Exploring the roles of microbes in facilitating plant adaptation to climate change

Petras D., Phelan V.V., Acharya D., Allen A.E., Aron A.T., Bandeira N., Bowen B.P., Belle-Oudry D., Boecker S., Cummings D.A., Deutsch J.M., Fahy E., Garg N., Gregor R., Handelsman J., et. al.

Jones C.Y., Engelhardt I., Patko D., Dupuy L., Holden N., Willats W.G.

Rhizospheres are microecological zones at the interface of roots and soils. Interactions between bacteria and roots are critical for maintaining plant and soil health but are difficult to study because of constraints inherent in working with underground systems. We have developed an in-situ rhizosphere imaging system based on transparent soils and molecular probes that can be imaged using confocal microscopy. We observed spatial patterning of polysaccharides along roots and on cells deposited into the rhizosphere and also co-localised fluorescently tagged soil bacteria. These studies provide insight into the complex glycan landscape of rhizospheres and suggest a means by which root / rhizobacteria interactions can be non-disruptively studied.

Hou S., Wolinska K.W., Hacquard S.

Reminiscent to the microbiota-gut-brain axis described in animals, recent advances indicate that plants can take advantage of belowground microbial commensals to orchestrate aboveground stress responses. Integration of plant responses to microbial cues belowground and environmental cues aboveground emerges as a mechanism that promotes stress tolerance in plants. Using recent examples obtained from reductionist and community-level approaches, we discuss the extent to which perception of aboveground biotic and abiotic stresses can cascade along the shoot–root axis to sculpt root microbiota assembly and modulate the growth of root commensals that bolster aboveground stress tolerance. We propose that host modulation of microbiota-root-shoot circuits contributes to phenotypic plasticity and decision-making in plants, thereby promoting adaptation to rapidly changing environmental conditions.

Santos-Medellín C., Liechty Z., Edwards J., Nguyen B., Huang B., Weimer B.C., Sundaresan V.

Microbial symbioses can mitigate drought stress in crops but harnessing these beneficial interactions will require an in-depth understanding of root microbiome responses to drought cycles. Here, by detailed temporal characterization of root-associated microbiomes of rice plants during drought stress and recovery, we find that endosphere communities remained compositionally altered after rewatering, with prolonged droughts leading to decreased resilience. Several endospheric Actinobacteria were significantly enriched during drought and for weeks after rewatering. Notably, the most abundant endosphere taxon during this period was a Streptomyces, and a corresponding isolate promoted root growth. Additionally, drought stress disrupted the temporal dynamics of late-colonizing microorganisms, permanently altering the normal successional trends of root microbiota. These findings reveal that severe drought results in enduring impacts on rice root microbiomes, including enrichment of taxonomic groups that could shape the recovery response of the host, and have implications relevant to drought protection strategies using root microbiota. Microbial symbioses can help plants mitigate environmental stresses and plant microbiome compositions are influenced, for example, by drought stress. The investigated temporal shifts of the rice root microbiome under various durations of drought show the progression of microbiome composition in response to stress and a long-lasting effect of severe conditions.

Song Y., Haney C.H.

Plants restructure their microbiomes as a ‘cry for help’ against biotic and abiotic stress. A recent study shows that prolonged drought stress causes a permanent shift in the rhizosphere microbiome, and provides clues to which drought-induced microbiome changes might sustain plant health.

Tracanna V., Ossowicki A., Petrus M.L., Overduin S., Terlouw B.R., Lund G., Robinson S.L., Warris S., Schijlen E.G., van Wezel G.P., Raaijmakers J.M., Garbeva P., Medema M.H.

Soil-borne plant-pathogenic fungi continue to be a major threat to agriculture and horticulture. The genus Fusarium in particular is one of the most devastating groups of soilborne fungal pathogens for a wide range of crops.

Singer E., Vogel J.P., Northen T., Mungall C.J., Juenger T.E.

In recent years, the root microbiome (i.e., microorganisms growing inside, on, or in close proximity to plant roots) has been shown to play an important role in plant health and productivity. Despite its importance, the root microbiome is challenging to study because of its complexity, heterogeneity, and subterranean location. Fortunately, root microbiome research has seen a tremendous influx of novel technologies (e.g., imaging tools, robotics, and molecular analyses), experimental platforms (e.g., micro- and mesocosms), and data integration, modeling, and prediction tools in the past decade that have greatly increased our ability to dissect the complex network of interactions between above- and belowground environmental parameters, plants, bacteria, and fungi that dictate soil and broader ecosystem health. Herein, we discuss methods that are currently used in root microbiome research and that can be expanded to phytobiome research in general ranging from laboratory studies to mesocosm-scale studies and, finally, to field studies; evaluate their relevance to ecosystem studies; and discuss future root microbiome research directions.

Zhou L., Song C., Li Z., Kuipers O.P.

Tomato plant growth is frequently hampered by a high susceptibility to pests and diseases. Traditional chemical control causes a serious impact on both the environment and human health. Therefore, seeking environment-friendly and cost-effective green methods in agricultural production becomes crucial nowadays. Plant Growth Promoting Rhizobacteria (PGPR) can promote plant growth through biological activity. Their use is considered to be a promising sustainable approach for crop growth. Moreover, a vast number of biosynthetic gene clusters (BGCs) for secondary metabolite production are being revealed in PGPR, which helps to find potential anti-microbial activities for tomato disease control. We isolated 181 Bacillus-like strains from healthy tomato, rhizosphere soil, and tomato tissues. In vitro antagonistic assays revealed that 34 Bacillus strains have antimicrobial activity against Erwinia carotovora, Pseudomonas syringae; Rhizoctonia solani; Botrytis cinerea; Verticillium dahliae and Phytophthora infestans. The genomes of 10 Bacillus and Paenibacillus strains with good antagonistic activity were sequenced. Via genome mining approaches, we identified 120 BGCs encoding NRPs, PKs-NRPs, PKs, terpenes and bacteriocins, including known compounds such as fengycin, surfactin, bacillibactin, subtilin, etc. In addition, several novel BGCs were identified. We discovered that the NRPs and PKs-NRPs BGCs in Bacillus species are encoding highly conserved known compounds as well as various novel variants. This study highlights the great number of varieties of BGCs in Bacillus strains. These findings pave the road for future usage of Bacillus strains as biocontrol agents for tomato disease control and are a resource arsenal for novel antimicrobial discovery.

Rudgers J.A., Afkhami M.E., Bell-Dereske L., Chung Y.A., Crawford K.M., Kivlin S.N., Mann M.A., Nuñez M.A.

Interactions between plants and microbes have important influences on evolutionary processes, population dynamics, community structure, and ecosystem function. We review the literature to document how climate change may disrupt these ecological interactions and develop a conceptual framework to integrate the pathways of plant-microbe responses to climate over different scales in space and time. We then create a blueprint to aid generalization that categorizes climate effects into changes in the context dependency of plant-microbe pairs, temporal mismatches and altered feedbacks over time, or spatial mismatches that accompany species range shifts. We pair a new graphical model of how plant-microbe interactions influence resistance to climate change with a statistical approach to predictthe consequences of increasing variability in climate. Finally, we suggest pathways through which plant-microbe interactions can affect resilience during recovery from climate disruption. Throughout, we take a forward-looking perspective, highlighting knowledge gaps and directions for future research.

Chen I.A., Chu K., Palaniappan K., Ratner A., Huang J., Huntemann M., Hajek P., Ritter S., Varghese N., Seshadri R., Roux S., Woyke T., Eloe-Fadrosh E.A., Ivanova N.N., Kyrpides N.

Abstract The Integrated Microbial Genomes & Microbiomes system (IMG/M: https://img.jgi.doe.gov/m/) contains annotated isolate genome and metagenome datasets sequenced at the DOE’s Joint Genome Institute (JGI), submitted by external users, or imported from public sources such as NCBI. IMG v 6.0 includes advanced search functions and a new tool for statistical analysis of mixed sets of genomes and metagenome bins. The new IMG web user interface also has a new Help page with additional documentation and webinar tutorials to help users better understand how to use various IMG functions and tools for their research. New datasets have been processed with the prokaryotic annotation pipeline v.5, which includes extended protein family assignments.

Wanke A., Malisic M., Wawra S., Zuccaro A.

Abstract To defend against microbial invaders but also to establish symbiotic programs, plants need to detect the presence of microbes through the perception of molecular signatures characteristic of a whole class of microbes. Among these molecular signatures, extracellular glycans represent a structurally complex and diverse group of biomolecules that has a pivotal role in the molecular dialog between plants and microbes. Secreted glycans and glycoconjugates such as symbiotic lipochitooligosaccharides or immunosuppressive cyclic β-glucans act as microbial messengers that prepare the ground for host colonization. On the other hand, microbial cell surface glycans are important indicators of microbial presence. They are conserved structures normally exposed and thus accessible for plant hydrolytic enzymes and cell surface receptor proteins. While the immunogenic potential of bacterial cell surface glycoconjugates such as lipopolysaccharides and peptidoglycan has been intensively studied in the past years, perception of cell surface glycans from filamentous microbes such as fungi or oomycetes is still largely unexplored. To date, only few studies have focused on the role of fungal-derived cell surface glycans other than chitin, highlighting a knowledge gap that needs to be addressed. The objective of this review is to give an overview on the biological functions and perception of microbial extracellular glycans, primarily focusing on their recognition and their contribution to plant–microbe interactions.

Berlanga‐Clavero M.V., Molina‐Santiago C., Vicente A., Romero D.

Plants and microbes have evolved sophisticated ways to communicate and coexist. The simplest interactions that occur in plant-associated habitats, i.e., those involved in disease detection, depend on the production of microbial pathogenic and virulence factors and the host's evolved immunological response. In contrast, microbes can also be beneficial for their host plants in a number of ways, including fighting pathogens and promoting plant growth. In order to clarify the mechanisms directly involved in these various plant-microbe interactions, we must still deepen our understanding of how these interkingdom communication systems, which are constantly modulated by resident microbial activity, are established and, most importantly, how their effects can span physically separated plant compartments. Efforts in this direction have revealed a complex and interconnected network of molecules and associated metabolic pathways that modulate plant-microbe and microbe-microbe communication pathways to regulate diverse ecological responses. Once sufficiently understood, these pathways will be biotechnologically exploitable, for example, in the use of beneficial microbes in sustainable agriculture. The aim of this review is to present the latest findings on the dazzlingly diverse arsenal of molecules that efficiently mediate specific microbe-microbe and microbe-plant communication pathways during plant development and on different plant organs.

Trivedi P., Leach J.E., Tringe S.G., Sa T., Singh B.K.

Healthy plants host diverse but taxonomically structured communities of microorganisms, the plant microbiota, that colonize every accessible plant tissue. Plant-associated microbiomes confer fitness advantages to the plant host, including growth promotion, nutrient uptake, stress tolerance and resistance to pathogens. In this Review, we explore how plant microbiome research has unravelled the complex network of genetic, biochemical, physical and metabolic interactions among the plant, the associated microbial communities and the environment. We also discuss how those interactions shape the assembly of plant-associated microbiomes and modulate their beneficial traits, such as nutrient acquisition and plant health, in addition to highlighting knowledge gaps and future directions. In this Review, Trivedi and colleagues explore the interactions between plants, their associated microbial communities and the environment, and also discuss how those interactions shape the assembly of plant-associated microbiomes and modulate their beneficial traits.

Leopold D.R., Busby P.E.

The composition of host-associated microbiomes can have important consequences for host health and fitness [1-3]. Yet we still lack understanding of many fundamental processes that determine microbiome composition [4, 5]. There is mounting evidence that historical contingency during microbiome assembly may overshadow more deterministic processes, such as the selective filters imposed by host traits [6-8]. More specifically, species arrival order has been frequently shown to affect microbiome composition [9-12], a phenomenon known as priority effects [13-15]. However, it is less clear whether priority effects during microbiome assembly are consequential for the host [16] or whether intraspecific variation in host traits can alter the trajectory of microbiome assembly under priority effects. In a greenhouse inoculation experiment using the black cottonwood (Populus trichocarpa) foliar microbiome, we manipulated host genotype and the colonization order of common foliar fungi. We quantified microbiome assembly outcomes using fungal marker gene sequencing and measured susceptibility of the colonized host to a leaf rust pathogen, Melampsora × columbiana. We found that the effect of species arrival order on microbiome composition, and subsequent disease susceptibility, depended on the host genotype. Additionally, we found that microbiome assembly history can affect host disease susceptibility independent of microbiome composition at the time of pathogen exposure, suggesting that the interactive effects of species arrival order and host genotype can decouple community composition and function. Overall, these results highlight the importance of a key process underlying stochasticity in microbiome assembly while also revealing which hosts are most likely to experience these effects.

de Vries F.T., Griffiths R.I., Knight C.G., Nicolitch O., Williams A.

Root-associated microbes can improve plant growth, and they offer the potential to increase crop resilience to future drought. Although our understanding of the complex feedbacks between plant and microbial responses to drought is advancing, most of our knowledge comes from non-crop plants in controlled experiments. We propose that future research efforts should attempt to quantify relationships between plant and microbial traits, explicitly focus on food crops, and include longer-term experiments under field conditions. Overall, we highlight the need for improved mechanistic understanding of the complex feedbacks between plants and microbes during, and particularly after, drought. This requires integrating ecology with plant, microbiome, and molecular approaches and is central to making crop production more resilient to our future climate.

Abdallah N.A., Hamwieh A., Radwan K., Fouad N., Baum M.

Wall C.B., Kajihara K., Rodriguez F.E., Vilonen L., Yogi D., Swift S.O., Hynson N.A.

AbstractPremiseThe ability of plants to adapt or acclimate to climate change is inherently linked to their interactions with symbiotic microbes, notably fungi. However, it is unclear whether fungal symbionts from different climates have different impacts on the outcome of plant–fungal interactions, especially under environmental stress.MethodsWe tested three provenances of fungal inoculum (originating from dry, moderate or wet environments) with one host plant genotype exposed to three soil moisture regimes (low, moderate and high). Inoculated and uninoculated plants were grown in controlled conditions for 151 days, then shoot and root biomass were weighed and fungal diversity and community composition determined via amplicon sequencing.ResultsThe source of inoculum and water regime elicited significant changes in plant resource allocation to shoots versus roots, but only specific inocula affected total plant biomass. Shoot biomass increased in the high water treatment but was negatively impacted by all inoculum treatments relative to the controls. The opposite was true for roots, where the low water treatment led to greater proportional root biomass, and plants inoculated with wet site fungi allocated significantly more resources to root growth than dry‐ or moderate‐site inoculated plants and the controls. Fungal communities of shoots and roots partitioned by inoculum source, water treatment, and the interaction of the two.ConclusionsThe provenance of fungi can significantly affect total plant biomass and resource allocation above‐ and belowground, with fungi derived from more extreme environments eliciting the strongest plant responses.

Tan W., Nian H., Tran L.P., Jin J., Lian T.

Abstract The crucial role of rhizosphere microbes in plant growth and their resilience to environmental stresses underscores the intricate communication between microbes and plants. Plants are equipped with a diverse set of signaling molecules that facilitate communication across different biological kingdoms, although our comprehension of these mechanisms is still evolving. Small peptides produced by plants (SPPs) and microbes (SPMs) play a pivotal role in intracellular signaling and are essential in orchestrating various plant development stages. In this review, we posit that SPPs and SPMs serve as crucial signaling agents for the bidirectional cross-kingdom communication between plants and rhizosphere microbes. We explore several potential mechanistic pathways through which this communication occurs. Additionally, we propose that leveraging small peptides, inspired by plant–rhizosphere microbe interactions, represents an innovative approach in the field of holobiont engineering.

Guo Y., Zeng Z., Wang J., Zou J., Shi Z., Chen S.

Abstract Soil, as the largest terrestrial carbon pool, has garnered significant attention concerning its response to global warming. However, accurately estimating the stocks and dynamics of soil organic carbon (SOC) remains challenging due to the complex and unclear influence mechanisms associated with biogeochemical processes in above- and belowground ecosystems, as well as technical limitations. Therefore, it is imperative to facilitate the integration of models and knowledge and promote dialogue between empiricists and modelers. This review provides a concise SOC turnover framework to understand the impact of climate change on SOC dynamics. It covers various factors such as warming, precipitation changes, elevated carbon dioxide, and nitrogen deposition. The review presents impact mechanisms from the perspective of organismal traits (plants, fauna, and microbes), their interactions, and abiotic regulation. Although valuable insights have been gained regarding SOC inputs, decomposition, and stabilization under climate change, there are still knowledge gaps that need to be addressed. In the future, it is essential to conduct systematic and refined research in this field. This includes standardizing the organismal traits most relevant to SOC, studying the standardization of SOC fractions and their resistance to decomposition, and focusing on the interactions and biochemical pathways of biological communities. Through further investigation of biotic and abiotic interactions, a clearer understanding can be attained regarding the physical protection, chemical stability, and biological driving mechanisms of SOC under climate change. This can be achieved by integrating multidisciplinary knowledge, utilizing novel technologies and methodologies, increasing in-situ experiments, and conducting long-term monitoring across multi-scales. By integrating reliable data and elucidating clear mechanisms, the accuracy of models can be enhanced, providing a scientific foundation for mitigating climate change.

Yang F., He J., Nan Z.

Phyllosphere fungi form close ecological ties with their hosts and participate in multiple ecosystem processes. This research investigated simulated climate change effects of warming and precipitation manipulationon the Aster tataricus fungal community in a Qinghai-Tibetan Plateau alpine meadow. Increased precipitation increased the fungal community diversity and richness indices, but warming had the opposite effect. Warming and precipitation adjustment in combination reduced the fungal community diversity. FUNGuild functional analysis of differences in the leaf fungal community in our study, and linked statistical analysis, determined that increasing precipitation significantly reduced relative abundance of pathogenic fungi and incidence of plant diseases, while warming and decreased precipitation did the opposite. Differences in the leaf fungal community in our study under warming and decreased precipitation would be predicted to increase incidence of plant diseases. These climate change simulations improve awareness of future plant disease risks in natural plant communities and provide opportunities to develop responses.

Kumar R., Kumar A., Dhaka R.K., Chahar M., Malyan S.K., Singh A.P., Rana A.

Climate change is one of the challenges of the twenty-first century towards sustainability, environment, energy supply, and health. The greenhouse gas (GHG) emission alters the climate of biosphere leading to change in frequency and pattern of natural phenomena like precipitation (snowfall and rain), cyclones, and storms. The climate change imposes stresses like salinity, drought, and rise in temperature that negatively impact the growth of plants, microorganisms, and animals. Climate change can potentially hamper the world food security goals via affecting the growth and development of plants resulting in yield loss. Further, the climate change impacts microbial diversity including rhizomicrobiome, which has an important role to maintain ecosystem under different environmental thresholds. Microorganisms can produce and sequester greenhouse gases (GHGs) during their metabolic activities. The microorganisms such as methanotrophs, archaebacteria, halophytes, and plant growth-promoting rhizobacteria (PGPRs) have been applied to develop plant tolerance under different abiotic and biotic stresses via various mechanisms such as ACC deaminase production, solubilization of nutrients (potassium, phosphorous, iron), nitrogen fixation, and production of siderophores, phytohormone, osmolytes, antioxidants, and exopolysaccharides. These beneficial microorganisms can be used as a tool for sustainable agriculture to cultivate crops under adverse climatic conditions.

Marčiulynienė D., Marčiulynas A., Mischerikova V., Lynikienė J., Gedminas A., Franic I., Menkis A.

The plant- and soil-associated microbial communities are critical to plant health and their resilience to stressors, such as drought, pathogens, and pest outbreaks. A better understanding of the structure of microbial communities and how they are affected by different environmental factors is needed to predict and manage ecosystem responses to climate change. In this study, we carried out a country-wide analysis of fungal communities associated with Pinus sylvestris growing under different environmental conditions. Needle, shoot, root, mineral, and organic soil samples were collected at 30 sites. By interconnecting the high-throughput sequencing data, environmental variables, and soil chemical properties, we were able to identify key factors that drive the diversity and composition of fungal communities associated with P. sylvestris. The fungal species richness and community composition were also found to be highly dependent on the site and the substrate they colonize. The results demonstrated that different functional tissues and the rhizosphere soil of P. sylvestris are associated with diverse fungal communities, which are driven by a combination of climatic (temperature and precipitation) and edaphic factors (soil pH), and stand characteristics.

Gutierrez M.M., Cameron-Harp M.V., Chakraborty P.P., Stallbaumer-Cyr E.M., Morrow J.A., Hansen R.R., Derby M.M.

Semi-arid regions faced with increasingly scarce freshwater resources must manage competing demands in the food-energy-water nexus. A possible solution modifies soil hydrologic properties using biosurfactants to reduce evaporation and improve water retention. In this study, two different soil textures representative of agricultural soils in Kansas were treated with a direct application of the biosurfactant, Surfactin, and an indirect application via inoculation of Bacillus subtilis. Evaporation rates of the wetted soils were measured when exposed to artificial sunlight (1000 W/m2) and compared to non-treated control soils. Experimental results indicate that both treatments alter soil moisture dynamics by increasing evaporation rates by when soil moisture is plentiful (i.e., constant rate period) and decreasing evaporation rates by when moisture is scarce (i.e., slower rate period). Furthermore, both treatments significantly reduced the soil moisture content at which the soil transitioned from constant rate to slower rate evaporation. Out of the two treatments, inoculation with B. subtilis generally produced greater changes in evaporation dynamics; for example, the treatment with B. subtilis in sandy loam soils increased constant rate periods of evaporation by 43% and decreased slower rate evaporation by 49%. In comparing the two soil textures, the sandy loam soil exhibited a larger treatment effect than the loam soil. To evaluate the potential significance of the treatment effects, a System Dynamics Model operationalized the evaporation rate results and simulated soil moisture dynamics under typical daily precipitation conditions. The results from this model indicate both treatment methods significantly altered soil moisture dynamics in the sandy loam soils and increased the probability of the soil exhibiting constant rate evaporation relative to the control soils. Overall, these findings suggest that the decrease in soil moisture threshold observed in the experimental setting could increase soil moisture availability by prolonging the constant rate stage of evaporation. As inoculation with B. subtilis in the sandy loam soil had the most pronounced effects in both the experimental and simulated contexts, future work should focus on testing this treatment in field trials with similar soil textures.

He D., Singh S.K., Peng L., Kaushal R., Vílchez J.I., Shao C., Wu X., Zheng S., Morcillo R.J., Paré P.W., Zhang H.

Flavonoids are stress-inducible metabolites important for plant-microbe interactions. In contrast to their well-known function in initiating rhizobia nodulation in legumes, little is known about whether and how flavonoids may contribute to plant stress resistance through affecting non-nodulating bacteria. Here we show that flavonoids broadly contribute to the diversity of the Arabidopsis root microbiome and preferentially attract Aeromonadaceae, which included a cultivable Aeromonas sp. H1 that displayed flavonoid-induced chemotaxis with transcriptional enhancement of flagellum biogenesis and suppression of fumarate reduction for smooth swims. Strain H1 showed multiple plant-beneficial traits and enhanced plant dehydration resistance, which required flavonoids but not through a sudden “cry-for-help” upon stress. Strain H1 boosted dehydration-induced H2O2 accumulation in guard cells and stomatal closure, concomitant with synergistic induction of jasmonic acid-related regulators of plant dehydration resistance. These findings revealed a key role of flavonoids, and the underlying mechanism, in mediating plant-microbiome interactions including the bacteria-enhanced plant dehydration resistance.

Kutos S., Barnes E.M., Bhutada A., Lewis J.D.

Abstract Soil fungi are vital to forest ecosystem function, in part through their role mediating tree responses to environmental factors, as well as directly through effects on resource cycling. While the distribution of soil fungi can vary with abiotic factors, plant species identity is also known to affect community composition. However, the particular influence that a plant will have on its soil microbiota remains difficult to predict. Here, we paired amplicon sequencing and enzymatic assays to assess soil fungal composition and function under three tree species, Quercus rubra, Betula nigra, and Acer rubrum, planted individually and in all combinations in a greenhouse. We observed that fungal communities differed between each of the individual planted trees, suggesting at least some fungal taxa may associate preferentially with these tree species. Additionally, fungal community composition under mixed-tree plantings broadly differed from the individual planted trees, suggesting mixing of these distinct soil fungal communities. The data also suggest that there were larger enzymatic activities in the individual plantings as compared to all mixed-tree plantings which may be due to variations in fungal community composition. This study provides further evidence of the importance of tree identity on soil microbiota and functional changes to forest soils.