Sorghum bicolor TX08001 Nodal root development Gene Expression Profiling
Genome-transcriptome
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Genome-transcriptome
Plant roots and associated microbes release a diverse range of functionally distinct exudates into the surrounding rhizosphere with direct impacts on soil carbon storage, nutrient availability, and contaminant dynamics. Yet mechanistic linkages between root exudation and emergent biogeochemical processes remain challenging to measure nondestructively, in real soil, over time. Here we used a novel combination of in situ microsensors with high-resolution mass spectrometry to measure, nondestructively, changing exudation and associated biogeochemical dynamics along single growing plant roots (Avena sativa). We found that metabolite and dissolved organic carbon (DOC) concentrations as well as microbial growth, redox potential (EH), and pH dynamics vary significantly among bulk soil, root tip, and more mature root zones. Surprisingly, the significant spike of rhizosphere DOC upon root tip emergence did not significantly correlate with any biogeochemical parameters. However, the presence of sugars significantly correlated with declines in EH following the arrival of the root tip, likely due to enhanced microbial oxygen demand. Similarly, the presence of organic acids significantly correlated to declines in pH upon root tip emergence. Altogether, our in situ measurements highlight how different exudates released along growing roots create functionally distinct soil microenvironments that evolve over time.
Carbon-rich peat soils have been drained and used extensively for agriculture throughout human history, leading to significant losses of their soil carbon. One solution for rewetting degraded peat is wet crop cultivation. Crops such as rice, which can grow in water-saturated conditions, could enable agricultural production to be maintained whilst reducing CO 2 and N 2 O emissions from peat. However, wet rice cultivation can release considerable methane (CH 4 ). Water table and soil management strategies may enhance rice yield and minimize CH 4 emissions, but they also influence plant biomass allocation strategies. It remains unclear how water and soil management influences rice allocation strategies and how changing plant allocation and associated traits, particularly belowground, influence CH 4 -related processes. We examined belowground biomass (BGB), aboveground biomass (AGB), belowground:aboveground ratio (BGB:ABG), and a range of root traits (root length, root diameter, root volume, root area, and specific root length) under different soil and water treatments; and evaluated plant trait linkages to CH 4 . Rice (Oryza sativa L.) was grown for six months in field mesocosms under high (saturated) or low water table treatments, and in either degraded peat soil or degraded peat covered with mineral soil. We found that BGB and BGB:AGB were lowest in water saturated conditions where mineral soil had been added to the peat, and highest in low-water table peat soils. Furthermore, CH 4 and BGB were positively related, with BGB explaining 60% of the variation in CH 4 but only under low water table conditions. Our results suggest that a mix of low water table and mineral soil addition could minimize belowground plant allocation in rice, which could further lower CH 4 likely because root-derived carbon is a key substrate for methanogenesis. Minimizing root allocation, in conjunction with water and soil management, could be explored as a strategy for lowering CH 4 emissions from wet rice cultivation in degraded peatlands.
Drought effects are pervasive in terrestrial ecosystems, yet there is limited understanding of how drought impacts the transformation of plant carbon (C) inputs to mineral-associated organic matter (MAOM)—the largest and slowest-cycling pool of soil organic carbon (SOC). In a 12-week 13 C-CO 2 greenhouse labeling experiment, we tracked the formation of MAOM derived from the two dominant sources of plant C input to the mineral soil—living root inputs ( 13 C-rhizodeposits) and decaying root inputs ( 13 C-root detritus)—under normal moisture and droughted conditions in a semiarid grassland soil. At the end of the 12-week period, we also measured the persistence of 13 C-MAOM formed from rhizodeposits versus root detritus via a subsequent persistence assay. Drought reduced the formation of MAOM derived from living roots by decreasing rhizodeposits, reducing microbial growth rates, and altering the composition of organic matter, lipids, and metabolites. Drought initially delayed the formation of MAOM derived from root detritus by slowing the early stages of root litter decomposition (week 4–8), but did not decrease total MAOM formation by the end of the 12-week period. Notably, drought enhanced the persistence of MAOM derived from root detritus, but did not influence the persistence of MAOM derived from rhizodeposits. Our results provide some of the first direct evidence that drought can reduce the formation of MAOM in a grassland soil, but may enhance its persistence, based on the source of plant input from which MAOM is derived.
Abstract The expansion of deciduous shrubs into the graminoid‐dominated arctic tundra is expected to alter litter decomposition by changing litter quality and local abiotic and biotic conditions. However, it remains unclear how shrub expansion will affect litter decomposition at regional scales, where macroclimate is expected to be the dominant regulator of decomposition. To determine the relative influence of macroclimate and local controls on regional patterns of litter mass loss and nitrogen release, we conducted two hierarchical litter decomposition experiments across spatial scales. We decomposed leaf and root litter from a prominent graminoid ( Eriophorum vaginatum ) and three genera of deciduous shrubs ( Betula , Alnus and Salix ) for 1 year within replicated plots at five sites spanning a 160 km latitudinal gradient in northern Alaska. Using Eriophorum litter as a substrate, we found that macroclimate was the primary regulator of mass loss but had opposing effects on leaf and root litter. As summer temperature increased along the latitudinal gradient (11.9 to 13.9°C), leaf litter mass loss increased by 20% whereas root litter mass loss decreased by 33%. Leaf nitrogen release also increased with summer temperature. Conversely, root nitrogen release was controlled by the vegetation type of the decomposition environment. Using different shrub litters as substrates, we found that litter quality and its interaction with soil microclimate and macroclimate controlled decomposition. Overall, shrub root litters decomposed faster than Eriophorum root litter, losing 53% more mass and 190% more nitrogen across all sites and decomposition environments. For leaf litter, however, patterns varied by litter genus, with Salix losing more mass and Betula and Alnus losing less mass than Eriophorum . Our findings demonstrate that shrub expansion in the Arctic can regulate leaf and root litter decomposition at the regional scale through its effects on local controls, primarily litter quality. Ongoing increases in shrub cover are likely to accelerate the turnover of root litter carbon and nitrogen pools in tundra ecosystems. Therefore, including shrub‐related processes in Earth system models will improve our ability to predict regional‐scale litter decomposition and its effects on carbon and nutrient cycling in a warming Arctic. Read the free Plain Language Summary for this article on the Journal blog.
Abstract Tree‐mycorrhizal associations are associated with patterns in nitrogen (N) availability and soil organic matter storage; however, we still lack a mechanistic understanding of what tree and fungal traits drive these patterns and how they will respond to global changes in soil N availability. To address this knowledge gap, we investigated how arbuscular mycorrhizal (AM)‐ and ectomycorrhizal (EcM)‐associated seedlings alter rhizodeposition in response to increased seedling inorganic N acquisition. We grew four species each of EcM and AM seedlings from forests of the eastern United States in a continuously 13 C‐labeled atmosphere within an environmentally controlled chamber and subjected to three levels of 15 N‐labeled fertilizer. We traced seedling 15 N uptake from, and 13 C‐labeled inputs (net rhizodeposition) into, root‐excluded or ‐included soil over a 5‐month growing season. N uptake by seedlings was positively related to rhizodeposition for EcM‐ but not AM‐associated seedlings in root‐included soils. Despite this contrast in rhizodeposition, there was no difference in soil C storage between mycorrhizal types over the course of the experiment. Instead root‐inclusive soils lost C, while root‐exclusive soils gained C. Our findings suggest that mycorrhizal associations mediate tree belowground C investment in response to inorganic N availability, but these differences do not affect C storage. Continued soil warming and N deposition under global change will increase soil inorganic N availability and our seedling results indicate this could lead to greater belowground C investment by EcM‐associated trees. This potential for less efficient N uptake by EcM‐trees could contribute to AM‐tree success and a shift toward more AM‐dominated temperate forests.
Root detritusphere, that is, the soil in the vicinity of decomposing root residues, plays an important role in soil microbial activity and C sequestration. Pore structure (size distributions and connectivity of soil pores) in the detritusphere serves as a major driver for these processes and, in turn, is influenced by the physical characteristics of both soil and roots. This study compared pore structure characteristics in the root detritusphere of soils of contrasting texture and mineralogy subjected to > 6 years of contrasting vegetation: monoculture switchgrass and polyculture prairie systems. Soil samples were collected from five experimental sites in the US Midwest representing three soil types. Soil texture and mineralogy were measured using a hydrometer and x-ray powder diffraction, respectively. The intact cores were scanned with x-ray computed micro-tomography to identify visible soil pores, biopores, and particulate organic matter (POM). We specifically focused on pore structure within the detritusphere around the POM of root origin. Results showed that the detritusphere of coarser textured soils, characterized by high sand and quartz contents, had lower porosity in the vicinity of POM compared with finer textured soils. POM vicinities in finer textured soils had high proportions of large (> 300 μm diameter) pores, and their pores were better connected than in the coarser soils. Lower porosity in the outer (> 1 mm) parts of the detritusphere of switchgrass than of prairie suggested soil compaction by roots, with the effect especially pronounced in the coarser soils. Here, the results demonstrated that soil texture and mineralogy played a major, while vegetation played a more modest, role in defining the pore structure in the root detritusphere.
Carbohydrates, including mixed-linkage glucan (MLG), in grass cell walls make them a valuable potential feedstock for biofuel production. Hence, the development of transgenic grasses with elevated levels of MLG is being actively pursued worldwide. Changes in chemical and physical root characteristics of MLG-overproducing transgenic plants can affect processing of the root-derived carbon (C) by soil microorganisms, impacting soil C cycling. Here, this study is the first attempt to elucidate the impact of MLG-related genetic modifications on root traits, root decomposition, and soil C processing. We explored four genotypes of Brachypodium ( Brachypodium distachyon ): a wildtype, a loss-of-function mutant with low MLG, an MLG overexpressing line, and a line lacking MLG hydrolase (with high MLG), incubating their roots in soils of two contrasting vegetation histories: monoculture switchgrass and polyculture restored prairie. The four genotypes exhibited contrasting root MLG and soluble sugar concentrations, and different growth phenotypes. Roots with the highest MLG content resulted in a ∼55 % increase in microbial biomass C compared to wildtype in both soils. However, the genotype effects on C mineralization rates were influenced by the vegetation history, with significant effects observed only in the soil from switchgrass but not prairie origin. While further work is required to understand the full impact of MLG-overproducing plants on soil C accrual, our findings suggest that their influence on soil C processes cannot be discounted.
The rhizosphere is a dynamic environment where rhizodeposits that include primary and secondary metabolites and mucilage serve as nutrient sources for soil microorganisms, attracting them toward plant roots. However, understanding how these microbes specifically respond to plant root chemical signals has been hindered by the challenges of disentangling physical and chemical interactions between the microbes and plant roots. To address this, we implemented an innovative filter-based experimental setup on plant roots that creates a physical barrier while facilitating the exchange of chemical signals. The proteomic analysis of 10 Populus root-associated bacterial strains grown in the presence or absence of a plant in either individual or mixed community conditions provided detailed insights into the functional responses of these strains to the root chemical environment. Additionally, this approach allowed us to discern the impact of root exudates on overall community dynamics. In particular, metaproteomic analyses revealed that each of these 10 microbial members responds uniquely to the presence of the plant, with Bacillus and Pantoea exhibiting the most dramatic favorable impact. Proteomic examination revealed the details of metabolism fine-tuning, including processes such as chemotaxis and ATP-binding cassette transporter proteins. This study demonstrates the application of a filter-based experimental setup to study microbial responses to plant chemicals and sheds light on adaptation strategies employed by various bacterial strains for survival in the rhizosphere.
Plants play a key role in mediating soil response to global change, and breeding or engineering crops to increase soil organic carbon (SOC) storage is a potential route to land-based carbon dioxide removal in agricultural systems. However, due to limited observational datasets plus shifting paradigms of SOC stabilization, it is unclear which plant traits are most important for enhancing different types of soil organic matter. Existing long-term common gardens of genetically diverse plant populations may provide an opportunity to evaluate biological controls on SOC, separate from environmental or management variability. Here we report on soil and root chemical data collected for 24 genotypes within a 13-year-old common garden in northwestern Oregon planted with a large natural variant population of Populus trichocarpa. Fractionating surface soil (0–15 cm) revealed substantial variation in stocks of mineral-associated organic matter (MAOM; 18–67 t C/ha) and particulate organic matter (POM; 2–22 t C/ha). Tree genotype explained 24% and 26% of the MAOM and POM stock variability, respectively, after controlling for background variability. We found minimal association between SOC concentration and either aboveground tree productivity or root biomass recalcitrance (C/N ratios and lignin content). In contrast, root elemental content appeared influential for MAOM-C concentration, which showed a strong positive association with root aluminum (Al) and a strong negative association with root boron (B) and magnesium (Mg). Furthermore, root concentrations of these elements were highly heritable (57%–78%) and not simply a reflection of background variation in soil elemental concentrations. We estimate that surface SOC stocks under these 24 genotypes have diverged at rates of up to 1.2–4.3 t C/ha/year. These results suggest that long-term genetic diversity trials have value for elucidating biological controls on soil organic matter dynamics, and that traits associated with root elemental content may be a useful target for enhancing biosequestration.
The below-ground growing season often extends beyond the above-ground growing season in tundra ecosystems and as the climate warms, shifts in growing seasons are expected. However, we do not yet know to what extent, when and where asynchrony in above- and below-ground phenology occurs and whether variation is driven by local vegetation communities or spatial variation in microclimate. Here, we combined above- and below-ground plant phenology metrics to compare the relative timings and magnitudes of leaf and fine-root growth and senescence across microclimates and plant communities at five sites across the Arctic and alpine tundra biome. We observed asynchronous growth between above- and below-ground plant tissue, with the below-ground season extending up to 74% (~56 days) beyond the onset of above-ground leaf senescence. Plant community type, rather than microclimate, was a key factor controlling the timing, productivity, and growth rates of fine roots, with graminoid roots exhibiting a distinct ‘pulse’ of growth later into the growing season than shrub roots. Our findings indicate the potential of vegetation change to influence below-ground carbon storage as the climate warms and roots remain active in unfrozen soils for longer. Taken together, our findings of increased root growth in soils that remain thawed later into the growing season, in combination with ongoing tundra vegetation change including increased shrub and graminoid abundance, indicate increased below-ground productivity and altered carbon cycling in the tundra biome.
Stomatal closure is a pervasive response among trees exposed to flooded soil. We tested whether this response is caused by reduced hydraulic conductance in the soil-to-leaf hydraulic continuum (k total ), and particularly by reduced root hydraulic conductance (k root ), which has been widely hypothesized. We tracked stomatal conductance at the leaf level (g s ) and canopy scale (G s ) along with physiological conditions in two temperate tree species, Magnolia grandiflora and Quercus virginiana, that were subjected to flood and control conditions in a greenhouse experiment. Flooding reduced g s , G s , k root and k total . Path analysis showed strong support for direct effects of k total on g s and for flood duration on k total , but not k root on k total . A process-based model that accounted for the k total reduction predicted the timeseries of G s in flood and control treatment trees reasonably well (predicted versus observed G s R 2 = 0.80 and 0.51 for M. grandiflora and Q. virginiana, respectively). However, accounting only for k root reduction in flooded trees was insufficient for predicting observed G s reduction. Together, these results suggest that hydraulic constraints were not limited to roots and highlight the need to account for flooding effects on k total when projecting forest ecosystem function using process-based models.
The soil environment affected by plant roots and their exudates, termed the rhizosphere, significantly impacts crop health and is an attractive target for engineering desirable agricultural traits. Engineering microbes in the rhizosphere is one approach to improving crop yields that directly minimizes the number of genetic modifications made to plants. Soil microbes have the potential to assist with nutrient acquisition, heat tolerance, and drought response if they can persist in the rhizosphere in the correct numbers. Unfortunately, the mechanisms by which microbes adhere and persist on plant roots are poorly understood, limiting their application. This study examined the membrane proteome shift upon adherence to roots in two bacteria of interest, Klebsiella variicola and Pseudomonas putida. From this surface proteome data, we identified a novel membrane protein from a non-laboratory isolate of P. putida that increases binding to maize roots using unlabeled proteomics. When this protein was moved from the environmental isolate to a common lab strain (P. putida KT2440), we observed increased binding capabilities of P. putida KT2440 to both abiotic mimic surfaces and maize roots. We observed a similar increased binding capability to maize roots when the protein was heterologously expressed in K. variicola and Stutzerimonas stutzeri. With the discovery of this novel binding protein, we outline a strategy for harnessing natural selection and wild isolates to build more persistent strains of bacteria for field applications and plant growth promotion.
The extensive use of nitrogen fertilizers has detrimental environmental consequences, and it is essential for society to explore sustainable alternatives. One promising avenue is engineering root nodule symbiosis, a naturally occurring process in certain plant species within the nitrogen-fixing clade, into non-leguminous crops. Advancements in single-cell transcriptomics provide unprecedented opportunities to dissect the molecular mechanisms underlying root nodule symbiosis at the cellular level. This review summarizes key findings from single-cell studies in Medicago truncatula, Lotus japonicus, and Glycine max. We highlight how these studies address fundamental questions about the development of root nodule symbiosis, including the following findings: (i) single-cell transcriptomics has revealed a conserved transcriptional program in root hair and cortical cells during rhizobial infection, suggesting a common infection pathway across legume species; (ii) characterization of determinate and indeterminate nodules using single-cell technologies supports the compartmentalization of nitrogen fixation, assimilation, and transport into distinct cell populations; (iii) single-cell transcriptomics data have enabled the identification of novel root nodule symbiosis genes and provided new approaches for prioritizing candidate genes for functional characterization; and (iv) trajectory inference and RNA velocity analyses of single-cell transcriptomics data have allowed the reconstruction of cellular lineages and dynamic transcriptional states during root nodule symbiosis.
Harnessing rhizosphere processes offers a valuable opportunity to optimize nutrient use efficiency in agroecosystems. In nutrient-limited soils, plants discharge part of photosynthate surplus via root exudation, including carboxylates, which may enhance mineral dissolution and nutrient mobilization. We aimed to assess how plant responses to nutrient limitation translated into changes in exudate profiles, and how these exudates, in turn, drive bioweathering processes across soils of contrasting mineralogy and weathering degree. We conducted a hydroponic experiment with Lupinus albus grown under five phosphorus (P) concentrations (5, 10, 20, 30, and 50 µM) over seven weeks. We measured plant biomass and root traits, performed a metabolomics analysis and quantified seven carboxylates in root exudates using gas chromatography-mass spectrometry. To assess bioweathering processes across contrasted soil domains, we conducted batch dissolution tests with exudates using three soil horizons—35 each with distinct physicochemical properties: enriched in organic matter, iron oxides, or primary silicates. At the intermediate level of P supply, shoot biomass was comparable to that under high P, but plants produced more root biomass and a higher total carboxylate exudation rate. Despite low carboxylate concentrations (<100 ppb), exudates promoted the dissolution of Ca, Mg, Si, Fe, P and K in all horizons. Yet, the degree of element released varied among horizons. These findings highlight the importance of root exudates in enhancing mineral dissolution, with effects dependent on soil physicochemical properties. The results suggest that managing agroecosystems under moderate nutrient limitation could be a sustainable strategy to increase root-to-shoot ratios, enhance bioweathering processes and nutrient release in soil solution.
Experimental soil heating experiments have found a consistent increase in soil-surface CO 2 emissions ( F s ), but inconsistent soil organic carbon (SOC) responses. Interpretation of heating effects is complicated by spatial heterogeneity and soil moisture, nitrogen availability, and microbial and plant responses. Here we applied a mechanistic ecosystem model to interpret heating impacts on a California forest subjected to 1 m deep, 4°C heating. The model accurately simulated control-plot CO 2 fluxes, SOC stocks, fine root biomass, soil moisture, and soil temperature, and the observed increases in F s and decreases in fine root biomass. We show that a complex suite of interactions can lead to a consistent increase in F s (~17%) over the 5-year study period, with very small changes in SOC stocks (<1%). Modeled increases in leaf water stress from soil drying reduced GPP and NPP. The resulting reduction in leaf and fine root allocation increased fine root litter inputs to the soil and reduced root exudation. Soil heating led to about a 50% larger increase in root autotrophic respiration than in heterotrophic respiration, with the heating effect on both these fluxes decreasing over the simulation period. Increased heterotrophic respiration led to increased soil N availability and plant N uptake. These heating responses are mechanistically linked, of magnitudes that can affect ecosystem dynamics, and long-term observations of them are rarely made. Therefore, we conclude that a coupled observational and mechanistic modeling framework is needed to interpret manipulation experiments, and to improve projections of climate change impacts on terrestrial ecosystem carbon dynamics.
Abstract The presence of Arbuscular Mycorrhizal Fungi (AMF) in vascular land plant roots is one of the most ancient of symbioses supporting nitrogen and phosphorus exchange for photosynthetically derived carbon. Here we provide a multi-scale modeling approach to predict AMF colonization of a worldwide crop from a Recombinant Inbred Line (RIL) population derived from Sorghum bicolor and S. propinquum . The high-throughput phenotyping methods of fungal structures here rely on a Mask Region-based Convolutional Neural Network (Mask R-CNN) in computer vision for pixel-wise fungal structure segmentations and mixed linear models to explore the relations of AMF colonization, root niche, and fungal structure allocation. Models proposed capture over 95% of the variation in AMF colonization as a function of root niche and relative abundance of fungal structures in each plant. Arbuscule allocation is a significant predictor of AMF colonization among sibling plants. Arbuscules and extraradical hyphae implicated in nutrient exchange predict highest AMF colonization in the top root section. Our work demonstrates that deep learning can be used by the community for the high-throughput phenotyping of AMF in plant roots. Mixed linear modeling provides a framework for testing hypotheses about AMF colonization phenotypes as a function of root niche and fungal structure allocations.
Plant strategies to acquire nutrients from limited environments help shape ecosystem carbon (C) and nitrogen (N) cycling and response to environmental change. The effects of plant strategies on ecosystem dynamics are largely uncharacterized in bioenergy agroecosystems, where the impacts could determine bioenergy's ability to meet its sustainability goals of storing C and reducing N loss. We used FUN-BioCROP (Fixation and Uptake of Nitrogen-Bioenergy Carbon, Rhizosphere, Organisms and Protection), a plant–microbe interaction model of coupled plant nutrient uptake and soil organic matter decomposition, to simulate the effects of nutrient acquisition strategies on soil microbial activity and ecosystem nutrient cycling in bioenergy feedstocks miscanthus (Miscanthus × giganteus) and sorghum (Sorghum bicolor (L.) Moench). We examined the model's ability to reproduce the relative effects of belowground nutrient uptake on microbial activity using a reanalysis of empirical data showing that miscanthus root exudation provoked a larger soil microbial response than sorghum. From baseline model simulations, we found that the ability of miscanthus to retranslocate N resulted in higher N uptake at a lower C cost than the sorghum/soybean rotation and that soil C and N pools increased under perennial (miscanthus) and decreased under annual (sorghum/soybean) cultivation. The model also predicted that greater root exudation increased soil C accumulation, highlighting the role of roots in forming stable soil C. Overall, the baseline model was unable to reproduce field observations of miscanthus root exudation stimulating microbial activity more than sorghum. To improve the model, we updated the soil microbial parameters in miscanthus to have faster decomposition, a higher C/N ratio, and greater carbon use efficiency. These changes improved the simulated soil microbial response to miscanthus root exudation, supporting the hypothesis that miscanthus soils foster a microbial community that is more responsive to root exudation than that of sorghum.