Quantitative genetic-by-soil microbiome interactions in a perennial grass affect functional traits.

Plants interact with diverse microbiomes that can impact plant growth and performance. Recent studies highlight the potential beneficial aspects of plant microbiomes, including the possibility that microbes facilitate the process of local adaptation in their host plants. Microbially mediated local adaptation in plants occurs when local host genotypes have higher fitness than foreign genotypes because of their affiliation with locally beneficial microbes. Here, plant adaptation results from genetic interactions of the host with locally beneficial microbes (e.g. host genotype-by-microbiome interactions). We used a recombinant inbred line (RIL) mapping population derived from upland and lowland ecotypes of the diploid C4 perennial bunch grass Panicum hallii to explore quantitative genetic responses to soil microbiomes focusing on functional root and shoot traits involved in ecotypic divergence. We show that the growth and development of ecotypes and their trait divergence depends on soil microbiomes. Moreover, we find that the genetic architecture is modified by soil microbiomes, revealing important plant genotype-by-microbiome interactions for quantitative traits. We detected a number of quantitative trait loci (QTL) that interact with the soil microbiome. Our results highlight the importance of microbial interactions in ecotypic divergence and trait genetic architecture in C4 perennial grasses.

Legacies of precipitation influence primary production in Panicum virgatum.

Precipitation is a key driver of primary production worldwide, but primary production does not always track year-to-year variation in precipitation linearly. Instead, plant responses to changes in precipitation may exhibit time lags, or legacies of past precipitation. Legacies can be driven by multiple mechanisms, including persistent changes in plant physiological and morphological traits and changes to the physical environment, such as plant access to soil water. We used three precipitation manipulation experiments in central Texas, USA to evaluate the magnitude, duration, and potential mechanisms driving precipitation legacies on aboveground primary production of the perennial C4 grass, Panicum virgatum. Specifically, we performed a rainout shelter study, where eight genotypes grew under different precipitation regimes; a transplant study, where plants that had previously grown in a rainout shelter under different precipitation regimes were moved to a common environment; and a mesocosm study, where the effect of swapping precipitation regime was examined with a single genotype. Across these experiments, plants previously grown under wet conditions generally performed better than expected when exposed to drought. Panicum virgatum exhibited stronger productivity legacies of past wet years on current-year responses to drought than of past dry years on current-year responses to wet conditions. Additionally, previous year tiller counts, a proxy for meristem availability, were important in determining legacy effects on aboveground production. As climate changes and precipitation extremes-both dry and wet-become more common, these results suggest that populations of P. virgatum may become less resilient.

Multiple constraints cause positive and negative feedbacks limiting grassland soil CO2 efflux under CO2 enrichment.

Terrestrial ecosystems are increasingly enriched with resources such as atmospheric CO2 that limit ecosystem processes. The consequences for ecosystem carbon cycling depend on the feedbacks from other limiting resources and plant community change, which remain poorly understood for soil CO2 efflux, JCO2, a primary carbon flux from the biosphere to the atmosphere. We applied a unique CO2 enrichment gradient (250 to 500 µL L-1) for eight years to grassland plant communities on soils from different landscape positions. We identified the trajectory of JCO2 responses and feedbacks from other resources, plant diversity [effective species richness, exp(H)], and community change (plant species turnover). We found linear increases in JCO2 on an alluvial sandy loam and a lowland clay soil, and an asymptotic increase on an upland silty clay soil. Structural equation modeling identified CO2 as the dominant limitation on JCO2 on the clay soil. In contrast with theory predicting limitation from a single limiting factor, the linear JCO2 response on the sandy loam was reinforced by positive feedbacks from aboveground net primary productivity and exp(H), while the asymptotic JCO2 response on the silty clay arose from a net negative feedback among exp(H), species turnover, and soil water potential. These findings support a multiple resource limitation view of the effects of global change drivers on grassland ecosystem carbon cycling and highlight a crucial role for positive or negative feedbacks between limiting resources and plant community structure. Incorporating these feedbacks will improve models of terrestrial carbon sequestration and ecosystem services.

The Genetic Architecture of Shoot and Root Trait Divergence Between Mesic and Xeric Ecotypes of a Perennial Grass.

Environmental heterogeneity can drive patterns of functional trait variation and lead to the formation of locally adapted ecotypes. Plant ecotypes are often differentiated by suites of correlated root and shoot traits that share common genetic, developmental, and physiological relationships. For instance, although plant water loss is largely governed by shoot systems, root systems determine water access and constrain shoot water status. To evaluate the genetic basis of root and shoot trait divergence, we developed a recombinant inbred population derived from mesic and xeric ecotypes of the perennial grass Panicum hallii. Our study sheds light on the genetic architecture underlying the relationships between root and shoot traits. We identified several genomic "hotspots" which control suites of correlated root and shoot traits, thus indicating genetic coordination between plant organ systems in the process of ecotypic divergence. Genomic regions of colocalized quantitative trait locus (QTL) for the majority of shoot and root growth related traits were independent of colocalized QTL for shoot and root resource acquisition traits. The allelic effects of individual QTL underscore ecological specialization for drought adaptation between ecotypes and reveal possible hybrid breakdown through epistatic interactions. These results have implications for understanding the factors constraining or facilitating local adaptation in plants.

CO2 enrichment and soil type additively regulate grassland productivity.

Atmospheric CO2 enrichment usually increases the aboveground net primary productivity (ANPP) of grassland vegetation, but the magnitude of the ANPP-CO2 response differs among ecosystems. Soil properties affect ANPP via multiple mechanisms and vary over topographic to geographic gradients, but have received little attention as potential modifiers of the ANPP-CO2 response. We assessed the effects of three soil types, sandy loam, silty clay and clay, on the ANPP response of perennial C3 /C4 grassland communities to a subambient to elevated CO2 gradient over 10 yr in Texas, USA. We predicted an interactive, rather than additive, effect of CO2 and soil type on ANPP. Contrary to prediction, CO2 and soil additively influenced grassland ANPP. Increasing CO2 by 250 µl l-1 increased ANPP by 170 g m-2 across soil types. Increased clay content from 10% to 50% among soils reduced ANPP by 50 g m-2 . CO2 enrichment increased ANPP via a predominant direct effect, accompanied by a smaller indirect effect mediated by a successional shift to increased dominance of the C4 tallgrass Sorghastrum nutans. Our results indicate a large, positive influence of CO2 enrichment on grassland productivity that resulted from the direct physiological benefits of CO2 augmented by species succession, and was expressed similarly across soils of differing physical properties.

The genomic landscape of molecular responses to natural drought stress in Panicum hallii.

Environmental stress is a major driver of ecological community dynamics and agricultural productivity. This is especially true for soil water availability, because drought is the greatest abiotic inhibitor of worldwide crop yields. Here, we test the genetic basis of drought responses in the genetic model for C4 perennial grasses, Panicum hallii, through population genomics, field-scale gene-expression (eQTL) analysis, and comparison of two complete genomes. While gene expression networks are dominated by local cis-regulatory elements, we observe three genomic hotspots of unlinked trans-regulatory loci. These regulatory hubs are four times more drought responsive than the genome-wide average. Additionally, cis- and trans-regulatory networks are more likely to have opposing effects than expected under neutral evolution, supporting a strong influence of compensatory evolution and stabilizing selection. These results implicate trans-regulatory evolution as a driver of drought responses and demonstrate the potential for crop improvement in drought-prone regions through modification of gene regulatory networks.

Flowering in grassland predicted by CO2 and resource effects on species aboveground biomass.

Continuing enrichment of atmospheric CO2 may change plant community composition, in part by altering the availability of other limiting resources including soil water, nutrients, or light. The combined effects of CO2 enrichment and altered resource availability on species flowering remain poorly understood. We quantified flowering culm and ramet production and biomass allocation to flowering culms/ramets for 10 years in C4 -dominated grassland communities on contrasting soils along a CO2 concentration gradient spanning pre-industrial to expected mid-21st century levels (250-500 µl/L). CO2 enrichment explained up to 77% of the variation in flowering culm count across soils for three of the five species, and was correlated with flowering culm count on at least one soil for four of five species. In contrast, allocation to flowering culms was only weakly correlated with CO2 enrichment for two species. Flowering culm counts were strongly correlated with species aboveground biomass (AGB; R2  = .34-.74), a measure of species abundance. CO2 enrichment also increased soil moisture and decreased light levels within the canopy but did not affect soil inorganic nitrogen availability. Structural equation models fit across the soils suggested species-specific controls on flowering in two general forms: (1) CO2 effects on flowering culm count mediated by canopy light level and relative species AGB (species AGB/total AGB) or by soil moisture effects on flowering culm count; (2) effects of canopy light level or soil inorganic nitrogen on flowering and/or relative species AGB, but with no significant CO2 effect. Understanding the heterogeneity in species responses to CO2 enrichment in plant communities across soils in edaphically variable landscapes is critical to predict CO2 effects on flowering and other plant fitness components, and species potential to adapt to future environmental changes.

A CO2 Concentration Gradient Facility for Testing CO2 Enrichment and Soil Effects on Grassland Ecosystem Function.

Continuing increases in atmospheric carbon dioxide concentrations (CA) mandate techniques for examining impacts on terrestrial ecosystems. Most experiments examine only two or a few levels of CA concentration and a single soil type, but if CA can be varied as a gradient from subambient to superambient concentrations on multiple soils, we can discern whether past ecosystem responses may continue linearly in the future and whether responses may vary across the landscape. The Lysimeter Carbon Dioxide Gradient Facility applies a 250 to 500 µl L-1 CA gradient to Blackland prairie plant communities established on lysimeters containing clay, silty clay, and sandy soils. The gradient is created as photosynthesis by vegetation enclosed in in temperature-controlled chambers progressively depletes carbon dioxide from air flowing directionally through the chambers. Maintaining proper air flow rate, adequate photosynthetic capacity, and temperature control are critical to overcome the main limitations of the system, which are declining photosynthetic rates and increased water stress during summer. The facility is an economical alternative to other techniques of CA enrichment, successfully discerns the shape of ecosystem responses to subambient to superambient CA enrichment, and can be adapted to test for interactions of carbon dioxide with other greenhouse gases such as methane or ozone.

Trait convergence and plasticity among native and invasive species in resource-poor environments.

PREMISE OF STUDY: Functional trait comparisons provide a framework with which to assess invasion and invasion resistance. However, recent studies have found evidence for both trait convergence and divergence among coexisting dominant native and invasive species. Few studies have assessed how multiple stresses constrain trait values and plasticity, and no study has included direct measurements of nutrient conservation traits, which are critical to plants growing in low-resource environments. METHODS: We evaluated how nutrient and water stresses affect growth and allocation, water potential and gas exchange, and nitrogen (N) allocation and use traits among a suite of six codominant species from the Intermountain West to determine trait values and plasticity. In the greenhouse, we grew our species under a full factorial combination of high and low N and water availability. We measured relative growth rate (RGR) and its components, total biomass, biomass allocation, midday water potential, photosynthetic rate, water-use efficiency (WUE), green leaf N, senesced leaf N, total N pools, N productivity, and photosynthetic N use efficiency. KEY RESULTS: Overall, soil water availability constrained plant responses to N availability and was the major driver of plant trait variation in our analysis. Drought decreased plant biomass and RGR, limited N conservation, and led to increased WUE. For most traits, native and nonnative species were similarly plastic. CONCLUSIONS: Our data suggest native and invasive biomass dominants may converge on functionally similar traits and demonstrate comparable ability to respond to changes in resource availability.