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Fritschi, F. B.

Publications and source records attributed to Fritschi, F. B..

At least 19 recordsLinked to original sources

Rapid adaptation and extinction across climates in synchronized outdoor evolution experiments of Arabidopsis thaliana

Climate change is threatening species with extinction, and rapid evolutionary adaptation may be their only option for population rescue over short ecological timescales. However, direct observations of rapid genetic adaptation and population dynamics across climates are rare across species. To fill this gap, we conducted a replicated, globally synchronized evolution experiment with the plant Arabidopsis thaliana for 5 years in over 30 outdoor experimental gardens with distinct climates across Europe, the Levant, and North America. We performed whole-genome sequencing on [~]70,000 surviving reproductive individuals and directly observed rapid and repeatable adaptation across climates. Allele frequency changes over time were parallel in experimental evolution replicates within the same climates, while they diverged across contrasting climates--with some allele frequency shifts best explained by strong selection between -46% to +60%. Screening the genome for signals of rapid climate adaptation identified a polygenic architecture with both known and novel adaptive genetic variants connected to important ecological phenotypes including environmental stress responses, CAM5 and HEAT SHOCK FACTORs, and germination and spring flowering timing, CYTOCHROME P450s and TSF. We found evolutionary adaptation trends were often predictable, but variable across environments. In warm climates, high evolutionary predictability was associated with population survival up to 5 years, while erratic trends were an early warning for population extinction. Together, these results show rapid climate adaptation may be possible, but understanding its limits across species will be key for biodiversity forecasting.

evolutionary biology↗

Enhanced cell aggregation in the Chlamydomonas reinhardtii rbo1 mutant in response to multifactorial stress combination

Global change factors associated with climate change and increased pollution are subjecting plants, microbes, and different ecosystems to conditions of multifactorial stress combination (MFSC). While recent studies centered on the effects of MFSC on different plants and ecosystems, much less is known about how these conditions impact unicellular organisms. Here, we report on the physiological and proteomic responses of wild type and respiratory burst oxidase homolog 1 (rbo1) mutant cells of Chlamydomonas reinhardtii to a MFSC of 5 different abiotic stresses. While several similarities were found between plant and C. reinhardtii responses to MFSC, our work revealed that MFSC induces aggregation in the unicellular organism C. reinhardtii. We further show that MFSC induced aggregation is enhanced in the rbo1 mutant and can be triggered by H2O2. As aggregation typically leads to reduced growth, respiration and/or photosynthesis, enhanced aggregation of unicellular organisms in different ecosystems subjected to MFSC could explain part of the negative impacts of MFSC on the services they provide. Our findings shed new light on the response of unicellular organisms to MFSC and suggest that one of the main drivers leading to multicellularity during evolution was early conditions of MFSC under an oxygenated environment.

plant biology↗

bHLH35 mediates specificity in plant responses to multiple stress conditions

How biological systems respond to stress is a fundamental question in biology, primarily addressed using the reductionist approach of applying one stress condition at a time. In nature, however, organisms experience a multitude of stresses, simultaneously or sequentially, questioning the validity of the reductionist approach for predicting plant responses to stress under natural conditions. Here, we reveal that in the flowering plant Arabidopsis thaliana, the transcriptional regulator bHLH35 is required for plant survival under a specific set of stress conditions that includes a combination of salinity, excess light, and heat, occurring simultaneously (but not for each of these stresses applied individually or in any other combination). Under these conditions, bHLH35 interacts with NAC069 and binds the promoter of LBD31, also specifically required for survival under the 3-stress combination. Our findings uncover a high degree of specificity in the response of organisms to stress, a specificity that would not have been revealed using the reductionist approach, and one that should be taken into consideration when developing agronomically important crops with heightened resilience to climate change.

plant biology↗

Transcriptomic and physiological responses of soybean plants subjected to a combination of water deficit and heat stress under field conditions

Water deficit, heat stress, and a combination of water deficit and heat stress are highly disruptive to crop yield worldwide. Unfortunately, the frequency and intensity of these conditions is gradually increasing due to climate change. Previous studies of water deficit and heat stress combination were primarily conducted under controlled growth conditions, revealing that the combination of water deficit and heat stress resulted in the activation of unique stress responses and acclimation pathways. However, whether similar responses to stress combination occur in the field remained largely unknown. Here we report on a two-year field study in which the transcriptomic and physiological responses of vegetative and reproductive tissues of soybean (Glycine max) to water deficit, heat treatment and their combination were studied. Our findings reveal that the transcriptomic responses of soybeans grown in the field are different from those grown under controlled growth chamber conditions. These differences were especially noticeable in plants subjected to the heat or water deficit treatments, and less in plants subjected to the stress combination. In addition, we report that differential transpiration between leaves and pods, that was originally discovered in plants grown under controlled growth conditions, occurs in field grown soybeans in response to heat stress, as well as heat stress combined with water deficit. We hope that the transcriptomic datasets generated by our study will contribute to future studies of crop responses to different stresses in the field, as well as highlight the need for more omics studies of plants grown under field conditions.

plant biology↗

Integrative analysis of plant responses to a combination of water deficit, heat stress and eCO2 reveals a role for OST1 and SLAH3 in regulating stomatal responses

The frequency, intensity and duration of global change factors and/or environmental stressors, such as droughts, heat waves, floods, and pollution, are increasing due to anthropogenic activities, subjecting plants to compound conditions of Global Change Factor combination (GCFc), or stress combination. These can have contrasting or additive effects on plant physiological performance and impact different ecosystems and agro-ecosystems worldwide. Using an integrative physiological, genetic, hormonal, and transcriptomic analysis, we studied the response of Arabidopsis thaliana (L.) Heynh to a combination of water deficit (WD), heat stress (HS) and/or elevated levels of CO2 (eCO2). Our findings reveal high specificity in plant responses to GCFc. We further reveal that stomatal aperture regulation under conditions of GCFc is controlled by a blend of unique and shared regulators, that together determine the specific aperture size under each different set of GCFc conditions. Under a combination of WD, HS, and eCO2 (WD+HS+eCO2), for example, stomatal closure required the function of nitric oxide, OPEN STOMATA 1 and the S-type anion channel SLAH3, but not the S-type anion channel SLAC1, or many other regulators typically found to control stomatal aperture under less complex conditions, including HS+WD. Our findings highlight the complexity of plant physiological and molecular responses to conditions of stress combination and open the way for future studies of plant responses to stress combination, crucial to our understanding of how GCFc impacts different ecosystems and agro-ecosystems worldwide. In addition, our study provides an initial definition for a stomatal hierarchical stress code that could apply to future studies.

plant biology↗

ERF transcription factor regulons underpin growth-defence trade-off under acute heat stress in rice seedlings

O_LIRice, a staple cereal crop, faces significant threats from rising temperatures, affecting all growth stages including early seedling establishment. Despite being critical in determining overall growth and productivity, response to heat stress during the early seedling stage remains understudied. This research aimed to assess the impact of acute heat stress on rice seedlings and unravel underlying molecular mechanisms. C_LIO_LIRice seedlings were exposed to varying intensities and durations of heat stress to determine a critical threshold affecting growth. To elucidate the transcription factor (TF)-mediated regulatory mechanisms and their functional interactome in response to stress, transcriptomic analysis of shoots and roots exposed to acute heat stress was performed. C_LIO_LITranscriptome analysis unveiled a comprehensive TF-target regulatory map for shoots and roots, potentially involved in the modulation of growth-defence trade-off in response to acute heat stress. Ethylene Responsive Factors (ERFs) emerged as central regulators, with phytohormones ethylene and jasmonic acid acting as upstream modulators. Pre-treatment with these phytohormones alleviated the adverse effects of heat stress. C_LIO_LIThis study uncovers key molecular mechanisms governing rice seedling responses to acute heat stress involving ERFs-hormonal interactions. Modulating these core regulators presents a promising strategy to enhance heat resilience, addressing global food security amid rising temperatures. C_LI

plant biology↗

Defining the limits of differential transpiration

Differential transpiration is a newly discovered acclimation strategy of annual plants to a combination of water deficit (WD) and heat stress (HS). Under these conditions (i.e., WD+HS), transpiration of vegetative tissues is suppressed in plants such as soybean and tomato, while transpiration of reproductive tissues is not (termed Differential Transpiration; DT). This newly discovered acclimation process enables the cooling of reproductive organs under conditions of WD+HS, limiting HS-induced damage to plant reproduction. However, at what temperature and WD extremes will this process be active and functional at reducing the internal temperature of reproductive tissues, and at what developmental stages of the plant is it activated, remain unknown. Here, we report that DT occurs at most nodes (leaf developmental stages) of soybean plants subjected to WD+HS, and that it can function under extreme conditions of WD+HS (i.e., 18% of field water capacity and 42{degrees}C combined). Our findings reveal that DT is an effective acclimation strategy that protects reproductive processes from extreme conditions of WD+HS, at almost all developmental stages. In addition, our findings suggest that under field conditions DT could also be active in plants subjected to low or mild levels of WD during a heat wave.

plant biology↗

Local adaptation of both plant and pathogen: an arms-race compromise in switchgrass rust

O_LIIn widespread species, parasites can locally adapt to host populations, or hosts can locally adapt to resist parasites. Parasites with rapid life cycles locally adapt more quickly, but host diversity, selective pressure, and climatic factors impact coevolution. C_LIO_LITo better understand local adaptation in co-evolved host-parasite systems, we examined switchgrass (Panicum virgatum), and its leaf rust pathogen (Puccinia novopanici) across a latitudinal range in North America. We grew diverse switchgrass genotypes in ten replicated common gardens spanning 16.78{degrees} latitude for three years, measuring rust severity from natural infection. We conducted genome wide association mapping to identify genetic loci associated with rust severity. C_LIO_LIGenetically differentiated rust populations were locally adapted to northern and southern switchgrass, despite host local adaptation in the same regions. Rust resistance was highly polygenic, and distinct loci were associated with rust severity in the north and south. We narrowed a previously identified large-effect QTL for rust severity to a candidate YSL3-like gene, and linked numerous other loci to immunity-related genes. C_LIO_LIBoth hosts and parasites can be locally adapted when parasites have a lower impact on fitness than other local selection pressures. In switchgrass, our results suggest variation in fungal resistance mechanisms between locally adapted regions. C_LI

evolutionary biology↗

Integrative phenotypic-transcriptomic analysis of soybean plants subjected to multifactorial stress combination

Global warming, climate change, and industrial pollution are altering our environment subjecting crops to an increasing number and complexity of abiotic stress conditions, concurrently or sequentially. Recent studies revealed that a combination of 3 or more stresses simultaneously impacting a plant (termed multifactorial stress combination; MFSC) can cause a drastic decline in plant growth and survival, even if the level of each stress involved in the MFSC has a negligible effect on plants. However, the impacts of MFSC on crops are largely unknown. We subjected soybean plants to a MFSC of up to five different stresses (water deficit, salinity, low phosphate, acidity, and cadmium), in an increasing level of complexity, and conducted integrative transcriptomic-phenotypic analysis of reproductive and vegetative tissues. We reveal that MFSC has a negative cumulative effect on soybean yield, that each set of MFSC condition elicits a unique transcriptomic response (that is different between flowers and leaves), and that selected genes expressed in leaves or flowers are linked to the effects of MFSC on different vegetative, physiological, and/or reproductive parameters. We further reveal that the transcriptomic response of soybean and Arabidopsis to MFSC shares common features associated with reactive oxygen and iron/copper signaling/metabolism. Our study provides unique phenotypic and transcriptomic datasets for dissecting the mechanistic effects of MFSC on the vegetative, physiological, and reproductive processes of a crop plant.

plant biology↗

The transcriptome of soybean reproductive tissues subjected to water deficit, heat stress, and a combination of water deficit and heat stress.

Global warming and climate change are driving an alarming increase in the frequency and intensity of extreme climate events, such as droughts, heat waves, and their combination, inflicting heavy losses to agricultural production. Recent studies revealed that the transcriptomic responses of different crops to water deficit (WD) or heat stress (HS) is very different from that to a combination of WD+HS. In addition, it was found that the effects of WD, HS, and WD+HS are significantly more devastating when these stresses occur during the reproductive growth phase of crops, compared to vegetative growth. As the molecular responses of different reproductive and vegetative tissues of plants to WD, HS, or WD+HS could be different from each other, and these differences could impact many current and future breeding and/or engineering attempts to enhance the resilience of crops to climate change, we conducted a transcriptomic analysis of different soybean (Glycine max) tissues to WD, HS, and WD+HS. Here we present a reference transcriptomic dataset that includes the response of soybean leaf, pod, anther, stigma, ovary, and sepal to WD, HS, and WD+HS conditions. Mining this data set for the expression pattern of different stress-response transcripts revealed that each tissue had a unique transcriptomic response to each of the different stress conditions. This finding is important as it suggests that attempting to enhance the overall resilience of crops to climate change could require a coordinated approach that simultaneously alters the expression of different groups of transcripts in different tissues in a stress-specific manner. SIGNIFICANCE STATEMENTA reference transcriptomic dataset of different reproductive tissues of soybean subjected to water deficit, heat stress, and their combination, generated by this study, reveals that different tissues display different responses to these stress conditions. Attempting to enhance the resilience of crops to different stress combinations, associated with climate change, might therefore require simultaneously altering the expression of different sets of transcripts in different tissues in a coordinated and stress-specific manner.

plant biology↗

The effects of multifactorial stress combination on rice and maize

The complexity of environmental factors affecting plants is gradually increasing due to global warming, an increase in the number and intensity of climate change-driven weather events, such as droughts, heat waves, and floods, and the accumulation of different pollutants. The impact of multiple stress conditions on plants was recently termed multifactorial stress combination (MFSC) and defined as the occurrence of three or more stressors that impact plants simultaneously or sequentially. We recently reported that with the increased number and complexity of different stressors, the growth and survival of Arabidopsis thaliana seedlings declines; even if the level of each individual stress is low enough to have no significant effect on plants. This finding is alarming since it reveals that MFSCs of different low-level stressors could impact crops and cause a dramatic reduction in overall growth. However, whether MFSC would impact commercial crop cultivars has not been studied. Here, we reveal that a MFSC of 5 different low level abiotic stresses (salinity, heat, the herbicide paraquat, phosphorus deficiency, and the heavy metal cadmium), applied in an increasing level of complexity, has a significant negative impact on the growth and biomass of a commercial rice (Oryza sativa) cultivar and a maize (Zea mays) hybrid. We further report on the first proteomics analysis of MFSC in plants that identified over 300 proteins common to all 4- and 5-MFSCs. Taken together our findings reveal that the impacts of MFSC on two different crop species are severe, and that MFSC may significantly affect agricultural productivity.

plant biology↗

Differential transpiration between pods and leaves during stress combination in soybean

Climate change is causing an increase in the frequency and intensity of droughts, heat waves, and their combinations, diminishing agricultural productivity and destabilizing societies worldwide. We recently reported that during a combination of water deficit (WD) and heat stress (HS) stomata on leaves of soybean plants are closed, while stomata on flowers are open. This unique stomatal response was accompanied by differential transpiration (higher in flowers, while lower in leaves) that cooled flowers during a combination of WD+HS. Here we reveal that developing pods of soybean plants subjected to a combination of WD+HS use a similar acclimation strategy of differential transpiration to reduce internal pod temperature by about 4{degrees}C. We further show that enhanced expression of transcripts involved in abscisic acid degradation accompanies this response, and that preventing pod transpiration by sealing stomata causes a significant increase in internal pod temperature. Using an RNA-Seq analysis of pods developing on plants subjected to WD+HS, we also show that the response of pods to WD, HS, or WD+HS is distinct from that of leaves or flowers. Interestingly, we report that although flower, pod and seed numbers per plant are decreased under conditions of WD+HS, seed mass of plants subjected to WD+HS is larger than that of plants subjected to HS, and number of seeds with suppressed/aborted development is lower in WD+HS compared to HS. Taken together our findings reveal that differential transpiration occurs in pods of soybean plants subjected to WD+HS and that this process limits heat-induced damage to seed production. One sentence summaryDifferential transpiration between pods and leaves of soybean plants subjected to a combination of water deficit and heat stress buffers internal pod temperature.

plant biology↗

Heritability and host genomic determinants of switchgrass root-associated microbiota in field sites spanning its natural range.

A fundamental goal in plant microbiome research is to determine the relative impacts of host and environmental effects on root microbiota composition, particularly how host genotype impacts bacterial community composition. Most studies characterizing the effect of plant genotype on root microbiota undersample host genetic diversity and grow plants outside of their native ranges, making the associations between host and microbes difficult to interpret. Here we characterized the root microbiota of a large population of switchgrass, a North American native C4 bioenergy crop, in three field locations spanning its native range. Our data, composed of >2000 samples, suggest field location is the primary determinant of microbiome composition; however, substantial heritable variation is widespread across bacterial taxa, especially those in the Sphingomonadaceae family. Despite diverse compositions, we find that relatively few highly prevalent bacterial taxa make up the majority of the switchgrass root microbiota, a large fraction of which is shared across sites. Local genotypes preferentially recruit / filter for local microbes, supporting the idea of affinity between local plants and their microbiota. Using genome-wide association, we identified loci impacting the abundance of >400 microbial strains and found an enrichment of genes involved in immune responses, signaling pathways, and secondary metabolism. We found loci associated with over half of the core microbiota (i.e. microbes in >80% of samples) regardless of field location. Finally, we show a genetic relationship between a basal plant immunity pathway and relative abundances of root microbiota. This study brings us closer to harnessing and manipulating beneficial microbial associations via host genetics.

plant biology↗

Physiological trait networks enhance understanding of crop growth and water use in contrasting environments

Plant function arises from a complex network of structural and physiological traits. Explicit representation of these traits, as well as their connections with other biophysical processes, is required to advance our understanding of plant-soil-climate interactions. We used the Terrestrial Regional Ecosystem Exchange Simulator (TREES) to evaluate physiological trait networks in maize. Net primary productivity (NPP) and grain yield were simulated across five contrasting climate scenarios. Simulations achieving high NPP and grain yield in high precipitation environments featured trait networks conferring high water use strategies: deep roots, high stomatal conductance at low water potential ("risky" stomatal regulation), high xylem hydraulic conductivity, and high maximal leaf area index. In contrast, high NPP and grain yield was achieved in dry environments with low late-season precipitation via water conserving trait networks: deep roots, high embolism resistance, and low stomatal conductance at low leaf water potential ("conservative" stomatal regulation). We suggest that our approach, which allows for the simultaneous evaluation of physiological traits and their interactions (i.e., networks), has potential to improve crop growth predictions in different environments. In contrast, evaluating single traits in isolation of other coordinated traits does not appear to be an effective strategy for predicting plant performance. Summary statementOur process-based model uncovered two beneficial but contrasting trait networks for maize which can be understood by their integrated effect on water use/conservation. Modification of multiple, physiologically aligned, traits were required to bring about meaningful improvements in NPP and yield.

plant biology↗

Differential regulation of flower transpiration during abiotic stress in plants

Heat waves, occurring during droughts, can have a devastating impact on yield, especially if they happen during the flowering and seed set stages of the crop cycle. Global warming and climate change are driving an alarming increase in the frequency and intensity of combined drought and heat stress episodes, critically threatening global food security. Previous studies revealed that during a combination of drought and heat stress stomata on leaves of many plants are closed, preventing cooling by transpiration. Because high temperature is detrimental to reproductive processes, essential for plant yield, we measured the inner temperature, transpiration, and sepal stomatal aperture of closed soybean flowers, developing on plants subjected to a combination of drought and heat stress. Here, we report that during a combination of drought and heat stress soybean plants prioritize transpiration through flowers over transpiration through leaves by opening their flower stomata, while keeping their leaf stomata closed. This acclimation strategy, termed differential transpiration, lowers flower inner temperature by about 2-3{degrees}C, protecting reproductive processes at the expense of vegetative tissues. Manipulating stomatal regulation, stomatal size and/or stomatal density of flowers could therefore serve as a viable strategy to enhance the yield of different crops and mitigate some of the current and future impacts of global warming and climate change on agriculture. One sentence summaryDuring stress conditions that result in higher flower inner temperature plants use a differential transpiration strategy to protect reproductive processes at the expense of vegetative tissues.

plant biology↗

Mapping of genotype-by-environment interactions in phenology identifies two cues for flowering in switchgrass (Panicum virgatum)

The timing of vegetative and reproductive growth in plants ("phenological timings") depend on genetic effects (G), environmental (e.g., weather) cues, and their interaction. Here, we measure phenological timings in two highly divergent switchgrass (Panicum virgatum) subpopulations using repeated plantings of cloned individuals at eight sites across the central United States. The timing of vegetative growth for the two subpopulations reversed between their two natural ranges and had strong negative correlations between these regions; in contrast, the timing of flowering was positively correlated between gardens. We expect that these phenotypic correlations consist of polygenic effects on phenology which have distinct patterns of GxE segregating at different mapped loci. Thus, we infer the mixture of ways genetic effects impact phenological timings, such as across common gardens (GxE) or with weather cues (GxWeather). We demonstrate that we can identify genetic variation with GxWeather and assign genetic loci to specific weather-based cues or other patterns. For example, in the Gulf subpopulation, 65% of genetic effects on the timing of vegetative growth covary with daylength 14 days prior to green-up date, and 33% of genetic effects on the timing of flowering covary with cumulative rainfall in the week prior to flowering. However, most variation in genetic effects cannot be attributed to variation in weather variables. Selective breeding for particular alleles at GxWeather loci could alter flowering responsiveness in a photoperiod or rainfall-specific way. More broadly, our approach refines the characterization of genotype-by-environment interactions and can be implemented in any species phenotyped in multiple environments.

genetics↗

Host genetic control of succession in the switchgrass leaf fungal microbiome

Leaf fungal microbiomes can be fundamental drivers of host plant success, as they contain pathogens that devastate crop plants and taxa that enhance nutrient uptake, discourage herbivory, and antagonize pathogens. We measured leaf fungal diversity with amplicon sequencing across an entire growing season in a diversity panel of switchgrass (Panicum virgatum). We also sampled a replicated subset of genotypes across three additional sites to compare the importance of time, space, ecology, and genetics. We found a strong successional pattern in the microbiome shaped both by host genetics and environmental factors. Further, we used genome-wide association mapping and RNA-sequencing to show that three cysteine-rich receptor-like kinases were linked to a genetic locus associated with microbiome structure. These genes were more highly expressed in genotypes susceptible to fungal pathogens, which were central to microbial covariance networks, suggesting that host immune genes are a principal means of controlling the entire leaf microbiome.

ecology↗

The impact of multifactorial stress combination on plant growth and survival

O_LIClimate change-driven extreme weather events, combined with increasing temperatures, harsh soil conditions, low water availability and quality, and the introduction of many man-made pollutants, pose a unique challenge to plants. Although our knowledge of the response of plants to each of these individual conditions is vast, we know very little about how a combination of many of these factors, occurring simultaneously, i.e., multifactorial stress combination, impacts plants. C_LIO_LISeedlings of wild type and different mutants of Arabidopsis thaliana plants were subjected to a multifactorial stress combination of six different stresses, each applied at a low level, and their survival, physiological and molecular responses determined. C_LIO_LIOur findings reveal that while each of the different stresses, applied individually, had a negligible effect on plant growth and survival, the accumulated impact of multifactorial stress combination on plants was detrimental. We further show that the response of plants to multifactorial stress combination is unique and that specific pathways and processes play a critical role in the acclimation of plants to multifactorial stress combination. C_LIO_LITaken together our findings reveal that further polluting our environment could result in higher complexities of multifactorial stress combinations that in turn could drive a critical decline in plant growth and survival. C_LI Plain Language SummaryThe effects of multiple stress conditions occurring simultaneously, i.e., multifactorial stress combination, on plants is currently unknown. Here we show that different co-occurring stresses can interact to negatively impact plant growth and survival, even if the effect of each individual stress is negligible. We further identify several key pathways essential for plant acclimation to multifactorial stress combination.

plant biology↗