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  1. Arias, Renee S. (Ed.)
    ABSTRACT

    Due to climate change, drought frequencies and severities are predicted to increase across the United States. Plant responses and adaptation to stresses depend on plant genetic and environmental factors. Understanding the effect of those factors on plant performance is required to predict species’ responses to environmental change. We used reciprocal gardens planted with distinct regional ecotypes of the perennial grassAndropogon gerardiiadapted to dry, mesic, and wet environments to characterize their rhizosphere communities using 16S rRNA metabarcode sequencing. Even though the local microbial pool was the main driver of these rhizosphere communities, the significant plant ecotypic effect highlighted active microbial recruitment in the rhizosphere, driven by ecotype or plant genetic background. Our data also suggest that ecotypes planted at their homesites were more successful in recruiting rhizosphere community members that were unique to the location. The link between the plants’ homesite and the specific local microbes supported the “home field advantage” hypothesis. The unique homesite microbes may represent microbial specialists that are linked to plant stress responses. Furthermore, our data support ecotypic variation in the recruitment of congeneric but distinct bacterial variants, highlighting the nuanced plant ecotype effects on rhizosphere microbiome recruitment. These results improve our understanding of the complex plant host–soil microbe interactions and should facilitate further studies focused on exploring the functional potential of recruited microbes. Our study has the potential to aid in predicting grassland ecosystem responses to climate change and impact restoration management practices to promote grassland sustainability.

    IMPORTANCE

    In this study, we used reciprocal gardens located across a steep precipitation gradient to characterize rhizosphere communities of distinct dry, mesic, and wet regional ecotypes of the perennial grassAndropogon gerardii. We used 16S rRNA amplicon sequencing and focused oligotyping analysis and showed that even though location was the main driver of the microbial communities, ecotypes could potentially recruit distinct bacterial populations. We showed that differentA. gerardiiecotypes were more successful in overall community recruitment and recruitment of microbes unique to the “home” environment, when growing at their “home site.” We found evidence for “home-field advantage” interactions between the host and host–root-associated bacterial communities, and the capability of ecotypes to recruit specialized microbes that were potentially linked to plant stress responses. Our study aids in a better understanding of the factors that affect plant adaptation, improve management strategies, and predict grassland function under the changing climate.

     
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    Free, publicly-accessible full text available October 17, 2024
  2. Abstract

    Meeting restoration targets may require active strategies to accelerate natural regeneration rates or overcome the resilience associated with degraded ecosystem states. Introducing desired ecosystem patches in degraded landscapes constitutes a promising active restoration strategy, with various mechanisms potentially causing these patches to become foci from which desired species can re‐establish throughout the landscape. This study considers three mechanisms previously identified as potential drivers of introduced patch dynamics: autocatalytic nucleation, directed dispersal, and resource concentration. These mechanisms reflect qualitatively different positive feedbacks. We developed an ecological model framework that compared how the occurrence of each mechanism was reflected in spatio‐temporal patch dynamics. We then analyzed the implications of these relationships for optimal restoration design. We found that patch expansion accelerated over time when driven by the autocatalytic nucleation mechanism, while patch expansion driven by the directed dispersal or resource concentration mechanisms decelerated over time. Additionally, when driven by autocatalytic nucleation, patch expansion was independent of patch position in the landscape. However, the proximity of other patches affected patch expansion either positively or negatively when driven by directed dispersal or resource concentration. For autocatalytic nucleation, introducing many small patches was a favorable strategy, provided that each individual patch exceeded a critical patch size. Introducing a single patch or a few large patches was the most effective restoration strategy to initiate the directed dispersal mechanism. Introducing many small patches was the most effective strategy for reaching restored ecosystem states driven by a resource concentration mechanism. Our model results suggest that introducing desirable patches can substantially accelerate ecosystem restoration, or even induce a critical transition from an otherwise stable degraded state toward a desired ecosystem state. However, the potential of this type of restoration strategy for a particular ecosystem may strongly depend on the mechanism driving patch dynamics. In turn, which mechanism drives patch dynamics may affect the optimal spatial design of an active restoration strategy. Each of the three mechanisms considered reflects distinct spatio‐temporal patch dynamics, providing novel opportunities for empirically identifying key mechanisms, and restoration designs that introduce desired patches in degraded landscapes according to these patch dynamics.

     
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  3. Abstract

    Baseline levels of glucosinolates—important defensive phytochemicals in brassicaceous plants—are determined by both genotype and environment. However, the ecological causes of glucosinolate plasticity are not well characterized. Fertilization is known to alter glucosinolate content of Brassica crops, but the effect of naturally occurring soil variation on glucosinolate content of wild plants is unknown. Here, we conducted greenhouse experiments using Boechera stricta to ask (i) whether soil variation among natural habitats shapes leaf and root glucosinolate profiles; (ii) whether such changes are caused by abiotic soil properties, soil microbes, or both; and (iii) whether soil-induced glucosinolate plasticity is genetically variable. Total glucosinolate quantity differed up to 2-fold between soils from different natural habitats, while the relative amounts of different compounds were less responsive. This effect was due to physico-chemical soil properties rather than microbial communities. We detected modest genetic variation for glucosinolate plasticity in response to soil. In addition, glucosinolate composition, but not quantity, of field-grown plants could be accurately predicted from measurements from greenhouse-grown plants. In summary, soil alone is sufficient to cause plasticity of baseline glucosinolate levels in natural plant populations, which may have implications for the evolution of this important trait across complex landscapes.

     
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  4. Abstract Background

    The maize inbred line A188 is an attractive model for elucidation of gene function and improvement due to its high embryogenic capacity and many contrasting traits to the first maize reference genome, B73, and other elite lines. The lack of a genome assembly of A188 limits its use as a model for functional studies.

    Results

    Here, we present a chromosome-level genome assembly of A188 using long reads and optical maps. Comparison of A188 with B73 using both whole-genome alignments and read depths from sequencing reads identify approximately 1.1 Gb of syntenic sequences as well as extensive structural variation, including a 1.8-Mb duplication containing the Gametophyte factor1 locus for unilateral cross-incompatibility, and six inversions of 0.7 Mb or greater. Increased copy number of carotenoid cleavage dioxygenase 1 (ccd1) in A188 is associated with elevated expression during seed development. Highccd1expression in seeds together with low expression of yellow endosperm 1 (y1) reduces carotenoid accumulation, accounting for the white seed phenotype of A188. Furthermore, transcriptome and epigenome analyses reveal enhanced expression of defense pathways and altered DNA methylation patterns of the embryonic callus.

    Conclusions

    The A188 genome assembly provides a high-resolution sequence for a complex genome species and a foundational resource for analyses of genome variation and gene function in maize. The genome, in comparison to B73, contains extensive intra-species structural variations and other genetic differences. Expression and network analyses identify discrete profiles for embryonic callus and other tissues.

     
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  5. Abstract

    Rooting depth is an ecosystem trait that determines the extent of soil development and carbon (C) and water cycling. Recent hypotheses propose that human‐induced changes to Earth's biogeochemical cycles propagate deeply into Earth's subsurface due to rooting depth changes from agricultural and climate‐induced land cover changes. Yet, the lack of a global‐scale quantification of rooting depth responses to human activity limits knowledge of hydrosphere‐atmosphere‐lithosphere feedbacks in the Anthropocene. Here we use land cover data sets to demonstrate that root depth distributions are changing globally as a consequence of agricultural expansion truncating depths above which 99% of root biomass occurs (D99) by ∼60 cm, and woody encroachment linked to anthropogenic climate change extending D99 in other regions by ∼38 cm. The net result of these two opposing drivers is a global reduction of D99 by 5%, or ∼8 cm, representing a loss of ∼11,600 km3of rooted volume. Projected land cover scenarios in 2100 suggest additional future D99 shallowing of up to 30 cm, generating further losses of rooted volume of ∼43,500 km3, values exceeding root losses experienced to date and suggesting that the pace of root shallowing will quicken in the coming century. Losses of Earth's deepest roots—soil‐forming agents—suggest unanticipated changes in fluxes of water, solutes, and C. Two important messages emerge from our analyses: dynamic, human‐modified root distributions should be incorporated into earth systems models, and a significant gap in deep root research inhibits accurate projections of future root distributions and their biogeochemical consequences.

     
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  6. Abstract

    Plant–microbe interactions play an important role in structuring plant communities. Arbuscular mycorrhizal fungi (AMF) are particularly important. Nonetheless, increasing anthropogenic disturbance will lead to novel plant–AMF interactions, altering longstanding co‐evolutionary trajectories between plants and their associated AMF. Although emerging work shows that plant–AMF response can evolve over relatively short time scales due to anthropogenic change, little work has evaluated how plant AMF responsespecificitymay evolve due to novel plant–mycorrhizal interactions. Here, we examine changes in plant–AMF interactions in novel grassland systems by comparing the mycorrhizal response of plant populations from unplowed native prairies with populations from post‐agricultural grasslands to inoculation with both native prairie AMF and non‐native novel AMF. Across four plant species, we find support for evolution of differential responses to mycorrhizal inocula types, that is, mycorrhizal response specificity, consistent with expectations of local adaptation, with plants from native populations responding most to native AMF and plants from post‐agricultural populations responding most to non‐native AMF. We also find evidence of evolution of mycorrhizal response in two of the four plant species, as overall responsiveness to AMF changed from native to post‐agricultural populations. Finally, across all four plant species, roots from native prairie populations had lower levels of mycorrhizal colonization than those of post‐agricultural populations. Our results report on one of the first multispecies assessment of local adaptation to AMF. The consistency of the responses in our experiment among four species provides evidence that anthropogenic disturbance may have unintended impacts on native plant species' association with AMF, causing evolutionary change in the benefit native plant species gain from native symbioses.

     
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  7. Summary

    Breeders and evolutionary geneticists have grappled with the complexity of the ‘genotype‐to‐phenotype map’ for decades. Now, recent studies highlight the relevance of this concept for understanding heritability of plant microbiomes. Because host phenotype is a more proximate cause of microbiome variation than host genotype, microbiome heritability varies across plant anatomy and development. Fine‐scale variation of plant traits within organs suggests that the well‐established concept of ‘microbiome compartment’ should be refined. Additionally, recent work shows that the balance of deterministic processes (including host genetic effects) vs stochastic processes also varies over time and space. Together, these findings suggest that re‐centering plant phenotype – both as a predictor and a readout of microbiome function – will accelerate new insights into microbiome heritability.

     
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  8. Abstract

    Microbiomes have profound effects on host fitness, yet we struggle to understand the implications for host ecology. Microbiome influence on host ecology has been investigated using two independent frameworks. Classical ecological theory powerfully represents mechanistic interactions predicting environmental dependence of microbiome effects on host ecology, but these models are notoriously difficult to evaluate empirically. Alternatively, host–microbiome feedback theory represents impacts of microbiome dynamics on host fitness as simple net effects that are easily amenable to experimental evaluation. The feedback framework enabled rapid progress in understanding microbiomes’ impacts on plant ecology, and can also be applied to animal hosts. We conceptually integrate these two frameworks by deriving expressions for net feedback in terms of mechanistic model parameters. This generates a precise mapping between net feedback theory and classic population modelling, thereby merging mechanistic understanding with experimental tractability, a necessary step for building a predictive understanding of microbiome influence on host ecology.

     
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  9. Abstract

    It remains unclear how warming will affect resource flows during soil organic matter (SOM) decomposition, in part due to uncertainty in how exoenzymes produced by microbes and roots will function. Rising temperatures can enhance the activity of most exoenzymes, but soil pH can impose limitations on their catalytic efficiency. The effects of temperature and pH on enzyme activity are often examined in environmental samples, but purified enzyme kinetics reveal fundamental attributes of enzymes’ intrinsic temperature responses and how relative release of decay‐liberated resources (their flow ratios) can change with environmental conditions. In this paper, we illuminate the principle that fundamental, biochemical limitations on SOM release of C, N, and P during decay, and differential exoenzymes’ responses to the environment, can exert biosphere‐scale significance on the stoichiometry of bioavailable soil resources. To that end, we combined previously published intrinsic temperature sensitivities of two hydrolytic enzymes that release C and N during decay with a novel data set characterizing the kinetics of a P‐releasing enzyme (acid phosphatase) across an ecologically relevant pH gradient. We use these data to estimate potential change in the flow ratios derived from these three enzymes’ activities (C:N, C:P, and N:P) at the global scale by the end of the century, based on temperature projections and soil pH distribution. Our results highlight how the temperature sensitivity of these hydrolytic enzymes and the influence of pH on that sensitivity can govern the relative availability of bioavailable resources derived from these enzymes. The work illuminates the utility of weaving well‐defined kinetic constraints of microbes’ exoenzymes into models that incorporate changing SOM inputs and composition, nutrient availability, and microbial functioning into their efforts to project terrestrial ecosystem functioning in a changing climate.

     
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  10. Abstract

    Riparian zones, the interfaces between land and stream, perform vital ecosystem functions including transformation and retention of nutrients and sediment moving across the landscape. Although many studies assess transport through and transformation of materials in riparian zones, less is known about the direct influence of precipitation falling on these zones on material retention and transport. Additionally, few experiments can compare riparian retention to stream‐channel retention.

    We present a novel experimental approach to assess retention of nitrate entering as precipitation in riparian zones and compare riparian retention and movement of nitrate, other ions, sediments to and within the adjacent stream channel. We simulated an intense precipitation event with15N‐labelled nitrate as a bioactive solute and bromide as an inert tracer. This method extends tracer release approaches applied to streams worldwide and links it to processes at the aquatic/ terrestrial interface. It further allows determination of movement of materials into streams from bankside precipitation.

    The riparian zone removed or retained a greater proportion of nitrate than the stream relative to bromide; over half the added bromide reached the stream through a few metres of riparian zone, compared to only 0.2% of the added nitrate. Of the 0.2% that reached the stream, 30% of that nitrate was removed or retained by instream processes after travelling 60 downstream. Roughly 10% of the total15N addition ended up sequestered in the above‐ground portions of the riparian grasses by the end of the growing season, and very little of it was recovered from the soil. We saw little evidence of bulk transport of other ions or sediment from this riparian soil to the stream.

    Our data are consistent with the concept of high nitrate retention in vegetated riparian zones, even for nitrate falling directly upon them in the form of atmospheric deposition in precipitation.

     
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