Almost all land plants form symbiotic associations with mycorrhizal fungi. These below-ground fungi play a key role in terrestrial ecosystems as they regulate nutrient and carbon cycles, and influence soil structure and ecosystem multifunctionality. Up to 80% of plant N and P is provided by mycorrhizal fungi andmany plant species depend on these symbionts for growth and survival. Estimates suggest that there are . 50 000 fungal species that form mycorrhizal associations with . 250 000 plant species. The development of high-throughput molecular tools has helped us to better understand the biology, evolution, and biodiversity of mycorrhizal associations. Nuclear genome assemblies and gene annotations of 33 mycorrhizal fungal species are now available providing fascinating opportunities to deepen our understanding of the mycorrhizal lifestyle, the metabolic capabilities of these plant symbionts, the molecular dialogue between symbionts, and evolutionary adaptations across a range of mycorrhizal associations. Large-scale molecular surveys have provided novel insights into the diversity, spatial and temporal dynamics of mycorrhizal fungal communities. At the ecological level, network theory makes it possible to analyze interactions between plant–fungal partners as complex underground multi-species networks. Our analysis suggests that nestedness, modularity and specificity of mycorrhizal networks vary and depend on mycorrhizal type. Mechanistic models explaining partner choice, resource exchange, and coevolution in mycorrhizal associations have been developed and are being tested. This review ends with major frontiers for further research.
Environmental stress conditions such as drought, heat, salinity, cold, or pathogen infection can have a devastating impact on plant growth and yield under field conditions. Nevertheless, the effects of these stresses on plants are typically being studied under controlled growth conditions in the laboratory. The field environment is very different from the controlled conditions used in laboratory studies, and often involves the simultaneous exposure of plants to more than one abiotic and/or biotic stress condition, such as a combination of drought and heat, drought and cold, salinity and heat, or any of the major abiotic stresses combined with pathogen infection. Recent studies have revealed that the response of plants to combinations of two or more stress conditions is unique and cannot be directly extrapolated from the response of plants to each of the different stresses applied individually. Moreover, the simultaneous occurrence of different stresses results in a high degree of complexity in plant responses, as the responses to the combined stresses are largely controlled by different, and sometimes opposing, signaling pathways that may interact and inhibit each other. In this review, we will provide an update on recent studies focusing on the response of plants to a combination of different stresses. In particular, we will address how different stress responses are integrated and how they impact plant growth and physiological traits.
Fine roots acquire essential soil resources and mediate biogeochemical cycling in terrestrial ecosystems. Estimates of carbon and nutrient allocation to build and maintain these structures remain uncertain because of the challenges of consistently measuring and interpreting fine-root systems. Traditionally, fine roots have been defined as all roots ≤ 2 mm in diameter, yet it is now recognized that this approach fails to capture the diversity of form and function observed among fine-root orders. Here, we demonstrate how order-based and functional classification frameworks improve our understanding of dynamic root processes in ecosystems dominated by perennial plants. In these frameworks, fine roots are either separated into individual root orders or functionally defined into a shorter-lived absorptive pool and a longer-lived transport fine-root pool. Using these frameworks, we estimate that fine-root production and turnover represent 22% of terrestrial net primary production globally – a . 30% reduction from previous estimates assuming a single fine-root pool. Future work developing tools to rapidly differentiate functional fine-root classes, explicit incorporation of mycorrhizal fungi into fine-root studies, and wider adoption of a two-pool approach to model fine roots provide opportunities to better understand below-ground processes in the terrestrial biosphere.
The establishment of modern terrestrial life is indissociable from angiosperm evolution. While available molecular clock estimates of angiosperm age range from the Paleozoic to the Late Cretaceous, the fossil record is consistent with angiosperm diversification in the Early Cretaceous. The time-frame of angiosperm evolution is here estimated using a sample representing 87% of families and sequences of five plastid and nuclear markers, implementing penalized likelihood and Bayesian relaxed clocks. A literature-based review of the palaeontological record yielded calibrations for 137 phylogenetic nodes. The angiosperm crown age was bound within a confidence interval calculated with a method that considers the fossil record of the group. An Early Cretaceous crown angiosperm age was estimated with high confidence. Magnoliidae, Monocotyledoneae and Eudicotyledoneae diversified synchronously 135–130 million yr ago (Ma); Pentapetalae is 126–121 Ma; and Rosidae (123–115 Ma) preceded Asteridae (119–110 Ma). Family stem ages are continuously distributed between . 140 and 20 Ma. This time-frame documents an early phylogenetic proliferation that led to the establishment of major angiosperm lineages, and the origin of over half of extant families, in the Cretaceous. While substantial amounts of angiosperm morphological and functional diversity have deep evolutionary roots, extant species richness was probably acquired later.
Plants can no longer be considered as standalone entities and a more holistic perception is needed. Indeed, plants harbor a wide diversity of microorganisms both inside and outside their tissues, in the endosphere and ectosphere, respectively. These microorganisms, which mostly belong to Bacteria and Fungi, are involved in major functions such as plant nutrition and plant resistance to biotic and abiotic stresses. Hence, the microbiota impact plant growth and survival, two key components of fitness. Plant fitness is therefore a consequence of the plant and its microbiota, which collectively form a holobiont. Complementary to the reductionist perception of evolutionary pressures acting on plant or symbiotic compartments, the plant holobiont concept requires a novel perception of evolution. The interlinkages between the plant holobiont components are explored here in the light of current ecological and evolutionary theories. Microbiome complexity and the rules of microbiotic community assemblage are not yet fully understood. It is suggested that the plant can modulate its microbiota to dynamically adjust to its environment. To better understand the level of plant dependence on the microbiotic components, the core microbiota need to be determined at different hierarchical scales of ecology while pan-microbiome analyses would improve characterization of the functions displayed.
We quantified the biomass allocation patterns to leaves, stems and roots in vegetative plants, and how this is influenced by the growth environment, plant size, evolutionary history and competition. Dose–response curves of allocation were constructed by means of a meta-analysis from a wide array of experimental data. They show that the fraction of whole-plant mass represented by leaves (LMF) increases most strongly with nutrients and decreases most strongly with light. Correction for size-induced allocation patterns diminishes the LMF-response to light, but makes the effect of temperature on LMF more apparent. There is a clear phylogenetic effect on allocation, as eudicots invest relatively more than monocots in leaves, as do gymnosperms compared with woody angiosperms. Plants grown at high densities show a clear increase in the stem fraction. However, in most comparisons across species groups or environmental factors, the variation in LMF is smaller than the variation in one of the other components of the growth analysis equation: the leaf area : leaf mass ratio (SLA). In competitive situations, the stem mass fraction increases to a smaller extent than the specific stem length (stem length : stem mass). Thus, we conclude that plants generally are less able to adjust allocation than to alter organ morphology.
Soil salinity reduces crop yield. The extent and severity of salt-affected agricultural land is predicted to worsen as a result of inadequate drainage of irrigated land, rising water tables and global warming. The growth and yield of most plant species are adversely affected by soil salinity, but varied adaptations can allow some crop cultivars to continue to grow and produce a harvestable yield under moderate soil salinity. Significant costs are associated with saline soils: the economic costs to the farming community and the energy costs of plant adaptations. We briefly consider mechanisms of adaptation and highlight recent research examples through a lens of their applicability to improving the energy efficiency of crops under saline field conditions.
Novel high-throughput sequencing methods outperform earlier approaches in terms of resolution and magnitude. They enable identification and relative quantification of community members and offer new insights into fungal community ecology. These methods are currently taking over as the primary tool to assess fungal communities of plant-associated endophytes, pathogens, and mycorrhizal symbionts, as well as free-living saprotrophs. Taking advantage of the collective experience of six research groups, we here review the different stages involved in fungal community analysis, from field sampling via laboratory procedures to bioinformatics and data interpretation. We discuss potential pitfalls, alternatives, and solutions. Highlighted topics are challenges involved in: obtaining representative DNA/RNA samples and replicates that encompass the targeted variation in community composition, selection of marker regions and primers, options for amplification and multiplexing, handling of sequencing errors, and taxonomic identification. Without awareness of methodological biases, limitations of markers, and bioinformatics challenges, large-scale sequencing projects risk yielding artificial results and misleading conclusions.
Climate change is expected to drive increased tree mortality through drought, heat stress, and insect attacks, with manifold impacts on forest ecosystems. Yet, climate-induced tree mortality and biotic disturbance agents are largely absent from process-based ecosystem models. Using data sets from the western USA and associated studies, we present a framework for determining the relative contribution of drought stress, insect attack, and their interactions, which is critical for modeling mortality in future climates. We outline a simple approach that identifies the mechanisms associated with two guilds of insects – bark beetles and defoliators – which are responsible for substantial tree mortality. We then discuss cross-biome patterns of insect-driven tree mortality and draw upon available evidence contrasting the prevalence of insect outbreaks in temperate and tropical regions. We conclude with an overview of tools and promising avenues to address major challenges. Ultimately, a multitrophic approach that captures tree physiology, insect populations, and tree–insect interactions will better inform projections of forest ecosystem responses to climate change.
Carbon (C) metabolism is at the core of ecosystem function. Decomposers play a critical role in this metabolism as they drive soil C cycle by mineralizing organic matter to CO . Their growth depends on the carbon-use efficiency (CUE), defined as the ratio of growth over C uptake. By definition, high CUE promotes growth and possibly C stabilization in soils, while low CUE favors respiration. Despite the importance of this variable, flexibility in CUE for terrestrial decomposers is still poorly characterized and is not represented in most biogeochemical models. Here, we synthesize the theoretical and empirical basis of changes in CUE across aquatic and terrestrial ecosystems, highlighting common patterns and hypothesizing changes in CUE under future climates. Both theoretical considerations and empirical evidence from aquatic organisms indicate that CUE decreases as temperature increases and nutrient availability decreases. More limited evidence shows a similar sensitivity of CUE to temperature and nutrient availability in terrestrial decomposers. Increasing CUE with improved nutrient availability might explain observed declines in respiration from fertilized stands, while decreased CUE with increasing temperature and plant C : N ratios might decrease soil C storage. Current biogeochemical models could be improved by accounting for these CUE responses along environmental and stoichiometric gradients.
Transcription factors belonging to the APETALA2/Ethylene Responsive Factor (AP2/ERF) family are conservatively widespread in the plant kingdom. These regulatory proteins are involved in the control of primary and secondary metabolism, growth and developmental programs, as well as responses to environmental stimuli. Due to their plasticity and to the specificity of individual members of this family, AP2/ERF transcription factors represent valuable targets for genetic engineering and breeding of crops. In this review, we integrate the evidence collected from functional and structural studies to describe their different mechanisms of action and the regulatory pathways that affect their activity.
Plants synthesize an amazing diversity of volatile organic compounds (VOCs) that facilitate interactions with their environment, from attracting pollinators and seed dispersers to protecting themselves from pathogens, parasites and herbivores. Recent progress in -omics technologies resulted in the isolation of genes encoding enzymes responsible for the biosynthesis of many volatiles and contributed to our understanding of regulatory mechanisms involved in VOC formation. In this review, we largely focus on the biosynthesis and regulation of plant volatiles, the involvement of floral volatiles in plant reproduction as well as their contribution to plant biodiversity and applications in agriculture via crop–pollinator interactions. In addition, metabolic engineering approaches for both the improvement of plant defense and pollinator attraction are discussed in light of methodological constraints and ecological complications that limit the transition of crops with modified volatile profiles from research laboratories to real-world implementation.
Summary The evolution of lignified xylem allowed for the efficient transport of water under tension, but also exposed the vascular network to the risk of gas emboli and the spread of gas between xylem conduits, thus impeding sap transport to the leaves. A well‐known hypothesis proposes that the safety of xylem (its ability to resist embolism formation and spread) should trade off against xylem efficiency (its capacity to transport water). We tested this safety–efficiency hypothesis in branch xylem across 335 angiosperm and 89 gymnosperm species. Safety was considered at three levels: the xylem water potentials where 12%, 50% and 88% of maximal conductivity are lost. Although correlations between safety and efficiency were weak (r2 < 0.086), no species had high efficiency and high safety, supporting the idea for a safety–efficiency tradeoff. However, many species had low efficiency and low safety. Species with low efficiency and low safety were weakly associated (r2 < 0.02 in most cases) with higher wood density, lower leaf‐ to sapwood‐area and shorter stature. There appears to be no persuasive explanation for the considerable number of species with both low efficiency and low safety. These species represent a real challenge for understanding the evolution of xylem. See also the Commentary by Brodersen
Although hypothesized for many years, the involvement of ectomycorrhizal fungi in decomposition of soil organic matter remains controversial and has not yet been fully acknowledged as an important factor in the regulation of soil carbon (C) storage. Here, we review recent findings, which support the view that some ectomycorrhizal fungi have the capacity to oxidize organic matter, either by ‘brown-rot’ Fenton chemistry or using ‘white-rot’ peroxidases. We propose that ectomycorrhizal fungi benefit from organic matter decomposition primarily through increased nitrogen mobilization rather than through release of metabolic C and question the view that ectomycorrhizal fungi may act as facultative saprotrophs. Finally, we discuss how mycorrhizal decomposition may influence organic matter storage in soils and mediate responses of ecosystem C sequestration to environmental changes.
Demand of all living organisms on the same nutrients forms the basis for interspecific competition between plants and microorganisms in soils. This competition is especially strong in the rhizosphere. To evaluate competitive and mutualistic interactions between plants and microorganisms and to analyse ecological consequences of these interactions, we analysed 424 data pairs from 41 N-labelling studies that investigated N redistribution between roots and microorganisms. Calculated Michaelis–Menten kinetics based on (Michaelis constant) and (maximum uptake capacity) values from 77 studies on the uptake of nitrate, ammonia, and amino acids by roots and microorganisms clearly showed that, shortly after nitrogen (N) mobilization from soil organic matter and litter, microorganisms take up most N. Lower values of microorganisms suggest that they are especially efficient at low N concentrations, but can also acquire more N at higher N concentrations ( ) compared with roots. Because of the unidirectional flow of nutrients from soil to roots, plants are the winners for N acquisition in the long run. Therefore, despite strong competition between roots and microorganisms for N, a temporal niche differentiation reflecting their generation times leads to mutualistic relationships in the rhizosphere. This temporal niche differentiation is highly relevant ecologically because it: protects ecosystems from N losses by leaching during periods of slow or no root uptake; continuously provides roots with available N according to plant demand; and contributes to the evolutionary development of mutualistic interactions between roots and microorganisms.
Boreal forest soils store a major proportion of the global terrestrial carbon (C) and belowground inputs contribute as much as above-ground plant litter to the total C stored in the soil. A better understanding of the dynamics and drivers of root-associated fungal communities is essential to predict long-term soil C storage and climate feedbacks in northern ecosystems. We used 454-pyrosequencing to identify fungal communities across fine-scaled soil profiles in a 5000 yr fire-driven boreal forest chronosequence, with the aim of pinpointing shifts in fungal community composition that may underlie variation in below-ground C sequestration. In early successional-stage forests, higher abundance of cord-forming ectomycorrhizal fungi (such as and species) was linked to rapid turnover of mycelial biomass and necromass, efficient nitrogen (N) mobilization and low C sequestration. In late successional-stage forests, cord formers declined, while ericoid mycorrhizal ascomycetes continued to dominate, potentially facilitating long-term humus build-up through production of melanized hyphae that resist decomposition. Our results suggest that cord-forming ectomycorrhizal fungi and ericoid mycorrhizal fungi play opposing roles in below-ground C storage. We postulate that, by affecting turnover and decomposition of fungal tissues, mycorrhizal fungal identity and growth form are critical determinants of C and N sequestration in boreal forests.
The design and function of leaf venation are important to plant performance, with key implications for the distribution and productivity of ecosystems, and applications in paleobiology, agriculture and technology.Wesynthesize classical concepts and the recent literature on a wide range of aspects of leaf venation. We describe 10 major structural features that contribute to multiple key functions, and scale up to leaf and plant performance. We describe the development and plasticity of leaf venation and its adaptation across environments globally, and a new global data compilation indicating trends relating vein length per unit area to climate, growth form and habitat worldwide. Wesynthesize the evolution of vein traits in the major plant lineages throughout paleohistory, highlighting the multiple origins of individual traits. We summarize the strikingly diverse current applications of leaf vein research in multiple fields of science and industry. A unified core understanding will enable an increasing range of plant biologists to incorporate leaf venation into their research.
Summary Desert plants are hypothesized to survive the environmental stress inherent to these regions in part thanks to symbioses with microorganisms, and yet these microbial species, the communities they form, and the forces that influence them are poorly understood. Here we report the first comprehensive investigation of the microbial communities associated with species of Agave, which are native to semiarid and arid regions of Central and North America and are emerging as biofuel feedstocks. We examined prokaryotic and fungal communities in the rhizosphere, phyllosphere, leaf and root endosphere, as well as proximal and distal soil samples from cultivated and native agaves, through Illumina amplicon sequencing. Phylogenetic profiling revealed that the composition of prokaryotic communities was primarily determined by the plant compartment, whereas the composition of fungal communities was mainly influenced by the biogeography of the host species. Cultivated A. tequilana exhibited lower levels of prokaryotic diversity compared with native agaves, although no differences in microbial diversity were found in the endosphere. Agaves shared core prokaryotic and fungal taxa known to promote plant growth and confer tolerance to abiotic stress, which suggests common principles underpinning Agave–microbe interactions. See also the Commentary by Hacquard
Although the molecular phylogeny, evolution and biodiversity of arbuscular mycorrhizal fungi (AMF) are becoming clearer, phylotaxonomically reliable sequence data are still limited. To fill this gap, a data set allowing resolution and environmental tracing across all taxonomic levels is provided. Two overlapping nuclear DNA regions, totalling 3 kb, were analysed: the small subunit (SSU) rRNA gene (up to 1800 bp) and a fragment spanning 250 bp of the SSU rDNA, the internal transcribed spacer (ITS) region ( 475–520 bp) and 800 bp of the large subunit (LSU) rRNA gene. Both DNA regions together could be analysed for 35 described species, the SSU rDNA for 76 named and 18 as yet undefined species, and the ITS region or LSU rDNA, or a combination of both, for 91 named and 16 as yet undefined species. Present phylogenetic analyses, based on the three rDNA markers, provide reliable and robust resolution from phylum to species level. Altogether, 109 named species and 27 cultures representing as yet undefined species were analysed. This study provides a reference data set for molecular systematics and environmental community analyses of AMF, including analyses based on deep sequencing.