02601nas a2200265 4500008004100000245007800041210006900119300001600188490000800204520179500212100002002007700001702027700003002044700002102074700002702095700002002122700002102142700001402163700002102177700002302198700001802221700001402239700002302253856005902276 2020 eng d00aResolving the Dust Bowl paradox of grassland responses to extreme drought0 aResolving the Dust Bowl paradox of grassland responses to extrem a22249-222550 v1173 a

During the 1930s Dust Bowl drought in the central United States, species with the C3 photosynthetic pathway expanded throughout C4-dominated grasslands. This widespread increase in C3 grasses during a decade of low rainfall and high temperatures is inconsistent with well-known traits of C3 vs. C4 pathways. Indeed, water use efficiency is generally lower, and photosynthesis is more sensitive to high temperatures in C3 than C4 species, consistent with the predominant distribution of C3 grasslands in cooler environments and at higher latitudes globally. We experimentally imposed extreme drought for 4 y in mixed C3/C4 grasslands in Kansas and Wyoming and, similar to Dust Bowl observations, also documented three- to fivefold increases in C3/C4 biomass ratios. To explain these paradoxical responses, we first analyzed long-term climate records to show that under nominal conditions in the central United States, C4 grasses dominate where precipitation and air temperature are strongly related (warmest months are wettest months). In contrast, C3 grasses flourish where precipitation inputs are less strongly coupled to warm temperatures. We then show that during extreme drought years, precipitation–temperature relationships weaken, and the proportion of precipitation falling during cooler months increases. This shift in precipitation seasonality provides a mechanism for C3 grasses to respond positively to multiyear drought, resolving the Dust Bowl paradox. Grasslands are globally important biomes and increasingly vulnerable to direct effects of climate extremes. Our findings highlight how extreme drought can indirectly alter precipitation seasonality and shift ecosystem phenology, affecting function in ways not predictable from key traits of C3 and C4 species.

1 aKnapp, Alan, K.1 aChen, Anping1 aGriffin-Nolan, Robert, J.1 aBaur, Lauren, E.1 aCarroll, Charles, J.W.1 aGray, Jesse, E.1 aHoffman, Ava, M.1 aLi, Xiran1 aPost, Alison, K.1 aSlette, Ingrid, J.1 aCollins, S, L1 aLuo, Yiqi1 aSmith, Melinda, D. uhttp://www.pnas.org/lookup/doi/10.1073/pnas.192203011703509nas a2200313 4500008004100000245008500041210006900126300001600195490000800211520253200219653000902751653001902760653003002779653001202809653002502821653002802846100003002874700002102904700002402925700002402949700002102973700002302994700002403017700001603041700002503057700002003082700001703102856007603119 2019 eng d00aShifts in plant functional composition following long-term drought in grasslands0 aShifts in plant functional composition following longterm drough a2133 - 21480 v1073 a

 1. Plant traits can provide unique insights into plant performance at the community scale. Functional composition, defined by both functional diversity and community-weighted trait means (CWMs), can affect the stability of above‐ground net primary production (ANPP) in response to climate extremes. Further complexity arises, however, when functional composition itself responds to environmental change. The duration of climate extremes, such as drought, is expected to increase with rising global temperatures; thus, understanding the impacts of long-term drought on functional composition and the corresponding effect that has on ecosystem function could improve predictions of ecosystem sensitivity to climate change.
 2. We experimentally reduced growing season precipitation by 66% across six temperate grasslands for 4 years and measured changes in three indices of functional diversity (functional dispersion, richness and evenness), community-weighted trait means and phylogenetic diversity (PD). Specific leaf area (SLA), leaf nitrogen content (LNC) and (at most sites) leaf turgor loss point (πTLP) were measured for species cumulatively representing ~90% plant cover at each site.
 3. Long-term drought led to increased community functional dispersion in three sites, with negligible effects on the remaining sites. Species re-ordering following the mortality/senescence of dominant species was the main driver of increased functional dispersion. The response of functional diversity was not consistently matched by changes in phylogenetic diversity. Community-level drought strategies (assessed as CWMs) largely shifted from drought tolerance to drought avoidance and/or escape strategies, as evidenced by higher community-weighted πTLP, SLA and LNC. Lastly, ecosystem drought sensitivity (i.e. relative reduction in ANPP in drought plots) was positively correlated with community-weighted SLA and negatively correlated with functional diversity.
 4. Synthesis. Increased functional diversity following long-term drought may stabilize ecosystem functioning in response to future drought. However, shifts in community-scale drought strategies may increase ecosystem drought sensitivity, depending on the nature and timing of drought. Thus, our results highlight the importance of considering both functional diversity and abundance‐weighted traits means of plant communities as their collective effect may either stabilize or enhance ecosystem sensitivity to drought.

10aANPP10aClimate change10acommunity weighted traits10aDrought10aFunctional diversity10aplant functional traits1 aGriffin-Nolan, Robert, J.1 aBlumenthal, D.M.1 aCollins, Scott., L.1 aFarkas, Timothy, E.1 aHoffman, Ava, M.1 aMueller, Kevin, E.1 aOcheltree, Troy, W.1 aSmith, M.D.1 aWhitney, Kenneth, D.1 aKnapp, Alan, K.1 aJones, Holly uhttps://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2745.1325202255nas a2200145 4500008004100000245011300041210006900154300001000223520176500233100002101998700001702019700002002036700001602056856003702072 2018 eng d00aCodominant grasses differ in gene expression under experimental climate extremes in native tallgrass prairie0 aCodominant grasses differ in gene expression under experimental  ae43943 a

Extremes in climate, such as heat waves and drought, are expected to become more frequent and intense with forecasted climate change. Plant species will almost certainly differ in their responses to these stressors. We experimentally imposed a heat wave and drought in the tallgrass prairie ecosystem near Manhattan, Kansas, USA to assess transcriptional responses of two ecologically important C4 grass species, Andropogon gerardii and Sorghastrum nutans. Based on previous research, we expected that S. nutans would regulate more genes, particularly those related to stress response, under high heat and drought. Across all treatments, S. nutans showed greater expression of negative regulatory and catabolism genes while A. gerardii upregulated cellular and protein metabolism. As predicted, S. nutans showed greater sensitivity to water stress, particularly with downregulation of non-coding RNAs and upregulation of water stress and catabolism genes. A. gerardii was less sensitive to drought, although A. gerardii tended to respond with upregulation in response to drought versus S. nutans which downregulated more genes under drier conditions. Surprisingly, A. gerardii only showed minimal gene expression response to increased temperature, while S. nutans showed no response. Gene functional annotation suggested that these two species may respond to stress via different mechanisms. Specifically, A. gerardii tends to maintain molecular function while S. nutans prioritizes avoidance. Sorghastrum nutans may strategize abscisic acid response and catabolism to respond rapidly to stress. These results have important implications for success of these two important grass species under a more variable and extreme climate forecast for the future.

1 aHoffman, Ava, M.1 aAvolio, M.L.1 aKnapp, Alan, K.1 aSmith, M.D. uhttps://peerj.com/articles/4394/02043nas a2200133 4500008004100000245007200041210006900113300001200182490000700194520160200201100002101803700001601824856006901840 2018 eng d00aGene expression differs in codominant prairie grasses under drought0 aGene expression differs in codominant prairie grasses under drou a334-3460 v183 a

Grasslands of the Central US are expected to experience severe droughts and other climate extremes in the future, yet we know little about how these grasses will respond in terms of gene expression. We compared gene expression in Andropogon gerardii and Sorghastrum nutans, two closely related co-dominant C4 grasses responsible for the majority of ecosystem function, using RNA-seq. We compared Trinity assemblies within each species to determine annotated functions of transcripts responding to drought. Subsequently, we compared homologous annotated gene-groups across the two species using cross-species meta-level analysis and functional clustering based on key terms. The majority of variation was found between species, as opposed to between drought and watered treatments. However, there is evidence for differential responses; Andropogon allocated gene expression differently compared to Sorghastrum, suggesting Andropogon focuses on stress alleviation (such as oxygen radical scavenging) rather than prevention. In contrast, Sorghastrum may employ a drought avoidance strategy by modulating osmotic response, especially with hormonal regulation. We found Sorghastrum tended to be more sensitive within 10 key gene-groups related to stress, abscisic acid, and trichomes, suggesting gene expression may mechanistically parallel sensitivity at the physiological level. Our findings corroborate phenotypic and physiological differences in the field, and may help explain the phenotypic mechanisms of these two species in the tallgrass prairie community under future drought scenarios.

1 aHoffman, Ava, M.1 aSmith, M.D. uhttps://onlinelibrary.wiley.com/doi/full/10.1111/1755-0998.1273302291nas a2200145 4500008004100000245011600041210006900157300001100226490000800237520179100245100001702036700002102053700001602074856005502090 2018 eng d00aLinking gene regulation, physiology, and plant biomass allocation in Andropogon gerardii in response to drought0 aLinking gene regulation physiology and plant biomass allocation  a1 - 150 v2193 a

Plant responses to drought are often initiated at the molecular level and cascade upwards to affect physiology and growth. How plants respond to and recover from drought have consequences for their growth and survival in drier climates predicted with climate change. We studied four ecologically relevant genotypes of a common C4 grass, Andropogon gerardii. These genotypes had differential responses to a decade of more variable precipitation patterns in a field experiment in native tallgrass prairie. Here, we conducted a greenhouse experiment examining how these genotypes responded to repeated 10-day drought-recovery cycles when experiencing either a severe or moderate drought. We did this twice over the course of the experiment, early, after 5 weeks, and late, after 9 weeks of drought. We studied nine genes involved in water stress signaling and drought response in leaf tissue using real-time reverse-transcriptase polymerase chain reaction (qRT-PCR). We also measured photosynthesis, stomatal conductance, and biomass accumulation and allocation. In early drought, we found consistent differences among genotypes in gene expression, leaf-level physiology, and biomass accumulation and allocation. We found genes involved in ABA, proline synthesis, and mitigating oxidative stress were differentially expressed between genotypes, while genes that coded for aquaporins and chaperones were not. In late drought, we found fewer overall differences, and little regulation of drought responsive genes. Ultimately, we found genotypes either had greater phenotypic plasticity, suggesting an ability to avoid drought and maximize water resources when they were present, or genotypes were better at tolerating drought.

1 aAvolio, M.L.1 aHoffman, Ava, M.1 aSmith, M.D. uhttp://link.springer.com/10.1007/s11258-017-0773-303181nas a2200289 4500008004100000245012300041210006900164300001600233490000700249520223100256100003002487700002202517700002802539700002002567700001802587700002102605700002102626700002102647700002302668700002002691700002102711700002402732700002202756700002002778700001702798856007602815 2018 eng d00aTrait selection and community weighting are key to understanding ecosystem responses to changing precipitation regimes0 aTrait selection and community weighting are key to understanding a1746 - 17560 v323 a

1. Plant traits can be used to predict ecosystem responses to environmental change using a response–effect trait framework. To do this, appropriate traits must be identified that explain a species' influence on ecosystem function (“effect traits”) and the response of those species to environmental change (“response traits”). Response traits are often identified and measured along gradients in plant resources, such as water availability; however, precipitation explains very little variation in most plant traits globally. Given the strong relationship between plant traits and ecosystem functions, such as net primary productivity (NPP), and between NPP and precipitation, the lack of correlation between precipitation and plant traits is surprising.

2. We address this issue through a systematic review of >500 published studies that describe plant trait responses to altered water availability. The overarching goal of this review was to identify potential causes for the weak relationship between commonly measured plant traits and water availability so that we may identify more appropriate “response traits.”

3. We attribute weak trait–precipitation relationships to an improper selection of traits (e.g., nonhydraulic traits) and a lack of trait‐based approaches that adjust for trait variation within communities (only 4% of studies measure community‐weighted traits). We then highlight the mechanistic value of hydraulic traits as more appropriate “response traits” with regard to precipitation, which should be included in future community‐scale trait surveys.

4. Trait‐based ecology has the potential to improve predictions of ecosystem responses to predicted changes in precipitation; however, this predictive power depends heavily on the identification of reliable response and effect traits. To this end, trait surveys could be improved by a selection of traits that reflect physiological functions directly related to water availability with traits weighted by species relative abundance.

1 aGriffin-Nolan, Robert, J.1 aBushey, Julie, A.1 aCarroll, Charles, J. W.1 aChallis, Anthea1 aChieppa, Jeff1 aGarbowski, Magda1 aHoffman, Ava, M.1 aPost, Alison, K.1 aSlette, Ingrid, J.1 aSpitzer, Daniel1 aZambonini, Dario1 aOcheltree, Troy, W.1 aTissue, David, T.1 aKnapp, Alan, K.1 aFox, Charles uhttps://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2435.13135