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.

Variable influence of photosynthetic thermal acclimation on future carbon uptake in Australian wooded ecosystems under climate change.

Climate change will impact gross primary productivity (GPP), net primary productivity (NPP), and carbon storage in wooded ecosystems. The extent of change will be influenced by thermal acclimation of photosynthesis-the ability of plants to adjust net photosynthetic rates in response to growth temperatures-yet regional differences in acclimation effects among wooded ecosystems is currently unknown. We examined the effects of changing climate on 17 Australian wooded ecosystems with and without the effects of thermal acclimation of C3 photosynthesis. Ecosystems were drawn from five ecoregions (tropical savanna, tropical forest, Mediterranean woodlands, temperate woodlands, and temperate forests) that span Australia's climatic range. We used the CABLE-POP land surface model adapted with thermal acclimation functions and forced with HadGEM2-ES climate projections from RCP8.5. For each site and ecoregion we examined (a) effects of climate change on GPP, NPP, and live tree carbon storage; and (b) impacts of thermal acclimation of photosynthesis on simulated changes. Between the end of the historical (1976-2005) and projected (2070-2099) periods simulated annual carbon uptake increased in the majority of ecosystems by 26.1%-63.3% for GPP and 15%-61.5% for NPP. Thermal acclimation of photosynthesis further increased GPP and NPP in tropical savannas by 27.2% and 22.4% and by 11% and 10.1% in tropical forests with positive effects concentrated in the wet season (tropical savannas) and the warmer months (tropical forests). We predicted minimal effects of thermal acclimation of photosynthesis on GPP, NPP, and carbon storage in Mediterranean woodlands, temperate woodlands, and temperate forests. Overall, positive effects were strongly enhanced by increasing CO2 concentrations under RCP8.5. We conclude that the direct effects of climate change will enhance carbon uptake and storage in Australian wooded ecosystems (likely due to CO2 enrichment) and that benefits of thermal acclimation of photosynthesis will be restricted to tropical ecoregions.

Higher global gross primary productivity under future climate with more advanced representations of photosynthesis.

Gross primary productivity (GPP) is the key determinant of land carbon uptake, but its representation in terrestrial biosphere models (TBMs) does not reflect our latest physiological understanding. We implemented three empirically well supported but often omitted mechanisms into the TBM CABLE-POP: photosynthetic temperature acclimation, explicit mesophyll conductance, and photosynthetic optimization through redistribution of leaf nitrogen. We used the RCP8.5 climate scenario to conduct factorial model simulations characterizing the individual and combined effects of the three mechanisms on projections of GPP. Simulated global GPP increased more strongly (up to 20% by 2070-2099) in more comprehensive representations of photosynthesis compared to the model lacking the three mechanisms. The experiments revealed non-additive interactions among the mechanisms as combined effects were stronger than the sum of the individual effects. The modeled responses are explained by changes in the photosynthetic sensitivity to temperature and CO2 caused by the added mechanisms. Our results suggest that current TBMs underestimate GPP responses to future CO2 and climate conditions.

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.

Bridge to the future: Important lessons from 20 years of ecosystem observations made by the OzFlux network.

In 2020, the Australian and New Zealand flux research and monitoring network, OzFlux, celebrated its 20th anniversary by reflecting on the lessons learned through two decades of ecosystem studies on global change biology. OzFlux is a network not only for ecosystem researchers, but also for those 'next users' of the knowledge, information and data that such networks provide. Here, we focus on eight lessons across topics of climate change and variability, disturbance and resilience, drought and heat stress and synergies with remote sensing and modelling. In distilling the key lessons learned, we also identify where further research is needed to fill knowledge gaps and improve the utility and relevance of the outputs from OzFlux. Extreme climate variability across Australia and New Zealand (droughts and flooding rains) provides a natural laboratory for a global understanding of ecosystems in this time of accelerating climate change. As evidence of worsening global fire risk emerges, the natural ability of these ecosystems to recover from disturbances, such as fire and cyclones, provides lessons on adaptation and resilience to disturbance. Drought and heatwaves are common occurrences across large parts of the region and can tip an ecosystem's carbon budget from a net CO2 sink to a net CO2 source. Despite such responses to stress, ecosystems at OzFlux sites show their resilience to climate variability by rapidly pivoting back to a strong carbon sink upon the return of favourable conditions. Located in under-represented areas, OzFlux data have the potential for reducing uncertainties in global remote sensing products, and these data provide several opportunities to develop new theories and improve our ecosystem models. The accumulated impacts of these lessons over the last 20 years highlights the value of long-term flux observations for natural and managed systems. A future vision for OzFlux includes ongoing and newly developed synergies with ecophysiologists, ecologists, geologists, remote sensors and modellers.

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.

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.

Thermal optima of gross primary productivity are closely aligned with mean air temperatures across Australian wooded ecosystems.

Gross primary productivity (GPP) of wooded ecosystems (forests and savannas) is central to the global carbon cycle, comprising 67%-75% of total global terrestrial GPP. Climate change may alter this flux by increasing the frequency of temperatures beyond the thermal optimum of GPP (Topt ). We examined the relationship between GPP and air temperature (Ta) in 17 wooded ecosystems dominated by a single plant functional type (broadleaf evergreen trees) occurring over a broad climatic gradient encompassing five ecoregions across Australia ranging from tropical in the north to Mediterranean and temperate in the south. We applied a novel boundary-line analysis to eddy covariance flux observations to (a) derive ecosystem GPP-Ta relationships and Topt (including seasonal analyses for five tropical savannas); (b) quantitatively and qualitatively assess GPP-Ta relationships within and among ecoregions; (c) examine the relationship between Topt and mean daytime air temperature (MDTa) across all ecosystems; and (d) examine how down-welling short-wave radiation (Fsd) and vapour pressure deficit (VPD) influence the GPP-Ta relationship. GPP-Ta relationships were convex parabolas with narrow curves in tropical forests, tropical savannas (wet season), and temperate forests, and wider curves in temperate woodlands, Mediterranean woodlands, and tropical savannas (dry season). Ecosystem Topt ranged from 15℃ (temperate forest) to 32℃ (tropical savanna-wet and dry seasons). The shape of GPP-Ta curves was largely determined by daytime Ta range, MDTa, and maximum GPP with the upslope influenced by Fsd and the downslope influenced by VPD. Across all ecosystems, there was a strong positive linear relationship between Topt and MDTa (Adjusted R2 : 0.81; Slope: 1.08) with Topt exceeding MDTa by >1℃ at all but two sites. We conclude that ecosystem GPP has adjusted to local MDTa within Australian broadleaf evergreen forests and that GPP is buffered against small Ta increases in the majority of these ecosystems.

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.

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.

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.

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.

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.

Root symbionts: Powerful drivers of plant above- and belowground indirect defenses.

Soil microbial mutualists of plants, including mycorrhizal fungi, non-mycorrhizal fungi and plant growth promoting rhizobacteria, have been typically characterized for increasing nutrient acquisition and plant growth. More recently, soil microbes have also been shown to increase direct plant defense against above- and belowground herbivores. Plants, however, do not only rely on direct defenses when attacked, but they can also recruit pest antagonists such as predators and parasitoids, both above and belowground, mainly via the release of volatile organic compounds (i.e., indirect defenses). In this review, we illustrate the main features and effects of soil microbial mutualists of plants on plant indirect defenses and discuss possible applications within the framework of sustainable crop protection against root- and shoot-feeding arthropod pests. We indicate the main knowledge gaps and the future challenges to be addressed in the study and application of these multifaceted interactions.

Research priorities for harnessing plant microbiomes in sustainable agriculture.

Feeding a growing world population amidst climate change requires optimizing the reliability, resource use, and environmental impacts of food production. One way to assist in achieving these goals is to integrate beneficial plant microbiomes-i.e., those enhancing plant growth, nutrient use efficiency, abiotic stress tolerance, and disease resistance-into agricultural production. This integration will require a large-scale effort among academic researchers, industry researchers, and farmers to understand and manage plant-microbiome interactions in the context of modern agricultural systems. Here, we identify priorities for research in this area: (1) develop model host-microbiome systems for crop plants and non-crop plants with associated microbial culture collections and reference genomes, (2) define core microbiomes and metagenomes in these model systems, (3) elucidate the rules of synthetic, functionally programmable microbiome assembly, (4) determine functional mechanisms of plant-microbiome interactions, and (5) characterize and refine plant genotype-by-environment-by-microbiome-by-management interactions. Meeting these goals should accelerate our ability to design and implement effective agricultural microbiome manipulations and management strategies, which, in turn, will pay dividends for both the consumers and producers of the world food supply.

Potato aphid Macrosiphum euphorbiae performance is determined by aphid genotype and not mycorrhizal fungi or water availability.

Intra- and interspecific variation in plant and insect traits can alter the strength and direction of insect-plant interactions, with outcomes modified by soil biotic and abiotic conditions. We used the potato aphid (Macrosiphum euphorbiae Thomas) feeding on cultivated Solanum tuberosum and wild Solanum berthaulti to study the impact of water availability and plant mutualistic arbuscular mycorrhizal (AM) fungi on aphid performance and susceptibility to a parasitoid wasp (Aphidius ervi Haliday). Plants were grown under glass with live or sterile AM fungal spores and supplied with sufficient or reduced water supply. Plants were infested with 1 of 3 genotypes of M. euphorbiae or maintained as aphid-free controls; aphid abundance was scored after 1 week, after which aphid susceptibility to A. ervi was assayed ex planta. Solanum tuberosum accumulated c. 20% more dry mass than S. berthaultii, and root mass of S. berthaultii was smallest under reduced water supply in the presence of AM fungi. Aphid abundance was lowest on S. berthaultii and highest for genotype "2" aphids; genotype "1" aphid density was particularly reduced on S. berthaultii. Aphid genotype "1" exhibited low susceptibility to parasitism and was attacked less frequently than the other two more susceptible aphid genotypes. Neither AM fungi nor water availability affected insect performance. Our study suggests a fitness trade-off in M. euphorbiae between parasitism resistance and aphid performance on poor quality Solanum hosts that warrants further exploration, and indicates the importance of accounting for genotype identity in determining the outcome of multitrophic interactions.

Does the Slow-Growth, High-Mortality Hypothesis Apply Below Ground?

Belowground tri-trophic study systems present a challenging environment in which to study plant-herbivore-natural enemy interactions. For this reason, belowground examples are rarely available for testing general ecological theories. To redress this imbalance, we present, for the first time, data on a belowground tri-trophic system to test the slow growth, high mortality hypothesis. We investigated whether the differing performance of entomopathogenic nematodes (EPNs) in controlling the common pest black vine weevil Otiorhynchus sulcatus could be linked to differently resistant cultivars of the red raspberry Rubus idaeus. The O. sulcatus larvae recovered from R. idaeus plants showed significantly slower growth and higher mortality on the Glen Rosa cultivar, relative to the more commercially favored Glen Ample cultivar creating a convenient system for testing this hypothesis. Heterorhabditis megidis was found to be less effective at controlling O. sulcatus than Steinernema kraussei, but conformed to the hypothesis. However, S. kraussei maintained high levels of O. sulcatus mortality regardless of how larval growth was influenced by R. idaeus cultivar. We link this to direct effects that S. kraussei had on reducing O. sulcatus larval mass, indicating potential sub-lethal effects of S. kraussei, which the slow-growth, high-mortality hypothesis does not account for. Possible origins of these sub-lethal effects of EPN infection and how they may impact on a hypothesis designed and tested with aboveground predator and parasitoid systems are discussed.