Anti-herbivory defences delivered by Epichloë fungal endophytes: a quantitative review of alkaloid concentration variation among hosts and plant parts.

BACKGROUND AND AIMS: In the subfamily Poöideae (Poaceae), certain grass species possess anti-herbivore alkaloids synthesized by fungal endophytes that belong to the genus Epichloë (Clavicipitaceae). The protective role of these symbiotic endophytes can vary, depending on alkaloid concentrations within specific plant-endophyte associations and plant parts. METHODS: We conducted a literature review to identify articles containing alkaloid concentration data for various plant parts in six important pasture species, Lolium arundinaceum, Lolium perenne, Lolium pratense, Lolium multiflorum|Lolium rigidum and Festuca rubra, associated with their common endophytes. We considered the alkaloids lolines (1-aminopyrrolizidines), peramine (pyrrolopyrazines), ergovaline (ergot alkaloids) and lolitrem B (indole-diterpenes). While all these alkaloids have shown bioactivity against insect herbivores, ergovaline and lolitrem B are harmful for mammals. KEY RESULTS: Loline alkaloid levels were higher in the perennial grasses L. pratense and L. arundinaceum compared to the annual species L. multiflorum and L. rigidum, and higher in reproductive tissues than in vegetative structures. This is probably due to the greater biomass accumulation in perennial species that can result in higher endophyte mycelial biomass. Peramine concentrations were higher in L. perenne than in L. arundinaceum and not affected by plant part. This can be attributed to the high within-plant mobility of peramine. Ergovaline and lolitrem B, both hydrophobic compounds, were associated with plant parts where fungal mycelium is usually present, and their concentrations were higher in plant reproductive tissues. Only loline alkaloid data were sufficient for below-ground tissue analyses and concentrations were lower than in above-ground parts. CONCLUSIONS: Our study provides a comprehensive synthesis of fungal alkaloid variation across host grasses and plant parts, essential for understanding the endophyte-conferred defence extent. The patterns can be understood by considering endophyte growth within the plant and alkaloid mobility. Our study identifies research gaps, including the limited documentation of alkaloid presence in roots and the need to investigate the influence of different environmental conditions.

Inoculation with extreme endophytes improves performance and nutritional quality in crop species grown under exoplanetary conditions.

Introduction: Technological advances have made possible long space travels and even exoplanetary colonies in the future. Nevertheless, the success of these activities depends on our ability to produce edible plants in stressful conditions such as high radiation, extreme temperatures and low oxygen levels. Since beneficial microorganisms, such as fungal endophytes from extreme environments, have helped agriculture cope with those difficulties, endophytic fungi may be a putative tool to ensure plant growth under exoplanetary conditions. Additionally, growing crops in polyculture has been shown to increase productivity and spatial efficiency, which is essential given the likely space restrictions in such conditions. Methods: We evaluated the effect of the inoculation with a mix of two fungal endophytes from the Atacama Desert on performance (survival and biomass) and nutritional quality of three crop species (lettuce, chard and spinach) grown under exoplanetary conditions. In addition, we measured the amount of antioxidants (flavonoids and phenolics) as possible mechanisms to cope with such abiotic conditions. The exoplanetary conditions were; high UV radiation, low temperature, low water availability, and low oxygen levels. These crops were put in growing chambers in monoculture, dual culture and polyculture (the three species in the same pot) for 30 days. Results and Discussion: Our results show that inoculation with extreme endophytes improved survival by ca. 15 - 35% and biomass by ca. 30 - 35% in all crop species. The most evident increase was when grown in polyculture, except for survival in spinach, where inoculated plants had higher survival only in dual culture. Nutritional quality and the amount of the antioxidant compounds antioxidants increased in all crop species when inoculated with the endophytes. Overall, fungal endophytes isolated from extreme environments such as the Atacama Desert, the driest desert in the world, could be a key biotechnological tool for future space agriculture, helping plants cope with environmental stress. Additionally, inoculated plants should be grown in polyculture to increase crop turnover and space-use efficiency. Lastly, these results provide useful insights to face the future challenges of space-farming.

Changes in Diversity and Community Composition of Root Endophytic Fungi Associated with Aristolochia chilensis along an Aridity Gradient in the Atacama Desert.

Despite the widespread occurrence of fungal endophytes (FE) in plants inhabiting arid ecosystems, the environmental and soil factors that modulate changes in FE diversity and community composition along an aridity gradient have been little explored. We studied three locations along the coast of the Atacama Desert in Chile, in which the plant Aristolochia chilensis naturally grows, and that differ in their aridity gradient from hyper-arid to semi-arid. We evaluated if root-associated FE diversity (frequency, richness and diversity indexes) and community composition vary as a function of aridity. Additionally, we assessed whether edaphic factors co-varying with aridity (soil water potential, soil moisture, pH and nutrients) may structure FE communities. We expected that FE diversity would gradually increase towards the aridity gradient declines, and that those locations that had the most contrasting environments would show more dissimilar FE communities. We found that richness indexes were inversely related to aridity, although this pattern was only partially observed for FE frequency and diversity. FE community composition was dissimilar among contrasting locations, and soil water availability significantly influenced FE community composition across the gradient. The results indicate that FE diversity and community composition associated with A. chilensis relate to differences in the aridity level across the gradient. Overall, our findings reveal the importance of climate-related factors in shaping changes in diversity, structure and distribution of FE in desert ecosystems.

Endophytic bacterial communities are associated with leaf mimicry in the vine Boquila trifoliolata.

The mechanisms behind the unique capacity of the vine Boquila trifoliolata to mimic the leaves of several tree species remain unknown. A hypothesis in the original leaf mimicry report considered that microbial vectors from trees could carry genes or epigenetic factors that would alter the expression of leaf traits in Boquila. Here we evaluated whether leaf endophytic bacterial communities are associated with the mimicry pattern. Using 16S rRNA gene sequencing, we compared the endophytic bacterial communities in three groups of leaves collected in a temperate rainforest: (1) leaves from the model tree Rhaphithamnus spinosus (RS), (2) Boquila leaves mimicking the tree leaves (BR), and (3) Boquila leaves from the same individual vine but not mimicking the tree leaves (BT). We hypothesized that bacterial communities would be more similar in the BR-RS comparison than in the BT-RS comparison. We found significant differences in the endophytic bacterial communities among the three groups, verifying the hypothesis. Whereas non-mimetic Boquila leaves and tree leaves (BT-RS) showed clearly different bacterial communities, mimetic Boquila leaves and tree leaves (BR-RS) showed an overlap concerning their bacterial communities. The role of bacteria in this unique case of leaf mimicry should be studied further.

Global trends in phenotypic plasticity of plants.

Predicting plastic responses is crucial to assess plant species potential to adapt to climate change, but little is known about which factors drive the biogeographical patterns of phenotypic plasticity in plants. Theory predicts that climatic variability would select for increased phenotypic plasticity, whereas evidence indicates that stressful conditions can limit phenotypic plasticity. Using a meta-analytic, phylogeny-corrected approach to global data on plant phenotypic plasticity, we tested whether latitude, climate, climatic variability and/or stressful conditions are predictors of plastic responses at a biogeographical scale. We found support for a positive association between phenotypic plasticity and climatic variability only for plasticity in allocation. Plasticity in leaf morphology, size and physiology were positively associated with mean annual temperature. We also found evidence that phenotypic plasticity in physiology is limited by cold stress. Overall, plant plastic responses to non-climatic factors were stronger than responses to climatic factors. However, while climatic conditions were associated with plant plastic responses to climatic factors, they generally did not relate to plastic responses to other abiotic or biotic factors. Our study highlights the need to consider those factors that favour and limit phenotypic plasticity in order to improve predictive frameworks addressing plant species' potential to adapt to climate change.

Disturbance reinforces community assembly processes differentially across spatial scales.

BACKGROUND AND AIMS: There is a paucity of empirical research and a lack of predictive models concerning the interplay between spatial scale and disturbance as they affect the structure and assembly of plant communities. We proposed and tested a trait dispersion-based conceptual model hypothesizing that disturbance reinforces assembly processes differentially across spatial scales. Disturbance would reinforce functional divergence at the small scale (neighbourhood), would not affect functional dispersion at the intermediate scale (patch) and would reinforce functional convergence at the large scale (site). We also evaluated functional and species richness of native and exotic plants to infer underlying processes. Native and exotic species richness were expected to increase and decrease with disturbance, respectively, at the neighbourhood scale, and to show similar associations with disturbance at the patch (concave) and site (negative) scales. METHODS: In an arid shrubland, we estimated species richness and functional dispersion and richness within 1 m2 quadrats (neighbourhood) nested within 100 m2 plots (patch) along a small-scale natural disturbance gradient caused by an endemic fossorial rodent. Data for the site scale (2500 m2 plots) were taken from a previous study. We also tested the conceptual model through a quantitative literature review and a meta-analysis. KEY RESULTS: As spatial scale increased, disturbance sequentially promoted functional divergence, random trait dispersion and functional convergence. Functional richness was unaffected by disturbance across spatial scales. Disturbance favoured natives over exotics at the neighbourhood scale, while both decreased under high disturbance at the patch and site scales. CONCLUSIONS: The results supported the hypothesis that disturbance reinforces assembly processes differentially across scales and hampers plant invasion. The quantitative literature review and the meta-analysis supported most of the model predictions.

Disturbance by an endemic rodent in an arid shrubland is a habitat filter: effects on plant invasion and taxonomical, functional and phylogenetic community structure.

Background and Aims: Disturbance often drives plant invasion and may modify community assembly. However, little is known about how these modifications of community patterns occur in terms of taxonomic, functional and phylogenetic structure. This study evaluated in an arid shrubland the influence of disturbance by an endemic rodent on community functional divergence and phylogenetic structure as well as on plant invasion. It was expected that disturbance would operate as a habitat filter favouring exotic species with short life cycles. Methods: Sixteen plots were sampled along a disturbance gradient caused by the endemic fossorial rodent Spalacopus cyanus , measuring community parameters and estimating functional divergence for life history traits (functional dispersion index) and the relative contribution to functional divergence of exotic and native species. The phylogenetic signal (Pagel's lambda) and phylogenetic community structure (mean phylogenetic distance and mean nearest taxon phylogenetic distance) were also estimated. The use of a continuous approach to the disturbance gradient allowed the identification of non-linear relationships between disturbance and community parameters. Key Results: The relationship between disturbance and both species richness and abundance was positive for exotic species and negative for native species. Disturbance modified community composition, and exotic species were associated with more disturbed sites. Disturbance increased trait convergence, which resulted in phylogenetic clustering because traits showed a significant phylogenetic signal. The relative contribution of exotic species to functional divergence increased, while that of natives decreased, with disturbance. Exotic and native species were not phylogenetically distinct. Conclusions: Disturbance by rodents in this arid shrubland constitutes a habitat filter over phylogeny-dependent life history traits, leading to phylogenetic clustering, and drives invasion by favouring species with short life cycles. Results can be explained by high phenotypic and phylogenetic resemblance between exotic and native species. The use of continuous gradients when studying the effects of disturbance on community assembly is advocated.

Evaluating Darwin's naturalization hypothesis in experimental plant assemblages: phylogenetic relationships do not determine colonization success.

Darwin's naturalization hypothesis (DNH) proposes that colonization is less likely when the colonizing species is related to members of the invaded community, because evolutionary closeness intensifies competition among species that share similar resources. Studies that have evaluated DNH from correlational evidence have yielded controversial results with respect to its occurrence and generality. In the present study we carried out a set of manipulative experiments in which we controlled the phylogenetic relatedness of one colonizing species (Lactuca sativa) with five assemblages of plants (the recipient communities), and evaluated the colonizing success using five indicators (germination, growth, flowering, survival, and recruitment). The evolutionary relatedness was calculated as the mean phylogenetic distance between Lactuca and the members of each assemblage (MPD) and by the mean phylogenetic distance to the nearest neighbor (MNND). The results showed that the colonization success of Lactuca was not affected by MPD or MNND values, findings that do not support DNH. These results disagree with experimental studies made with communities of microorganisms, which show an inverse relation between colonization success and phylogenetic distances. We suggest that these discrepancies may be due to the high phylogenetic distance used, since in our experiments the colonizing species (Lactuca) was a distant relative of the assemblage members, while in the other studies the colonizing taxa have been related at the congeneric and conspecific levels. We suggest that under field conditions the phylogenetic distance is a weak predictor of competition, and it has a limited role in determining colonization success, contrary to prediction of the DNH. More experimental studies are needed to establish the importance of phylogenetic distance between colonizing species and invaded community on colonization success.