellular kingdoms, Fungi evolved increased size, complexity, and metabolic functioning. Interactions of fungi with plants changed terrestrial ecology and geology and modified the Earths atmosphere. In this review, we discuss the diversification and ecological roles of the fungi over their first 600 million years, from their origin through their colonization of land, drawing on phylogenomic evidence for their relationships and metabolic capabilities and on molecular dating, fossils, and modeling of Earths paleoclimate.

The origin and evolution of mycorrhizal symbioses: from palaeomycology to phylogenomics

Contents Summary 1012 I. Introduction 1013 II. The mycorrhizal symbiosis at the dawn and rise of the land flora 1014 III. From early land plants to early trees: the origin of roots and true mycorrhizas 1016 IV. The diversification of the AM symbiosis 1019 V. The ECM symbiosis 1021 VI. The recently evolved ericoid and orchid mycorrhizas 1023 VII. Limits of paleontological vs genetic approaches and perspectives 1023 Acknowledgements 1025 References 1025 SUMMARY: The ability of fungi to form mycorrhizas with plants is one of the most remarkable and enduring adaptations to life on land. The occurrence of mycorrhizas is now well established in c. 85% of extant plants, yet the geological record of these associations is sparse. Fossils preserved under exceptional conditions provide tantalizing glimpses into the evolutionary history of mycorrhizas, showing the extent of their occurrence and aspects of their evolution in extinct plants. The fossil record has important roles to play in establishing a chronology of when key fungal associations evolved and in understanding their importance in ecosystems through time. Together with calibrated phylogenetic trees, these approaches extend our understanding of when and how groups evolved in the context of major environmental change on a global scale. Phylogenomics furthers this understanding into the evolution of different types of mycorrhizal associations, and genomic studies of both plants and fungi are shedding light on how the complex set of symbiotic traits evolved. Here we present a review of the main phases of the evolution of mycorrhizal interactions from palaeontological, phylogenetic and genomic perspectives, with the aim of highlighting the potential of fossil material and a geological perspective in a cross-disciplinary approach.

A New Chytridiomycete Fungus Intermixed with Crustacean Resting Eggs in a 407-Million-Year-Old Continental Freshwater Environment

The 407-million-year-old Rhynie Chert (Scotland) contains the most intact fossilised remains of an early land-based ecosystem including plants, arthropods, fungi and other microorganisms. Although most studies have focused on the terrestrial component, fossilised freshwater environments provide critical insights into fungal-algal interactions and the earliest continental branchiopod crustaceans. Here we report interactions between an enigmatic organism and an exquisitely preserved fungus. The fungal reproductive structures are intermixed with exceptionally well-preserved globular spiny structures interpreted as branchiopod resting eggs. Confocal laser scanning microscopy enabled us to reconstruct the fungus and its possible mode of nutrition, the affinity of the resting eggs, and their spatial associations. The new fungus (Cultoraquaticus trewini gen. et sp. nov) is attributed to Chytridiomycota based on its size, consistent formation of papillae, and the presence of an internal rhizoidal system. It is the most pristine fossil Chytridiomycota known, especially in terms of rhizoidal development and closely resembles living species in the Rhizophydiales. The spiny resting eggs are attributed to the crustacean Lepidocaris rhyniensis, dating branchiopod adaptation to life in ephemeral pools to the Early Devonian. The new fungal interaction suggests that, as in modern freshwater environments, chytrids were important to the mobilisation of nutrients in early aquatic foodwebs.

Biota and palaeoenvironment of a high middle-latitude Late Triassic peat-forming ecosystem from Hopen, Svalbard archipelago

Abstract A siliceous permineralized peat block recovered from Hopen in the Svalbard archipelago hosts a low-diversity Late Triassic flora dominated by autochthonous roots and stems of bennettitaleans and lycophytes, and parautochthonous leaves, sporangia, spores and pollen from a small range of pteridophytes and gymnosperms. Some parenchymatous bennettitalean root cells show interactions with chytrid fungi and bacteria; the remains of other fungi and fungi-like organisms are dispersed within the peats detrital matrix. Cavities excavated through some roots and compacted detritus contain abundant coprolites probably derived from sapro-xylophagous oribatid mites, although no body fossils have yet been identified. Sparse larger coprolites containing leaf fragments attest to the presence of invertebrate folivores in the ancient ecosystem. The low-diversity flora, relatively few trophic levels and simple nutritional web, together with sedimentological aspects of the host formation and the peat structure, collectively favour accumulation of the organic mass as a fibric (root-dominated) peat within a temperate (high middle-latitude), well-aerated mire.

The early land plants from the Armorican Massif: sedimentological and palynological considerations on age and environment

The Châteaupanne Unit belongs to the South Armorican domain of the Armorican Massif (France), which is part of the Variscan belt. This unit includes two Lower Devonian plant levels and one of them corresponds to the Basal Member of the Chalonnes Formation. A sedimentological and palaeontological analysis of these fossiliferous deposits from the Châteaupanne quarry (Montjean/Loire, Maine et Loire, France) is presented here for the first time. The age determination based on palynology indicates that the locality records the earliest occurrence of plant megafossils in the Armorican Massif. Their presence suggests an emergence event that has never been described before. Our study highlights the promising potential of the Basal Member of the Chalonnes Formation to aid in understanding these occurrences, and provides new insights into the history of the Variscan belt.

New insights into the evolutionary history of Fungi from a 407 Ma Blastocladiomycota fossil showing a complex hyphal thallus

Zoosporic fungi are key saprotrophs and parasites of plants, animals and other fungi, playing important roles in ecosystems. They comprise at least three phyla, of which two, Chytridiomycota and Blastocladiomycota, developed a range of thallus morphologies including branching hyphae. Here we describe Retesporangicus lyonii gen. et sp. nov., an exceptionally well preserved fossil, which is the earliest known to produce multiple sporangia on an expanded hyphal network. To better characterize the fungus we develop a new method to render surfaces from image stacks generated by confocal laser scanning microscopy. Here, the method helps to reveal thallus structure. Comparisons with cultures of living species and character state reconstructions analysed against recent molecular phylogenies of 24 modern zoosporic fungi indicate an affinity with Blastocladiomycota. We argue that in zoosporic fungi, kinds of filaments such as hyphae, rhizoids and rhizomycelium are developmentally similar structures adapted for varied functions including nutrient absorption and anchorage. The fossil is the earliest known type to develop hyphae which likely served as a saprotrophic adaptation to patchy resource availability. Evidence from the Rhynie chert provides our earliest insights into the biology of fungi and their roles in the environment. It demonstrates that zoosporic fungi were already diverse in 407 million-year-old terrestrial ecosystems. This article is part of a discussion meeting issue ‘The Rhynie cherts: our earliest terrestrial ecosystem revisited’.