The Influence of Arbuscular Mycorrhizal Fungi on Plant Reproduction.

Arbuscular mycorrhizal (AM) fungi can influence all components of plant reproduction including pollen delivery, pollen germination, pollen tube growth, fertilization, and seed germination. AM fungi associate with plant roots, uptake nutrients, and prime plants for faster defense responses. Our literature review first identified four testable hypotheses describing how AM fungi could alter pollen delivery: (1) We hypothesize AM fungi promote floral display size. The influence of AM fungi on flower size and number is supported by literature, however there are no studies on floral color. (2) We hypothesize AM fungi promote pollen and nectar quality and quantity, and, as reported before, AM fungi promote male fitness over female fitness. (3) We hypothesize AM fungi promote both earlier and longer flowering times, but we found no consistent trend in the data for earlier or later or longer flowering times. (4) We hypothesize AM fungi alter floral secondary chemistry and VOCs, and find there is clear evidence for the alteration of floral chemistry but little data on VOCs. Second, we focus on how AM fungi could alter pollen germination, pollen tube growth, and fertilization, and present three testable hypotheses. We found evidence that AM fungi influence pollen germination and pollen tube growth, production of seeds, and seed germination. However, while most of these influences are positive they are not conclusive, because studies have been conducted in small numbers of systems and groups. Therefore, we conclude that the majority of research to date may not be measuring the influence of AM fungi on the most important components of plant reproduction: pollen germination, pollen tube growth, fertilization, and seed germination.

Experimentally altered rainfall regimes and host root traits affect grassland arbuscular mycorrhizal fungal communities.

Future climate scenarios predict changes in rainfall regimes. These changes are expected to affect plants via effects on the expression of root traits associated with water and nutrient uptake. Associated microorganisms may also respond to these new precipitation regimes, either directly in response to changes in the soil environment or indirectly in response to altered root trait expression. We characterized arbuscular mycorrhizal (AM) fungal communities in an Australian grassland exposed to experimentally altered rainfall regimes. We used Illumina sequencing to assess the responses of AM fungal communities associated with four plant species sampled in different watering treatments and evaluated the extent to which shifts were associated with changes in root traits. We observed that altered rainfall regimes affected the composition but not the richness of the AM fungal communities, and we found distinctive communities in the increased rainfall treatment. We found no evidence of altered rainfall regime effects via changes in host physiology because none of the studied traits were affected by changes in rainfall. However, specific root length was observed to correlate with AM fungal richness, while concentrations of phosphorus and calcium in root tissue and the proportion of root length allocated to fine roots were correlated to community composition. Our study provides evidence that climate change and its effects on rainfall may influence AM fungal community assembly, as do plant traits related to plant nutrition and water uptake. We did not find evidence that host responses to altered rainfall drive AM fungal community assembly in this grassland ecosystem.

Priorities for research in soil ecology.

The ecological interactions that occur in and with soil are of consequence in many ecosystems on the planet. These interactions provide numerous essential ecosystem services, and the sustainable management of soils has attracted increasing scientific and public attention. Although soil ecology emerged as an independent field of research many decades ago, and we have gained important insights into the functioning of soils, there still are fundamental aspects that need to be better understood to ensure that the ecosystem services that soils provide are not lost and that soils can be used in a sustainable way. In this perspectives paper, we highlight some of the major knowledge gaps that should be prioritized in soil ecological research. These research priorities were compiled based on an online survey of 32 editors of Pedobiologia - Journal of Soil Ecology. These editors work at universities and research centers in Europe, North America, Asia, and Australia.The questions were categorized into four themes: (1) soil biodiversity and biogeography, (2) interactions and the functioning of ecosystems, (3) global change and soil management, and (4) new directions. The respondents identified priorities that may be achievable in the near future, as well as several that are currently achievable but remain open. While some of the identified barriers to progress were technological in nature, many respondents cited a need for substantial leadership and goodwill among members of the soil ecology research community, including the need for multi-institutional partnerships, and had substantial concerns regarding the loss of taxonomic expertise.

Stressed out symbiotes: hypotheses for the influence of abiotic stress on arbuscular mycorrhizal fungi.

Abiotic stress is a widespread threat to both plant and soil communities. Arbuscular mycorrhizal (AM) fungi can alleviate effects of abiotic stress by improving host plant stress tolerance, but the direct effects of abiotic stress on AM fungi are less well understood. We propose two hypotheses predicting how AM fungi will respond to abiotic stress. The stress exclusion hypothesis predicts that AM fungal abundance and diversity will decrease with persistent abiotic stress. The mycorrhizal stress adaptation hypothesis predicts that AM fungi will evolve in response to abiotic stress to maintain their fitness. We conclude that abiotic stress can have effects on AM fungi independent of the effects on the host plant. AM fungal communities will change in composition in response to abiotic stress, which may mean the loss of important individual species. This could alter feedbacks to the plant community and beyond. AM fungi will adapt to abiotic stress independent of their host plant. The adaptation of AM fungi to abiotic stress should allow the maintenance of the plant-AM fungal mutualism in the face of changing climates.

Plant lignin content altered by soil microbial community.

Questions have been raised in various fields of research about the consequences of plants with modified lignin production. As a result of their roles in nutrient cycling and plant diversity, plant-soil interactions should be a major focus of ecological studies on lignin-modified plants. However, most studies have been decomposition studies conducted in a single soil or in sterile soil. Thus, we understand little about plant-soil interactions in living lignin-modified plants. In lignin mutants of three different barley (Hordeum vulgare) cultivars and their corresponding wild-types associated with three different soil microbial communities, we asked: do plant-soil microbiome interactions influence the lignin content of plants?; does a mutation in lignin production alter the outcome of plant-soil microbiome interactions?; does the outcome of plant-soil microbiome interactions depend on host genotype or the presence of a mutation altering lignin production? In roots, the soil community explained 6% of the variation in lignin content, but, in shoots, the soil community explained 21% of the variation in lignin content and was the only factor influencing lignin content. Neither genotype nor mutations in lignin production explained associations with fungi. Lignin content changes in response to a plant's soil microbial community, and may be a defensive response to particular components of the soil community.

Improving intercropping: a synthesis of research in agronomy, plant physiology and ecology.

Intercropping is a farming practice involving two or more crop species, or genotypes, growing together and coexisting for a time. On the fringes of modern intensive agriculture, intercropping is important in many subsistence or low-input/resource-limited agricultural systems. By allowing genuine yield gains without increased inputs, or greater stability of yield with decreased inputs, intercropping could be one route to delivering 'sustainable intensification'. We discuss how recent knowledge from agronomy, plant physiology and ecology can be combined with the aim of improving intercropping systems. Recent advances in agronomy and plant physiology include better understanding of the mechanisms of interactions between crop genotypes and species ­ for example, enhanced resource availability through niche complementarity. Ecological advances include better understanding of the context-dependency of interactions, the mechanisms behind disease and pest avoidance, the links between above- and below-ground systems, and the role of microtopographic variation in coexistence. This improved understanding can guide approaches for improving intercropping systems, including breeding crops for intercropping. Although such advances can help to improve intercropping systems, we suggest that other topics also need addressing. These include better assessment of the wider benefits of intercropping in terms of multiple ecosystem services, collaboration with agricultural engineering, and more effective interdisciplinary research.

Herbivore-mediated material fluxes in a northern deciduous forest under elevated carbon dioxide and ozone concentrations.

Anthropogenic changes in atmospheric carbon dioxide (CO2 ) and ozone (O3 ) are known to alter tree physiology and growth, but the cascading effects on herbivore communities and herbivore-mediated nutrient cycling are poorly understood. We sampled herbivore frass, herbivore-mediated greenfall, and leaf-litter deposition in temperate forest stands under elevated CO2 (c. 560 ppm) and O3 (c. 1.5× ambient), analyzed substrate chemical composition, and compared the quality and quantity of fluxes under multiple atmospheric treatments. Leaf-chewing herbivores fluxed 6.2 g m(-2)  yr(-1) of frass and greenfall from the canopy to the forest floor, with a carbon : nitrogen (C : N) ratio 32% lower than that of leaf litter. Herbivore fluxes of dry matter, C, condensed tannins, and N increased under elevated CO2 (35, 32, 63 and 39%, respectively), while fluxes of N decreased (18%) under elevated O3 . Herbivore-mediated dry matter inputs scaled across atmospheric treatments as a constant proportion of leaf-litter inputs. Increased fluxes under elevated CO2 were consistent with increased herbivore consumption and abundance, and with increased plant growth and soil respiration, previously reported for this experimental site. Results suggest that insect herbivory will reinforce other factors, such as photosynthetic rate and fine-root production, impacting C sequestration by forests in future environments.

Soil microbiota and herbivory drive the assembly of tomato plant-associated microbial communities through different mechanisms.

Plant-associated microbial communities are key to shaping many aspects of plant biology. In this study, we tested whether soil microbial communities and herbivory influence the bacterial community of tomato plants and whether their influence in different plant compartments is driven by microbial spillover between compartments or whether plants are involved in mediating this effect. We grew our plants in soils hosting three different microbial communities and covered (or not) the soil surface to prevent (or allow) passive microbial spillover between compartments, and we exposed them (or not) to herbivory by Manduca sexta. Here we show that the soil-driven effect on aboveground compartments is consistently detected regardless of soil coverage, whereas soil cover influences the herbivore-driven effect on belowground microbiota. Together, our results suggest that the soil microbiota influences aboveground plant and insect microbial communities via changes in plant metabolism and physiology or by sharing microorganisms via xylem sap. In contrast, herbivores influence the belowground plant microbiota via a combination of microbial spillover and changes in plant metabolism. These results demonstrate the important role of plants in linking aboveground and belowground microbiota, and can foster further research on soil microbiota manipulation for sustainable pest management.

Identification and quantification of pigments in plant leaves using thin layer chromatography-Raman spectroscopy (TLC-Raman).

Carotenoids are yellow, orange, and red pigments commonly found in plants. In leaves, these molecules are essential for photosynthesis, but they also play a major role in plant growth and development. Efficiently monitoring concentrations of specific carotenoids in plant tissues could help to explain plant responses to environmental stressors, infection and disease, fertilization, and other conditions. Previously, Raman methods have been used to demonstrate a correlation between plant fitness and the carotenoid content of leaves. Due to solvatochromatic effects and structural similarities within the carotenoid family, current Raman spectroscopy techniques struggle to assign signals to specific carotenoids with certainty, complicating the determination of amounts of individual carotenoids present in a sample. In this work, we use thin layer chromatography-Raman spectroscopy, or TLC-Raman, to identify and quantify carotenoids extracted from tomato leaves. These quick and accurate methods could be applied to study the relationship between pigment content and a number of factors affecting plant health.

Unpredicted impacts of insect endosymbionts on interactions between soil organisms, plants and aphids.

Ecologically significant symbiotic associations are frequently studied in isolation, but such studies of two-way interactions cannot always predict the responses of organisms in a community setting. To explore this issue, we adopt a community approach to examine the role of plant-microbial and insect-microbial symbioses in modulating a plant-herbivore interaction. Potato plants were grown under glass in controlled conditions and subjected to feeding from the potato aphid Macrosiphum euphorbiae. By comparing plant growth in sterile, uncultivated and cultivated soils and the performance of M. euphorbiae clones with and without the facultative endosymbiont Hamiltonella defensa, we provide evidence for complex indirect interactions between insect- and plant-microbial systems. Plant biomass responded positively to the live soil treatments, on average increasing by 15% relative to sterile soil, while aphid feeding produced shifts (increases in stem biomass and reductions in stolon biomass) in plant resource allocation irrespective of soil treatment. Aphid fecundity also responded to soil treatment with aphids on sterile soil exhibiting higher fecundities than those in the uncultivated treatment. The relative allocation of biomass to roots was reduced in the presence of aphids harbouring H. defensa compared with plants inoculated with H. defensa-free aphids and aphid-free control plants. This study provides evidence for the potential of plant and insect symbionts to shift the dynamics of plant-herbivore interactions.

Spore traits mediate disturbance effects on arbuscular mycorrhizal fungal community composition and mutualisms.

Trait-based approaches in ecology are powerful tools for understanding how organisms interact with their environment. These approaches show particular promise in disturbance and community ecology contexts for understanding how disturbances like prescribed fire and bison grazing influence interactions between mutualists like arbuscular mycorrhizal (AM) fungi and their plant hosts. In this work we examined how disturbance effects on AM fungal spore community composition and mutualisms were mediated by selection for specific functional spore traits at both the species and community level. We tested these questions by analyzing AM fungal spore communities and traits from a frequently burned and grazed (bison) tallgrass prairie system and using these spores to inoculate a plant growth response experiment. Selection for darker, pigmented AM fungal spores, changes in the abundance and volume of individual AM fungal taxa, and altered sporulation, were indicators of fire and grazing effects on AM fungal community composition. Disturbance associated changes in AM fungal community composition were then correlated with altered growth responses of Schizachyrium scoparium grass. Our work shows that utilization of trait-based approaches in ecology can clarify the mechanisms that underly belowground responses to disturbance, and provide a useful framework for understanding interactions between organisms and their environment.

The Costs and Benefits of Plant-Arbuscular Mycorrhizal Fungal Interactions.

The symbiotic interaction between plants and arbuscular mycorrhizal (AM) fungi is often perceived as beneficial for both partners, though a large ecological literature highlights the context dependency of this interaction. Changes in abiotic variables, such as nutrient availability, can drive the interaction along the mutualism-parasitism continuum with variable outcomes for plant growth and fitness. However, AM fungi can benefit plants in more ways than improved phosphorus nutrition and plant growth. For example, AM fungi can promote abiotic and biotic stress tolerance even when considered parasitic from a nutrient provision perspective. Other than being obligate biotrophs, very little is known about the benefits AM fungi gain from plants. In this review, we utilize both molecular biology and ecological approaches to expand our understanding of the plant-AM fungal interaction across disciplines.

Multiple mechanisms enable invasive species to suppress native species.

PREMISE OF THE STUDY: Invasive plants represent a significant threat to ecosystem biodiversity. To decrease the impacts of invasive species, a major scientific undertaking of the last few decades has been aimed at understanding the mechanisms that drive invasive plant success. Most studies and theories have focused on a single mechanism for predicting the success of invasive plants and therefore cannot provide insight as to the relative importance of multiple interactions in predicting invasive species' success. METHODS: We examine four mechanisms that potentially contribute to the success of invasive velvetgrass Holcus lanatus: direct competition, indirect competition mediated by mammalian herbivores, interference competition via allelopathy, and indirect competition mediated by changes in the soil community. Using a combination of field and greenhouse approaches, we focus on the effects of H. lanatus on a common species in California coastal prairies, Erigeron glaucus, where the invasion is most intense. KEY RESULTS: We found that H. lanatus had the strongest effects on E. glaucus via direct competition, but it also influenced the soil community in ways that feed back to negatively influence E. glaucus and other native species after H. lanatus removal. CONCLUSIONS: This approach provided evidence for multiple mechanisms contributing to negative effects of invasive species, and it identified when particular strategies were most likely to be important. These mechanisms can be applied to eradication of H. lanatus and conservation of California coastal prairie systems, and they illustrate the utility of an integrated set of experiments for determining the potential mechanisms of invasive species' success.

Herbivory shapes the rhizosphere bacterial microbiota in potato plants.

Plant-associated microbiomes assist their host in a variety of activities, spanning from nutrition to defence against herbivores and diseases. Previous research showed that plant-associated microbiomes shift their composition when plants are exposed to stressors, including herbivory. However, existing studies explored only single herbivore-plant combinations, whereas plants are often attacked by several different herbivores, but the effects of multiple herbivore types on the plant microbiome remain to be determined. Here, we first tested whether feeding by different herbivores (aphids, nematodes and slugs) produces a shift in the rhizosphere bacterial microbiota associated with potato plants. Then, we expanded this question asking whether the identity of the herbivore produces different effects on the rhizosphere microbial community. While we found shifts in microbial diversity and structure due to herbivory, we observed that the herbivore identity does not influence the diversity or community structure of bacteria thriving in the rhizosphere. However, a deeper analysis revealed that the herbivores differentially affected the structure of the network of microbial co-occurrences. Our results have the potential to increase our ability to predict how plant microbiomes assemble and aid our understanding of the role of plant microbiome in plant responses to biotic stress.

Climate change influences mycorrhizal fungal-plant interactions, but conclusions are limited by geographical study bias.

Climate change is altering the interactions among plants and soil organisms in ways that will alter the structure and function of ecosystems. We reviewed the literature and developed a map of studies focused on how the three most common types of mycorrhizal fungi (arbuscular mycorrhizal [AM], ectomycorrhizal [EcM], and ericoid mycorrhizal [ErM] fungi) respond to elevated atmospheric carbon dioxide concentrations (eCO2 ), climatic warming, and changes in the distribution of precipitation. Broadly, we ask how do mycorrhizal fungi respond to climate change, how do these responses vary by fungal type, and how do mycorrhizal traits influence plant adaptation, movement, or extinction in response to climatic change? First, we found that 92% of studies were conducted in the northern hemisphere, and plant host, ecosystem type and study location were only correlated with each other in the northern hemisphere because studies across all mycorrhizal fungal types were only common in the northern hemisphere. Second, we show that temperature and rainfall variability had more variable effects than eCO2 on mycorrhizal fungal structures, but these effects were context dependent. Third, while mycorrhizal fungal types vary in their responses to climate change, it appears that warming leads to more variable responses in ectomycorrhizal than in arbuscular mycorrhizal fungi. Finally, we discuss common traits of mycorrhizal fungi that could aid in fungal and plant adaption to climate change. We posit that mycorrhizal fungi can buffer plant hosts against extinction risk, they can facilitate or retard the dispersal success of plants moving away from poor environments, and, by buffering host plants, they can enable host plant adaptation to new climates. All of these influences are, however, context dependent a finding that reflects the complex traits of mycorrhizal fungi as a group, the diversity of plant species they associate with and the variation in ecosystems in which they reside. Overall, while we point out many gaps in our understanding of the influence of climate changes on mycorrhizal fungi, we also highlight the large number of opportunities for researching plant and mycorrhizal fungal responses to and mitigation of climate changes.

Biological invasions alter environmental microbiomes: A meta-analysis.

Biological invasions impact both agricultural and natural systems. The damage can be quantified in terms of both economic loss and reduction of biodiversity. Although the literature is quite rich about the impact of invasive species on plant and animal communities, their impact on environmental microbiomes is underexplored. Here, we re-analyze publicly available data using a common framework to create a global synthesis of the effects of biological invasions on environmental microbial communities. Our findings suggest that non-native species are responsible for the loss of microbial diversity and shifts in the structure of microbial populations. Therefore, the impact of biological invasions on native ecosystems might be more pervasive than previously thought, influencing both macro- and micro-biomes. We also identified gaps in the literature which encourage research on a wider variety of environments and invaders, and the influence of invaders across seasons and geographical ranges.

Bacterial disease induced changes in fungal communities of olive tree twigs depend on host genotype.

In nature, pathogens live and interact with other microorganisms on plant tissues. Yet, the research area exploring interactions between bacteria-fungi and microbiota-plants, within the context of a pathobiome, is still scarce. In this study, the impact of olive knot (OK) disease caused by the bacteria Pseudomonas savastanoi pv. savastanoi (Psv) on the epiphytic and endophytic fungal communities of olive tree twigs from three different cultivars, was investigated in field conditions. The ITS-DNA sequencing of cultivable fungi, showed that OK disease disturbs the resident fungal communities, which may reflect changes in the habitat caused by Psv. In particular, a reduction on epiphyte abundance and diversity, and changes on their composition were observed. Compared to epiphytes, endophytes were less sensitive to OK, but their abundance, in particular of potential pathogens, was increased in plants with OK disease. Host genotype, at cultivar level, contributed to plant fungal assembly particularly upon disease establishment. Therefore, besides fungi - Psv interactions, the combination of cultivar - Psv also appeared to be critical for the composition of fungal communities in olive knots. Specific fungal OTUs were associated to the presence and absence of disease, and their role in the promotion or suppression of OK disease should be studied in the future.

Mycorrhizal species differentially alter plant growth and response to herbivory.

Plants simultaneously interact with multiple organisms which can both positively and negatively affect their growth. Herbivores can reduce plant growth through loss of plant biomass and photosynthetic area, while plant mutualists, such as mycorrhizal fungi, can increase plant growth through uptake of essential nutrients. This is the first study examining whether species-specific associations with mycorrhizal fungi alter plant tolerance to herbivory. We grew Plantago lanceolata plants with three species of mycorrhizal fungi previously shown to have differential impacts on plant growth and subjected them to herbivory by the specialist lepidopteran herbivore, Junonia coenia. Association with mycorrhizal fungus Glomus white provided the greatest growth benefit but did not alter plant response to herbivory. Alternatively, association with Archaeospora trappei provided less growth promotion but did lead to tolerance to herbivory in the form of an increased growth rate. Finally, an association with the fungus Scutellospora calospora led to neither plant growth promotion nor tolerance to herbivory. In fact, an association with S. calospora appeared to reduce plant tolerance to herbivory. An association with all three species of mycorrhizae resulted in a pattern of growth similar to that of plants grown only with Glomus white, suggesting that growth promotion by multiple mycorrhizal species is driven by the inclusion of a "super fungus," in this case, Glomus white. This work illustrates that plant response to herbivory depends upon the mycorrhizal fungal mutualist with which a plant is associated.

Three-way interactions among mutualistic mycorrhizal fungi, plants, and plant enemies: hypotheses and synthesis.

A number of studies have shown that an association with mycorrhizal fungi can alter the outcome of interactions between plants and their enemies. While the directions of these effects vary, their strength suggests the need for greater attention to multispecies interactions among plant enemies, plants, and mycorrhizal fungi. We recognize that mycorrhizal fungi could effect plant enemies by improving plant nutrition, modifying plant tolerance, or modifying plant defenses. In addition, mycorrhizal fungi could directly interfere with pathogen infection, herbivory, or parasitism by occupying root space. We formalize these alternative outcomes of multispecies interactions and explore the long-term dynamics of the plant-enemy interactions based on these different scenarios using a general model of interactions between plants and plant enemies. We then review the literature in terms of the assumptions of the alternative mechanisms and the predictions of these models. Through this effort, we identify new directions in the study of tritrophic interactions between enemies, plants, and soil mutualists.