School of BioSciences - Research Publications

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    Plant Growth Promotion and Heat Stress Amelioration in Arabidopsis Inoculated with Paraburkholderia phytofirmans PsJN Rhizobacteria Quantified with the GrowScreen-Agar II Phenotyping Platform
    Macabuhay, A ; Arsova, B ; Watt, M ; Nagel, KA ; Lenz, H ; Putz, A ; Adels, S ; Mueller-Linow, M ; Kelm, J ; Johnson, AAT ; Walker, R ; Schaaf, G ; Roessner, U (MDPI, 2022-11)
    High temperatures inhibit plant growth. A proposed strategy for improving plant productivity under elevated temperatures is the use of plant growth-promoting rhizobacteria (PGPR). While the effects of PGPR on plant shoots have been extensively explored, roots-particularly their spatial and temporal dynamics-have been hard to study, due to their below-ground nature. Here, we characterized the time- and tissue-specific morphological changes in bacterized plants using a novel non-invasive high-resolution plant phenotyping and imaging platform-GrowScreen-Agar II. The platform uses custom-made agar plates, which allow air exchange to occur with the agar medium and enable the shoot to grow outside the compartment. The platform provides light protection to the roots, the exposure of it to the shoots, and the non-invasive phenotyping of both organs. Arabidopsis thaliana, co-cultivated with Paraburkholderia phytofirmans PsJN at elevated and ambient temperatures, showed increased lengths, growth rates, and numbers of roots. However, the magnitude and direction of the growth promotion varied depending on root type, timing, and temperature. The root length and distribution per depth and according to time was also influenced by bacterization and the temperature. The shoot biomass increased at the later stages under ambient temperature in the bacterized plants. The study offers insights into the timing of the tissue-specific, PsJN-induced morphological changes and should facilitate future molecular and biochemical studies on plant-microbe-environment interactions.
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    Nutrient deficiency effects on root architecture and root-to-shoot ratio in arable crops.
    Lopez, G ; Ahmadi, SH ; Amelung, W ; Athmann, M ; Ewert, F ; Gaiser, T ; Gocke, MI ; Kautz, T ; Postma, J ; Rachmilevitch, S ; Schaaf, G ; Schnepf, A ; Stoschus, A ; Watt, M ; Yu, P ; Seidel, SJ (Frontiers Media SA, 2022)
    Plant root traits play a crucial role in resource acquisition and crop performance when soil nutrient availability is low. However, the respective trait responses are complex, particularly at the field scale, and poorly understood due to difficulties in root phenotyping monitoring, inaccurate sampling, and environmental conditions. Here, we conducted a systematic review and meta-analysis of 50 field studies to identify the effects of nitrogen (N), phosphorous (P), or potassium (K) deficiencies on the root systems of common crops. Root length and biomass were generally reduced, while root length per shoot biomass was enhanced under N and P deficiency. Root length decreased by 9% under N deficiency and by 14% under P deficiency, while root biomass was reduced by 7% in N-deficient and by 25% in P-deficient soils. Root length per shoot biomass increased by 33% in N deficient and 51% in P deficient soils. The root-to-shoot ratio was often enhanced (44%) under N-poor conditions, but no consistent response of the root-to-shoot ratio to P-deficiency was found. Only a few K-deficiency studies suited our approach and, in those cases, no differences in morphological traits were reported. We encountered the following drawbacks when performing this analysis: limited number of root traits investigated at field scale, differences in the timing and severity of nutrient deficiencies, missing data (e.g., soil nutrient status and time of stress), and the impact of other conditions in the field. Nevertheless, our analysis indicates that, in general, nutrient deficiencies increased the root-length-to-shoot-biomass ratios of crops, with impacts decreasing in the order deficient P > deficient N > deficient K. Our review resolved inconsistencies that were often found in the individual field experiments, and led to a better understanding of the physiological mechanisms underlying root plasticity in fields with low nutrient availability.
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    Root Growth and Architecture of Wheat and Brachypodium Vary in Response to Algal Fertilizer in Soil and Solution
    Mau, L ; Junker, S ; Bochmann, H ; Mihiret, YE ; Kelm, JM ; Schrey, SD ; Roessner, U ; Schaaf, G ; Watt, M ; Kant, J ; Arsova, B (MDPI, 2022-02)
    Alternative, recycled sources for mined phosphorus (P) fertilizers are needed to sustain future crop growth. Quantification of phenotypic adaptations and performance of plants with a recycled nutrient source is required to identify breeding targets and agronomy practices for new fertilization strategies. In this study, we tested the phenotypic responses of wheat (Triticum aestivum) and its genetic model, Brachypodium (Brachypodium distachyon), to dried algal biomass (with algae or high or low mineral P) under three growing conditions (fabricated ecosystems (EcoFABs), hydroponics, and sand). For both species, algal-grown plants had similar shoot biomass to mineral-grown plants, taking up more P than the low mineral P plants. Root phenotypes however were strongly influenced by nutrient form, especially in soilless conditions. Algae promoted the development of shorter and thicker roots, notably first and second order lateral roots. Root hairs were 21% shorter in Brachypodium, but 24% longer in wheat with algae compared to mineral high P. Our results are encouraging to new recycled fertilization strategies, showing algae is a nutrient source to wheat and Brachypodium. Variation in root phenotypes showed algal biomass is sensed by roots and is taken up at a higher amount per root length than mineral P. These phenotypes can be selected and further adapted in phenotype-based breeding for future renewal agriculture systems.
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    N-dependent dynamics of root growth and nitrate and ammonium uptake are altered by the bacterium Herbaspirillum seropedicae in the cereal model Brachypodium distachyon
    Kuang, W ; Sanow, S ; Kelm, JM ; Muller Linow, M ; Andeer, P ; Kohlheyer, D ; Northen, T ; Vogel, JP ; Watt, M ; Arsova, B ; Janni, M (OXFORD UNIV PRESS, 2022-09-03)
    Nitrogen (N) fixation in cereals by root-associated bacteria is a promising solution for reducing use of chemical N fertilizers in agriculture. However, plant and bacterial responses are unpredictable across environments. We hypothesized that cereal responses to N-fixing bacteria are dynamic, depending on N supply and time. To quantify the dynamics, a gnotobiotic, fabricated ecosystem (EcoFAB) was adapted to analyse N mass balance, to image shoot and root growth, and to measure gene expression of Brachypodium distachyon inoculated with the N-fixing bacterium Herbaspirillum seropedicae. Phenotyping throughput of EcoFAB-N was 25-30 plants h-1 with open software and imaging systems. Herbaspirillum seropedicae inoculation of B. distachyon shifted root and shoot growth, nitrate versus ammonium uptake, and gene expression with time; directions and magnitude depended on N availability. Primary roots were longer and root hairs shorter regardless of N, with stronger changes at low N. At higher N, H. seropedicae provided 11% of the total plant N that came from sources other than the seed or the nutrient solution. The time-resolved phenotypic and molecular data point to distinct modes of action: at 5 mM NH4NO3 the benefit appears through N fixation, while at 0.5 mM NH4NO3 the mechanism appears to be plant physiological, with H. seropedicae promoting uptake of N from the root medium.Future work could fine-tune plant and root-associated microorganisms to growth and nutrient dynamics.
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    Rhizosphere models: their concepts and application to plant-soil ecosystems
    Kuppe, CW ; Schnepf, A ; von Lieres, E ; Watt, M ; Postma, JA (SPRINGER, 2022-05)
    Abstract Background The rhizosphere is the influence-sphere of the root. It is a local ecosystem with complex functions that determine nutrient uptake, cycling of resources, and plant health. Mathematical models can quantitatively explain and help to understand rhizosphere complexity. To interpret model predictions and relevance of processes, we require understanding of the underlying concepts. Conceptualization of rhizosphere processes bridges mathematical modeling and experimental work and thus is key to understanding the rhizosphere. Scope We review concepts and assumptions foundational to the modeling of soil-plant-microorganism processes in the rhizosphere. Rhizosphere models are designed to simulate a plurality of components (solutes, substrates, and microorganisms). They specify components and interactions, drawing from the disciplines of soil science, botany, microbiology, and ecology. Solute transport models are applied to describe bioavailability in the rhizosphere. The root is typically a sink (e.g. nutrient uptake) or source (e.g. exudation) for one or more solutes. Microorganisms are usually described in time only, neglecting possible spatial movement. Interactions between components, e.g. chemical reactions and substrate-dependent bacterial growth rates, are usually described by coupling via reaction terms. Conclusions Rhizosphere models share concepts that we organized in a collective framework. This collective framework facilitates the development of new models. The interdisciplinary approach in which knowledge from soil ecology, botany, and soil physics are combined in rhizosphere models has proven fruitful for applications in plant and soil systems. We advocate multi-component-multi-interaction ecosystems around the root, with each component represented by an advection-diffusion-motility-reaction equation.
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    Modulators or facilitators? Roles of lipids in plant root-microbe interactions
    Macabuhay, A ; Arsova, B ; Walker, R ; Johnson, A ; Watt, M ; Roessner, U (CELL PRESS, 2022-02)
    Lipids have diverse functions in regulating the plasma membrane's cellular processes and signaling mediation. Plasma membrane lipids are also involved in the plant's complex interactions with the surrounding microorganisms, with which plants are in various forms of symbiosis. The roles of lipids influence the whole microbial colonization process, thus shaping the rhizomicrobiome. As chemical signals, lipids facilitate the stages of rhizospheric interactions - from plant root to microbe, microbe to microbe, and microbe to plant root - and modulate the plant's defense responses upon perception or contact with either beneficial or phytopathogenic microorganisms. Although studies have come a long way, further investigation is needed to discover more lipid species and elucidate novel lipid functions and profiles under various stages of plant root-microbe interactions.
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    A toolkit to rapidly modify root systems through single plant selection
    Rambla, C ; Van der Meer, S ; Voss-Fels, KP ; Makhoul, M ; Obermeier, C ; Rod, S ; Ober, ES ; Watt, M ; Alahmad, S ; Hickey, LT (BMC, 2022-01-10)
    BACKGROUND: The incorporation of root traits into elite germplasm is typically a slow process. Thus, innovative approaches are required to accelerate research and pre-breeding programs targeting root traits to improve yield stability in different environments and soil types. Marker-assisted selection (MAS) can help to speed up the process by selecting key genes or quantitative trait loci (QTL) associated with root traits. However, this approach is limited due to the complex genetic control of root traits and the limited number of well-characterised large effect QTL. Coupling MAS with phenotyping could increase the reliability of selection. Here we present a useful framework to rapidly modify root traits in elite germplasm. In this wheat exemplar, a single plant selection (SPS) approach combined three main elements: phenotypic selection (in this case for seminal root angle); MAS using KASP markers (targeting a root biomass QTL); and speed breeding to accelerate each cycle. RESULTS: To develop a SPS approach that integrates non-destructive screening for seminal root angle and root biomass, two initial experiments were conducted. Firstly, we demonstrated that transplanting wheat seedlings from clear pots (for seminal root angle assessment) into sand pots (for root biomass assessment) did not impact the ability to differentiate genotypes with high and low root biomass. Secondly, we demonstrated that visual scores for root biomass were correlated with root dry weight (r = 0.72), indicating that single plants could be evaluated for root biomass in a non-destructive manner. To highlight the potential of the approach, we applied SPS in a backcrossing program which integrated MAS and speed breeding for the purpose of rapidly modifying the root system of elite bread wheat line Borlaug100. Bi-directional selection for root angle in segregating generations successfully shifted the mean root angle by 30° in the subsequent generation (P ≤ 0.05). Within 18 months, BC2F4:F5 introgression lines were developed that displayed a full range of root configurations, while retaining similar above-ground traits to the recurrent parent. Notably, the seminal root angle displayed by introgression lines varied more than 30° compared to the recurrent parent, resulting in lines with both narrow and wide root angles, and high and low root biomass phenotypes. CONCLUSION: The SPS approach enables researchers and plant breeders to rapidly manipulate root traits of future crop varieties, which could help improve productivity in the face of increasing environmental fluctuations. The newly developed elite wheat lines with modified root traits provide valuable materials to study the value of different root systems to support yield in different environments and soil types.
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    Manipulating exudate composition from root apices shapes the microbiome throughout the root system
    Kawasaki, A ; Dennis, PG ; Forstner, C ; Raghavendra, AKH ; Mathesius, U ; Richardson, AE ; Delhaize, E ; Gilliham, M ; Watt, M ; Ryan, PR (OXFORD UNIV PRESS INC, 2021-12)
    Certain soil microorganisms can improve plant growth, and practices that encourage their proliferation around the roots can boost production and reduce reliance on agrochemicals. The beneficial effects of the microbial inoculants currently used in agriculture are inconsistent or short-lived because their persistence in soil and on roots is often poor. A complementary approach could use root exudates to recruit beneficial microbes directly from the soil and encourage inoculant proliferation. However, it is unclear whether the release of common organic metabolites can alter the root microbiome in a consistent manner and if so, how those changes vary throughout the whole root system. In this study, we altered the expression of transporters from the ALUMINUM-ACTIVATED MALATE TRANSPORTER and the MULTIDRUG AND TOXIC COMPOUND EXTRUSION families in rice (Oryza sativa L.) and wheat (Triticum aestivum L.) and tested how the subsequent release of their substrates (simple organic anions, including malate, citrate, and γ-amino butyric acid) from root apices affected the root microbiomes. We demonstrate that these exudate compounds, separately and in combination, significantly altered microbiome composition throughout the root system. However, the root type (seminal or nodal), position along the roots (apex or base), and soil type had a greater influence on microbiome structure than the exudates. These results reveal that the root microbiomes of important cereal species can be manipulated by altering the composition of root exudates, and support ongoing attempts to improve plant production by manipulating the root microbiome.
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    The Metabolic Response of Brachypodium Roots to the Interaction with Beneficial Bacteria Is Affected by the Plant Nutritional Status
    Schillaci, M ; Kehelpannala, C ; Martinez-Seidel, F ; Smith, PMC ; Arsova, B ; Watt, M ; Roessner, U (MDPI, 2021-06)
    The potential of plant growth promoting (PGP) bacteria in improving the performance of plants in suboptimal environments is increasingly acknowledged, but little information is available on the mechanisms underlying this interaction, particularly when plants are subjected to a combination of stresses. In this study, we investigated the effects of the inoculation with the PGP bacteria Azospirillum brasilense (Azospirillum) on the metabolism of the model cereal Brachypodium distachyon (Brachypodium) grown at low temperatures and supplied with insufficient phosphorus. Investigating polar metabolite and lipid fluctuations during early plant development, we found that the bacteria initially elicited a defense response in Brachypodium roots, while at later stages Azospirillum reduced the stress caused by phosphorus deficiency and improved root development of inoculated plants, particularly by stimulating the growth of branch roots. We propose that the interaction of the plant with Azospirillum was influenced by its nutritional status: bacteria were sensed as pathogens while plants were still phosphorus sufficient, but the interaction became increasingly beneficial for the plants as their phosphorus levels decreased. Our results provide new insights on the dynamics of the cereal-PGP bacteria interaction, and contribute to our understanding of the role of beneficial microorganisms in the growth of cereal crops in suboptimal environments.
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    The microbiomes on the roots of wheat (Triticum aestivum L.) and rice (Oryza sativa L.) exhibit significant differences in structure between root types and along root axes
    Kawasaki, A ; Dennis, PG ; Forstner, C ; Raghavendra, AKH ; Richardson, AE ; Watt, M ; Mathesius, U ; Gilliham, M ; Ryan, PR (CSIRO PUBLISHING, 2021)
    There is increasing interest in understanding how the microbial communities on roots can be manipulated to improve plant productivity. Root systems are not homogeneous organs but are comprised of different root types of various ages and anatomies that perform different functions. Relatively little is known about how this variation influences the distribution and abundance of microorganisms on roots and in the rhizosphere. Such information is important for understanding how root-microbe interactions might affect root function and prevent diseases. This study tested specific hypotheses related to the spatial variation of bacterial and fungal communities on wheat (Triticum aestivum L.) and rice (Oryza sativa L.) roots grown in contrasting soils. We demonstrate that microbial communities differed significantly between soil type, between host species, between root types, and with position along the root axes. The magnitude of variation between different root types and along individual roots was comparable with the variation detected between different plant species. We discuss the general patterns that emerged in this variation and identify bacterial and fungal taxa that were consistently more abundant on specific regions of the root system. We argue that these patterns should be measured more routinely so that localised root-microbe interactions can be better linked with root system design, plant health and performance.