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Earth’s long-term climate may have profoundly influenced plant evolution. Local climatic factors, including water availability, light, and temperature, play a key role in plant physiology and growth, and have fluctuated substantially over geological time. However, the impact of these key climate variables on global plant biomass across the Phanerozoic has not yet been established. Linking climate and dynamic vegetation modelling, we identify two key ‘windows of opportunity’ during the Ordovician and Jurassic-Paleogene capable of supporting dramatic expansions of potential plant biomass. These conditions are driven by continental dispersion, paleolatitude of continental area and a lack of glaciation, allowing for an intense hydrological cycle and greater water availability. These windows coincide with the initial expansion of land plants and the later angiosperm radiation. Our findings suggest that the timing and expansion of habitable space for plants played an important role in plant evolution and diversification.

Societal Impact Statement\ud \ud The Earth's population is projected to rise to 9.7 billion by 2050 resulting in mounting pressure to increase agricultural yields in a sustainable manner. Arbuscular mycorrhizal (AM) fungi may be important players in this agricultural transition given their capacity to improve soil and plant health. Benefits gained by crops hosting AM fungi can be cultivar-specific and also affected by insect herbivory, although the combined effect of these factors remains unclear. Here, we show that, in an economically and socially significant tri-partite system, there is interplay between crop cultivar, AM colonisation and aphid herbivory on plant growth and nutritional status.\ud \ud \ud \ud Summary\ud \ud - Arbuscular mycorrhizal (AM) fungi are critical components of the rhizosphere across nearly all terrestrial biomes. AM fungi associate with most plants, including major crops, usually increasing plant access to soil nutrients and enhancing defence against pests and pathogens in return for photosynthetic carbon (C). However, plant growth responses to AM fungi vary according to species and genotype, an issue pertinent in agro-ecosystems where crop cultivar can play an important role in AM function. Evidence suggests other biotic interactions, including with sap-feeding aphids, impact the function of AM symbioses in plants. Nonetheless, whether these biotic factors alter genotype (or cultivar)-specific plant growth and nutritional responses to colonisation by AM fungi remains unclear.\ud \ud \ud \ud - Here, we investigated whether mycorrhizal responsiveness of three cultivars of wheat (Triticum eastivum L.) to colonisation by a ubiquitously occurring AM fungus (Rhizophagus irregularis) differ in the presence or absence of bird cherry-oat aphids (Rhopalosiphum padi), a major pest of cereals.\ud \ud \ud \ud - Our findings show that although AM fungal colonisation and AM-mediated plant growth responses were not affected by aphid feeding, there was variation between cultivars in the benefits gained by host plants in terms of nutrient acquisition and root growth, while aphid abundances also differed between wheat varieties.\ud \ud \ud \ud - Understanding what causes cultivar-specific outcomes and how they ultimately impact plant growth promotion, crop yields and food production represent key future research goals in agroecology.

Root exudates and rhizosheaths of attached soil are important features of growing roots. To elucidate factors involved in rhizosheath formation, wild type (WT) barley (Hordeum vulgare L. cv. Pallas) and a root hairless mutant, bald root barley (brb), were investigated with a combination of physiological, biochemical and immunochemical assays. When grown in soil, WT barley roots bound ∼5-fold more soil than brb per unit root length. High molecular weight (HMW) polysaccharide exudates of brb roots had less soil-binding capacity than those of WT root exudates. Carbohydrate and glycan monoclonal antibody analyses of HMW polysaccharide exudates indicated differing glycan profiles. Relative to WT plants, root exudates of brb had reduced signals for arabinogalactan-protein (AGP), extensin and heteroxylan epitopes. In contrast, the root exudate of 2-week old brb plants contained ∼25-fold more detectable xyloglucan epitope relative to WT. Root system immunoprints confirmed the higher levels of release of the xyloglucan epitope from brb root apices and root axes relative to WT. Epitope detection with anion-exchange chromatography indicated that the increased detection of xyloglucan in brb exudates was due to enhanced abundance of a neutral polymer. Conversely, brb root exudates contained decreased amounts of an acidic polymer, with soil-binding properties, containing the xyloglucan epitope and glycoprotein and heteroxylan epitopes relative to WT. We therefore propose that, in addition to physically structuring soil particles, root hairs facilitate rhizosheath formation by releasing a soil-binding polysaccharide complex.

Mycorrhizal associations between fungi and plant roots have globally significant impacts on nutrient cycling. Mucoromycotina ‘fine root endophytes’ (MFRE) are a distinct and recently characterised group of mycorrhiza-forming fungi that associate with the roots of a range of host plant species. Given their previous misidentification and assignment as arbuscular mycorrhizal fungi (AMF) of the Glomeromycotina, it is now important to untangle the specific form and function of MFRE symbioses. In particular, relatively little is known about the nature of MFRE colonisation and their role in N uptake and transfer to host plants. Even less is known about the mechanisms by which MFRE access and assimilate N, and how this N is processed and subsequently exchanged with host plants for photosynthates. Here, we summarise and contrast the structures formed by MFRE and arbuscular mycorrhizal fungi in host plants as well as compare the N source preference of each mycorrhizal fungal group with what is currently known of MFRE N uptake. We compare the mechanisms of N assimilation and transfer to host plants utilised by the main groups of mycorrhizal fungi and hypothesise potential mechanisms for MFRE N assimilation and transfer, outlining directions for future research.

1. Plants typically interact with multiple above‐ and below‐ground organisms simultaneously, with their symbiotic relationships spanning a continuum ranging from mutualism, such as with arbuscular mycorrhizal fungi (AMF), to parasitism, including symbioses with plant‐parasitic nematodes (PPN).\ud \ud \ud \ud 2. Although research is revealing the patterns of plant resource allocation to mutualistic AMF partners under different host and environmental constraints, the root ecosystem, with multiple competing symbionts, is often ignored. Such competition is likely to heavily influence resource allocation to symbionts.\ud \ud \ud \ud 3.Here, we outline and discuss the competition between AMF and PPN for the finite supply of host plant resources, highlighting the need for a more holistic understanding of the influence of below‐ground interactions on plant resource allocation. Based on recent developments in our understanding of other symbiotic systems such as legume–rhizobia and AMF‐aphid‐plant, we propose hypotheses for the distribution of plant resources between contrasting below‐ground symbionts and how such competition may affect the host.\ud \ud \ud \ud 4. We identify relevant knowledge gaps at the physiological and molecular scales which, if resolved, will improve our understanding of the true ecological significance and potential future exploitation of AMF‐PPN‐plant interactions in order to optimize plant growth. To resolve these outstanding knowledge gaps, we propose the application of well‐established methods in isotope tracing and nutrient budgeting to monitor the movement of nutrients between symbionts. By combining these approaches with novel time of arrival experiments and experimental systems involving multiple plant hosts interlinked by common mycelial networks, it may be possible to reveal the impact of multiple, simultaneous colonizations by competing symbionts on carbon and nutrient flows across ecologically important scales.

Green plants (Viridiplantae) include around 450,000–500,000 species1,2 of great diversity and have important roles in terrestrial and aquatic ecosystems. Here, as part of the One Thousand Plant Transcriptomes Initiative, we sequenced the vegetative transcriptomes of 1,124 species that span the diversity of plants in a broad sense (Archaeplastida), including green plants (Viridiplantae), glaucophytes (Glaucophyta) and red algae (Rhodophyta). Our analysis provides a robust phylogenomic framework for examining the evolution of green plants. Most inferred species relationships are well supported across multiple species tree and supermatrix analyses, but discordance among plastid and nuclear gene trees at a few important nodes highlights the complexity of plant genome evolution, including polyploidy, periods of rapid speciation, and extinction. Incomplete sorting of ancestral variation, polyploidization and massive expansions of gene families punctuate the evolutionary history of green plants. Notably, we find that large expansions of gene families preceded the origins of green plants, land plants and vascular plants, whereas whole-genome duplications are inferred to have occurred repeatedly throughout the evolution of flowering plants and ferns. The increasing availability of high-quality plant genome sequences and advances in functional genomics are enabling research on genome evolution across the green tree of life., The One Thousand Plant Transcriptomes Initiative provides a robust phylogenomic framework for examining green plant evolution that comprises the transcriptomes and genomes of diverse species of green plants.

Soil is a crucial component of the biosphere and is a major sink for organic carbon. Plant roots are known to release a wide range of carbon‐based compounds into soils, including polysaccharides, but the functions of these are not known in detail.\ud \ud Using a monoclonal antibody to plant cell wall xyloglucan, we show that this polysaccharide is secreted by a wide range of angiosperm roots, and relatively abundantly by grasses. It is also released from the rhizoids of liverworts, the earliest diverging lineage of land plants. Using analysis of water‐stable aggregate size, dry dispersion particle analysis and scanning electron microscopy, we show that xyloglucan is effective in increasing soil particle aggregation, a key factor in the formation and function of healthy soils.\ud \ud To study the possible roles of xyloglucan in the formation of soils, we analysed the xyloglucan contents of mineral soils of known age exposed upon the retreat of glaciers. These glacial forefield soils had significantly higher xyloglucan contents than detected in a UK grassland soil.\ud \ud We propose that xyloglucan released from plant rhizoids/roots is an effective soil particle aggregator and may, in this role, have been important in the initial colonization of land.

It has long been postulated that symbiotic fungi facilitated plant migrations onto land through enhancing the scavenging of mineral nutrients and exchanging these for photosynthetically fixed organic carbon. Today, land plant–fungal symbioses are both widespread and diverse. Recent discoveries show that a variety of potential fungal associates were likely available to the earliest land plants, and that these early partnerships were probably affected by changing atmospheric CO2 concentrations. Here, we evaluate current hypotheses and knowledge gaps regarding early plant–fungal partnerships in the context of newly discovered fungal mutualists of early and more recently evolved land plants and the rapidly changing views on the roles of plant–fungal symbioses in the evolution and ecology of the terrestrial biosphere.

Plants suffer multiple, simultaneous assaults from above and below ground. In the laboratory, pests and/or pathogen attack are commonly studied on an individual basis. The molecular response of the plant to attack from multiple organisms and the interaction of different defence pathways is unclear. The inducible systemic responses of the potato (Solanum tuberosum L.) host plant were analysed to characterise the plant-mediated indirect interactions between a sedentary, endoparasitic nematode (Globodera pallida) and a phloem-sucking herbivore (Myzus persicae). The reproductive success of M. persicae was greater on potato plants pre-infected with G. pallida compared to control plants. Salicylic acid (SA) increased systemically in the leaves of potato plants following nematode and aphid infection singly with a corresponding increase in expression of SA-mediated marker genes. An increase in jasmonic acid (JA) associated with aphid infection was suppressed when plants were co-infected with nematodes. Our data suggests a positive, asymmetric interaction between a sedentary endoparasitic nematode and a sap-sucking insect. The systemic response of the potato plant following infection with G. pallida indirectly influences the performance of M. persicae. This work reveals additional secondary benefits of controlling individual crop pests.

Current understanding of the nature and function of fungal associations in pteridophytes is surprisingly patchy given their key evolutionary position, current research foci on other early‐branching plant clades, and major efforts at unravelling mycorrhizal evolution and the mechanisms underlying this key interaction between plants and fungi. Here we provide a critical review of current knowledge of fungal associations across pteridophytes and consider future directions making recommendations along the way. From a comprehensive survey of the literature, a confused picture emerges: suggestions that members of the Lycopsida harbour Basidiomycota fungi contrast sharply with extensive cytological and recent molecular evidence pointing to exclusively Glomeromycota and/or Mucoromycotina associations in this group. Similarly, reports of dark septate, assumingly ascomycetous, hyphae in a range of pteridophytes, advocating a mutualistic relationship, are not backed by functional evidence and the fact that the fungus invariably occupies dead host tissue points to saprotrophy and not mutualism. The best conclusion that can be reached based on current evidence is that the fungal symbionts of pteridophytes belong to the two fungal lineages Mucoromycotina and Glomeromycota. Do symbiotic fungi and host pteridophytes engage in mutually beneficial partnerships? To date, only two pioneering studies have addressed this key question demonstrating reciprocal exchange of nutrients between the sporophytes of Ophioglossum vulgatum and Osmunda regalis and their fungal symbionts. There is a pressing need for more functional investigations also extending to the gametophyte generation and coupled with in vitro isolation and resynthesis studies to unravel the effect of the fungi on their host.