The epidermal patterning factor (EPF) family of secreted signaling peptides regulate the frequency of stomatal development in model dicot and basal land plant species. Here, we identify and ...manipulate the expression of a barley (Hordeum vulgare) ortholog and demonstrate that when overexpressed HvEPF1 limits entry to, and progression through, the stomatal development pathway. Despite substantial reductions in leaf gas exchange, barley plants with significantly reduced stomatal density show no reductions in grain yield. In addition, HvEPF1OE barley lines exhibit significantly enhanced water use efficiency, drought tolerance, and soil water conservation properties. Our results demonstrate the potential of manipulating stomatal frequency for the protection and optimization of cereal crop yields under future drier environments.
Endosymbiosis allows hosts to acquire new functional traits such that the combined host and endosymbiont can exploit vacant ecological niches and occupy novel environments 1, 2; consequently, ...endosymbiosis affects the structure and function of ecosystems 3, 4. However, for many endosymbioses, it is unknown whether their evolutionary basis is mutualism or exploitation 5–9. We estimated the fitness consequences of symbiosis using the interaction between the protist host Paramecium bursaria and the algal symbiont Chlorella sp. 10. Host fitness was strongly context dependent: whereas hosts benefited from symbiosis at high light intensity, carrying endosymbionts was costly to hosts in the dark and conferred no benefit over growing autonomously at intermediate light levels. Autonomous Chlorella densities increased monotonically with light intensity, whereas per-host symbiont load and symbiont abundance peaked at intermediate light levels and were lowest at high light intensity. This suggests that hosts controlled the costs of symbiosis by manipulating symbiont load according to light intensity. Photosynthetic efficiency was consistently lower for symbiotic compared to autonomous algae, suggesting nutritional constraints upon algae in symbiosis. At intermediate light levels, we observed the establishment of small populations of free-living algae alongside the hosts with endosymbionts, suggesting that symbionts could escape symbiosis, but only under conditions where hosts didn’t benefit from symbiosis. Together, these data suggest that hosts exerted strong control over endosymbionts and that there were no conditions where this nutritional symbiosis was mutually beneficial. Our findings support theoretical predictions (e.g., 5, 9) that controlled exploitation is an important evolutionary pathway toward stable endosymbiosis.
•For protozoa and their algal symbionts, fitness in symbiosis is context dependent•Symbiosis changes from costly to beneficial for hosts with increasing light•Symbiosis is always costly for algae whose interests do not align with the host’s•Evolutionary stability of the symbiosis results from exploitation not mutualism
Lowe et al. show that a photosynthetic symbiosis between an algal symbiont and a protist host is based on exploitation of symbionts by the host, not mutual benefit. Symbiosis becomes more beneficial for hosts with increasing light, but more costly for symbionts, such that the fitness interests of the interacting species do not align.
Arbuscular mycorrhizal fungi (AMF) can transfer nitrogen (N) to host plants, but the ecological relevance is debated, as total plant N and biomass do not generally increase. The extent to which the ...symbiosis is mutually beneficial is thought to rely on the stoichiometry of N, phosphorus (P) and carbon (C) availability. While inorganic N fertilization has been shown to elicit strong mutualism, characterized by improved plant and fungal growth and mineral nutrition, similar responses following organic N addition are lacking. Using a compartmented microcosm experiment, we determined the significance to a mycorrhizal plant of placing a 15N‐labelled, nitrogen‐rich patch of organic matter in a compartment to which only AMF hyphae had access. Control microcosms denied AMF hyphal access to the patch compartment. When permitted access to the patch compartment, the fungus proliferated extensively in the patch and transferred substantial quantities of N to the plant. Moreover, our data demonstrate that allowing hyphal access to an organic matter patch enhanced total plant N and P contents, with a simultaneous and substantial increase in plant biomass. Furthermore, we demonstrate that organic matter fertilization of arbuscular mycorrhizal plants can foster a mutually beneficial symbiosis based on nitrogen transfer, a phenomenon previously thought irrelevant.
When granted access to an organic matter patch, arbuscular mycorrhizal fungi were found to obtain significant amounts of nitrogen (N) from the patch and transfer a substantial amount to their partner plant. The patch‐derived N contributed significantly to, and increased, total plant N. Total plant phosphorus (P) increased also, as did total plant mass. This study is the first to demonstrate simultaneous increases in N, P and biomass of plants with arbuscular mycorrhizal hyphal access to a patch of organic matter.
Manipulation of stomatal density was investigated as a potential tool for enhancing drought tolerance or nutrient uptake.
Drought tolerance and soil water retention were assessed using Arabidopsis ...epidermal patterning factor mutants manipulated to have increased or decreased stomatal density. Root nutrient uptake via mass flow was monitored under differing plant watering regimes using nitrogen-15 (15N) isotope and mass spectrometry.
Plants with less than half of their normal complement of stomata, and correspondingly reduced levels of transpiration, conserve soil moisture and are highly drought tolerant but show little or no reduction in shoot nitrogen concentrations especially when water availability is restricted. By contrast, plants with over twice the normal density of stomata have a greater capacity for nitrogen uptake, except when water availability is restricted.
We demonstrate the possibility of producing plants with reduced transpiration which have increased drought tolerance, with little or no loss of nutrient uptake. We demonstrate that increasing transpiration can enhance nutrient uptake when water is plentiful.
Endosymbiosis drives evolutionary innovation and underpins the function of diverse ecosystems. The mechanistic origins of symbioses, however, remain unclear, in part because early evolutionary events ...are obscured by subsequent evolution and genetic drift. This Essay highlights how experimental studies of facultative, host-switched, and synthetic symbioses are revealing the important role of fitness trade-offs between within-host and free-living niches during the early-stage evolution of new symbiotic associations. The mutational targets underpinning such trade-offs are commonly regulatory genes, such that single mutations have major phenotypic effects on multiple traits, thus enabling and reinforcing the transition to a symbiotic lifestyle.
•We propose a novel four-phase model of mycorrhiza-induced resistance (MIR).•Phase I: root exudation of mycorrhiza-recruiting chemicals.•Phase II: the plant immune system responding to infection by ...abuscular mycorrhizal fungi (AMF).•Phase III: immune suppression by AMF and recruitment of mycorrhizosphere bacteria.•Phase IV: establishment of the mycorrhizosphere and induction of systemic resistance by mycorrhizosphere bacteria.
Plants can develop an enhanced defensive capacity in response to infection by arbuscular mycorrhizal fungi (AMF). This ‘mycorrhiza-induced resistance’ (MIR) provides systemic protection against a wide range of attackers and shares characteristics with systemic acquired resistance (SAR) after pathogen infection and induced systemic resistance (ISR) following root colonisation by non-pathogenic rhizobacteria. It is commonly assumed that fungal stimulation of the plant immune system is solely responsible for MIR. In this opinion article, we present a novel model of MIR that integrates different aspects of the induced resistance phenomenon. We propose that MIR is a cumulative effect of direct plant responses to mycorrhizal infection and indirect immune responses to ISR-eliciting rhizobacteria in the mycorrhizosphere.
The discovery that Mucoromycotina, an ancient and partially saprotrophic fungal lineage, associates with the basal liverwort lineage Haplomitriopsida casts doubt on the widely held view that ...Glomeromycota formed the sole ancestral plant–fungus symbiosis. Whether this association is mutualistic, and how its functioning was affected by the fall in atmospheric CO₂concentration that followed plant terrestrialization in the Palaeozoic, remains unknown. We measured carbon‐for‐nutrient exchanges between Haplomitriopsida liverworts and Mucoromycotina fungi under simulated mid‐Palaeozoic (1500 ppm) and near‐contemporary (440 ppm) CO₂concentrations using isotope tracers, and analysed cytological differences in plant–fungal interactions. Concomitantly, we cultured both partners axenically, resynthesized the associations in vitro, and characterized their cytology. We demonstrate that liverwort–Mucoromycotina symbiosis is mutualistic and mycorrhiza‐like, but differs from liverwort–Glomeromycota symbiosis in maintaining functional efficiency of carbon‐for‐nutrient exchange between partners across CO₂concentrations. Inoculation of axenic plants with Mucoromycotina caused major cytological changes affecting the anatomy of plant tissues, similar to that observed in wild‐collected plants colonized by Mucoromycotina fungi. By demonstrating reciprocal exchange of carbon for nutrients between partners, our results provide support for Mucoromycotina establishing the earliest mutualistic symbiosis with land plants. As symbiotic functional efficiency was not compromised by reduced CO₂, we suggest that other factors led to the modern predominance of the Glomeromycota symbiosis.
The rhizobiome is an important regulator of plant growth and health. Plants shape their rhizobiome communities through production and release of primary and secondary root metabolites. Benzoxazinoids ...(BXs) are common tryptophan-derived secondary metabolites in grasses that regulate belowground and aboveground biotic interactions. In addition to their biocidal activity, BXs can regulate plant-biotic interactions as semiochemicals or within-plant defence signals. However, the full extent and mechanisms by which BXs shape the root-associated microbiome has remained largely unexplored. Here, we have taken a global approach to examine the regulatory activity of BXs on the maize root metabolome and associated bacterial and fungal communities. Using untargeted mass spectrometry analysis in combination with prokaryotic and fungal amplicon sequencing, we compared the impacts of three genetic mutations in different steps in the BX pathway. We show that BXs regulate global root metabolism and concurrently influence the rhizobiome in a root type-dependent manner. Correlation analysis between BX-controlled root metabolites and bacterial taxa suggested a dominant role for BX-dependent metabolites, particularly flavonoids, in constraining a range of soil microbial taxa, while stimulating methylophilic bacteria. Our study supports a multilateral model by which BXs control root-microbe interactions via a global regulatory function in root secondary metabolism.
• Liverworts, which are amongst the earliest divergent plant lineages and important ecosystem pioneers, often form nutritional mutualisms with arbuscular mycorrhiza-forming Glomeromycotina and ...fine-root endophytic Mucoromycotina fungi, both of which coevolved with early land plants. Some liverworts, in common with many later divergent plants, harbour both fungal groups, suggesting these fungi may complementarily improve plant access to different soil nutrients.
• We tested this hypothesis by growing liverworts in single and dual fungal partnerships under a modern atmosphere and under 1500 ppm CO₂, as experienced by early land plants. Access to soil nutrients via fungal partners was investigated with 15N-labelled algal necromass and 33P orthophosphate. Photosynthate allocation to fungi was traced using 14CO₂.
• Only Mucoromycotina fungal partners provided liverworts with substantial access to algal 15N, irrespective of atmospheric CO₂ concentration. Both symbionts increased 33P uptake, but Glomeromycotina were often more effective. Dual partnerships showed complementarity of nutrient pool use and greatest photosynthate allocation to symbiotic fungi.
• We show there are important functional differences between the plant–fungal symbioses tested, providing new insights into the functional biology of Glomeromycotina and Mucoromycotina fungal groups that form symbioses with plants. This may explain the persistence of the two fungal lineages in symbioses across the evolution of land plants.
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