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DOE OSTI2021

Synergies and Entanglement in Secondary Cell Wall Development and Abiotic Stress Response in Trees

A major challenge for sustainable food, fuel, and fiber production is simultaneous genetic improvement of yield, biomass quality, and resilience to episodic environmental stress and climate change. For Populus and other forest trees, quality traits involve alterations in the secondary cell wall (SCW) of wood for traditional uses, as well as for a growing diversity of biofuels and bioproducts. Alterations in wood properties that are desirable for specific end uses can have negative effects on growth and stress tolerance. Understanding of the diverse roles of SCW genes is necessary for the genetic improvement of fast-growing, short-rotation trees that face perennial challenges in their growth and development. Here, we review recent progress into the synergies and antagonisms of SCW development and abiotic stress responses, particularly, the roles of transcription factors, SCW biogenesis genes, and paralog evolution.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2025

Roles for epigenetics in wood formation and stress response intrees–from basic biology to forest management

Annual model and crop species have been the subject of most epigenetic studies for plants. In contrast to annuals, forest trees persist on natural landscapes and experience environmental variation within and across seasons, years, and decades or even centuries. Most forest trees species are undomesticated and typically grown on variable landscapes with no irrigation or application of agricultural chemicals. Forest trees must thus rely on their inherent ability to alter growth and physiology to mitigate the effects of changing abiotic and biotic stressors. Like other plants, trees have mechanisms encoded in their genomic DNA sequence that can respond directly to stress events such as drought or heat. Hypothetically, it would be highly advantageous to join these mechanisms with a dynamic “memory” of past exposure to stress. It is now well established that annual model and crop plants can establish epigenetic-based memory of stress events that support more rapid and robust response to stress in the future. Here, evidence is discussed for epigenetic regulation and “memory” in two fundamental biological processes in trees, wood formation and abiotic stress response. Wood formation is an ideal trait for epigenetic research in trees, as wood formation is highly responsive to environmental conditions and includes multiple rapid developmental changes as cells adopt distinct fates within complex tissues. This is followed by a discussion of research needs that would provide the foundation for new epigenetic applications for forestry.

Groover, Andrew↗

DOE OSTI2026

OxyR regulates the oxidative stress response in Zymomonas mobilis during oxic growth and anoxic biofuel fermentation

The bacterium Zymomonas mobilis is widely studied for its potential as an industrial biofuel producer. Anoxic fermentation by Z. mobilis in lignocellulosic hydrolysate can generate bioethanol from renewable plant biomass. In this study, we deleted a gene from the Z. mobilis genome encoding a homolog of OxyR, a transcription factor that activates an oxidative stress response in bacteria to reduce reactive oxygen species (ROS). Deletion of this transcription factor inhibited growth of Z. mobilis in oxic, but not anoxic, conditions in laboratory media. A ROS probe revealed that the oxyR response is required to reduce intracellular ROS during oxic growth. Importantly for biofuel production, the absence of oxyR inhibited growth and delayed ethanol production during anoxic hydrolysate fermentation. To determine the source of oxidative stress in hydrolysates, we grew ΔoxyR in a synthetic hydrolysate containing known inhibitors found in hydrolysates. There was no growth defect in ΔoxyR in the synthetic hydrolysate, indicating that known inhibitory compounds are not the source of anoxic oxidative stress. We determined that ammonia-fiber expansion switchgrass hydrolysate contains significant peroxide concentrations. Addition of catalase to hydrolysate improves growth of both ΔoxyR and wild-type Z. mobilis in hydrolysate. This study uncovers an important source of stress to Z. mobilis during biofuel fermentation.

OxyR↗

DOE OSTI2026

OxyR regulates the oxidative stress response in Zymomonas mobilis during oxic growth and anoxic biofuel fermentation

bioenergy↗

DOE OSTI2020

Pharmacological inhibition of PRMT7 links arginine monomethylation to the cellular stress response

Protein arginine methyltransferases (PRMTs) regulate diverse biological processes and are increasingly being recognized for their potential as drug targets. Here we report the discovery of a potent, selective, and cell-active chemical probe for PRMT7. SGC3027 is a cell permeable prodrug, which in cells is converted to SGC8158, a potent, SAM-competitive PRMT7 inhibitor. Inhibition or knockout of cellular PRMT7 results in drastically reduced levels of arginine monomethylated HSP70 family stress-associated proteins. Structural and biochemical analyses reveal that PRMT7-driven in vitro methylation of HSP70 at R469 requires an ATP-bound, open conformation of HSP70. In cells, SGC3027 inhibits methylation of both constitutive and inducible forms of HSP70, and leads to decreased tolerance for perturbations of proteostasis including heat shock and proteasome inhibitors. These results demonstrate a role for PRMT7 and arginine methylation in stress response.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2025

Engineered Methylobacterium extorquens grows well on methoxylated aromatics due to its formaldehyde metabolism and stress response

ABSTRACT Lignin is a vast yet underutilized source of renewable energy. The microbial valorization of lignin is challenging due to the toxicity of its degradation intermediates, particularly formaldehyde. In this study, we engineeredMethylobacterium extorquensPA1 to metabolize lignin-derived methoxylated aromatics, vanillate (VA) and protocatechuate (PCA), by introducing thevanandpcagene clusters. Compared toPseudomonas putida,M. extorquensPA1 exhibited better formaldehyde detoxification, enabling robust growth on VA without accumulation of formaldehyde. Genetic analyses confirmed that formaldehyde oxidation and stress response systems, rather than C 1 assimilation, were important for VA metabolism. Additionally, VA and PCA were found to disrupt membrane potential, contributing to their inherent toxicity. Our findings establishM. extorquensPA1 as a promising chassis for lignin valorization and provide a framework for engineering formaldehyde-resistant microbial platforms. IMPORTANCE In developing biotechnological solutions for a circular economy, it is critical to valorize all parts of renewable resources, such as lignocellulose from vegetative components of agricultural crops and from bioenergy feedstocks. After chemical breakdown, the aromatics arising from lignin present significant challenges for use due to their toxicity. Here, we address one component of this challenge—the methoxy groups that get released as formaldehyde—and show that existing biotechnological platform organisms with strong formaldehyde metabolism, such asMethylobacterium extorquens, can be transformed into highly capable utilizers of methoxylated aromatics.

Microbiology↗

DOE OSTI2025

Climate history modulates stress responses of common soil bacteria under experimental drought

Soil drying challenges microbial viability and survival, with bacteria employing various mechanisms to respond to shifts in osmolarity, including dormancy or metabolic upregulation of osmoprotectants. However, the extent to which these responses are shaped by an organism's phylogeny, or the climate history of a given environment is poorly understood. This study examines the responses of phylogenetically similar bacteria from semi-arid and humid tropical forest soils to osmotic and matric stress using synchrotron radiation-based Fourier Transform Infrared spectromicroscopy. This non-destructive approach depicts the biochemical phenotype for whole cells under control and stress conditions. We observed that, under osmotic stress, bacteria upregulated cell-signaling pathways, rapidly turned over lipid-storage compounds, and increased osmolyte production. In contrast, matric stress induced a more muted response, typically elevating the production of carbohydrate stress compounds, such as glycine betaine and trehalose. Whereas phylogenetically similar bacteria showed comparable biochemistry under control conditions, climate history played an important role in regulating responses to stress, whereby a stronger metabolic response was observed from semi-arid relative to tropical forest isolates. We conclude that bacterial stress response to drought can be more diverse than previously observed and regulated by both phylogeny and climate history.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2026

Pixel-Registered Multimodal Synchrotron XRF and FTIR Microscopies Reveal Salinity Stress Response Mechanisms in Pistachio

Background: Salinity is a major abiotic stress that negatively affects nearly all plant species at all stages of growth. Drought and poor-quality irrigation cause high soil salinity and salt accumulation via evaporation, reducing crop productivity. Despite its critical importance, the spatial localization of salt ions and associated biochemical changes within plants experiencing high salinity remains largely unknown. In this study, we developed a multimodal imaging pipeline to understand the impact of salinity on the pistachio rootstock UCB-1 (Pistacia atlantica x Pistacia integerrima). We directly link biochemical fingerprints in stem tissue architecture with salt ion localization to provide insights into the strategies pistachio uses to tolerate salinity. Results: We observed that Pistacia spp. exposed to high salt conditions accumulated Ca, Si, Cl, Al and Mg as hotspots within the pith, compared to the control (of which only Ca and Al co-locate). In contrast, there was a decrease in K between the control and salinity treatment. Hotspots of amide I and II were present in the cortex and pith of the salinity treated sample. Additionally, the salinity treatment resulted in an increased abundance of pectin and carbohydrates within the pith compared to the control, and the abundance of esters/carboxylic acid was greater in the salinity treatment. Conclusions: We determined that Cl and K, S and P, and biochemical components polysaccharide and pectin, esters and carboxylic acid, amide I and cellulose are the strongest drivers of salinity- treatment induced variability. In the cortex and phloem/xylem, a negative K-Ca correlation decreases in the salinity treatment. Several hotspots of elements and amide I (proteins) appear under salinity treatment, particularly in the cortex, suggesting an increase in the production of stress-related proteins (in response to high Cl) and/or structural proteins (i.e. Ca). Together, these results indicate that pistachio responds to salinity through ion compartmentalization coupled with a targeted biochemical adjustment, rather than a broadscale tissue-wide response. Overall, these novel, spatially resolved pixel-registered multimodal imaging data provide an enabling platform to understand the mechanisms of salinity tolerance in Pistacia spp and can be broadly applied to studying stress-related phenotype response in various plant tissues.

FTIR spectromicroscopy↗

DOE OSTI2026

A tissue‐resolved, network‐based transcriptomic framework for abiotic stress responses in sorghum

Developing climate‐resilient crops requires a detailed understanding of stress‐induced gene expression dynamics, as maladaptive responses can compromise their productivity and survival. Sorghum, a globally important cereal with exceptional tolerance to multiple abiotic stresses, provides a powerful system for investigating these dynamics. However, how stress type, tissue specificity, and temporal progression jointly shape transcriptomic responses in crops remains poorly understood. Here, we present a comparative, time‐resolved transcriptomic atlas of sorghum responses to drought, heat, and salinity stress across shoot and root tissues. Integrative analyses revealed that tissue specificity is the dominant determinant of abiotic stress‐induced gene reprogramming across all three stresses. Building on these global comparisons, we focused on heat stress, as it elicited the most coherent and pronounced transcriptional and regulatory responses, enabling deeper network‐level interrogation. Co‐expression network analysis identified tissue‐specific modules enriched for phytohormone‐responsive genes, while gene regulatory network (GRN) mapping and cistrome analyses uncovered transcription factors (TFs) controlling key hub genes within these modules. Together, this study provides a foundational transcriptomic and network‐based resource for dissecting the regulatory architecture of abiotic stress responses in sorghum and offers prioritized candidates for future functional validation and engineering of climate‐resilient crops.

abiotic stress↗

DOE OSTI2023

SPOTTED-LEAF7 targets the gene encoding β-galactosidase9, which functions in rice growth and stress responses

Abstract β-Galactosidases (Bgals) remove terminal β-D-galactosyl residues from the nonreducing ends of β-D-galactosidases and oligosaccharides. Bgals are present in bacteria, fungi, animals, and plants and have various functions. Despite the many studies on the evolution of BGALs in plants, their functions remain obscure. Here, we identified rice (Oryza sativa) β-galactosidase9 (OsBGAL9) as a direct target of the heat stress-induced transcription factor SPOTTED-LEAF7 (OsSPL7), as demonstrated by protoplast transactivation analysis and yeast 1-hybrid and electrophoretic mobility shift assays. Knockout plants for OsBGAL9 (Osbgal9) showed short stature and growth retardation. Histochemical β-glucuronidase (GUS) analysis of transgenic lines harboring an OsBGAL9pro:GUS reporter construct revealed that OsBGAL9 is mainly expressed in internodes at the mature stage. OsBGAL9 expression was barely detectable in seedlings under normal conditions but increased in response to biotic and abiotic stresses. Ectopic expression of OsBGAL9 enhanced resistance to the rice pathogens Magnaporthe oryzae and Xanthomonas oryzae pv. oryzae, as well as tolerance to cold and heat stress, while Osbgal9 mutant plants showed the opposite phenotypes. OsBGAL9 localized to the cell wall, suggesting that OsBGAL9 and its plant putative orthologs likely evolved functions distinct from those of its closely related animal enzymes. Enzyme activity assays and analysis of the cell wall composition of OsBGAL9 overexpression and mutant plants indicated that OsBGAL9 has activity toward galactose residues of arabinogalactan proteins (AGPs). Our study clearly demonstrates a role for a member of the BGAL family in AGP processing during plant development and stress responses.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2024

Quantitative trait locus (QTL) mapping and transcriptome profiling identify QTLs and candidate genes associated with heat stress response during reproductive development in Camelina sativa

Camelina sativa (L.) Crantz is a low-input oilseed crop that has great potential in providing sustainable feedstock for biofuels and bioproducts. Climate change is threatening production of camelina with rising global temperatures. Elucidating the genetic response to high temperatures is essential for successful breeding of heat-tolerant camelina varieties. Here, we report a combinatorial approach to identifying candidate genes associated with heat stress by quantitative trait locus (QTL) mapping and comparative transcriptome profiling. A population of recombinant inbred lines (RILs) was grown in a controlled growth chamber under the high-temperature regimes for 14 days beginning at the onset of the reproductive stage. Several traits related to seed production were evaluated at maturity. The QTL analysis identified several regions with co-located traits on chromosomes 8, 10, and 12. Two RILs with contrasting phenotypic responses to heat stress were chosen for gene expression profiling via RNA sequencing. Multiple pathways and genes were found to be strongly affected by heat stress, and many genes expressed differently between the two RILs. Several genes identified within the QTL regions were considered strong candidates that may control heat tolerance during reproduction in camelina. These studies provide resources for future studies that may assist in improving the heat tolerance of camelina.

60 APPLIED LIFE SCIENCES↗

DOE OSTI2023

A transcriptomic atlas of acute stress response to low pH in multiple Issatchenkia orientalis strains

Because of its natural stress tolerance to low pH, Issatchenkia orientalis (a.k.a. Pichia kudriavzevii) is a promising non-model yeast for bio-based production of organic acids. Yet, this organism is relatively unstudied, and specific mechanisms of its tolerance to low pH are poorly understood, limiting commercial use. In this study, we selected 12 I. orientalis strains with varying acid stress tolerance (six tolerant and six susceptible) and profiled their transcriptomes in different pH conditions to study potential mechanisms of pH tolerance in this species. We identified hundreds of genes whose expression response is shared by tolerant strains but not by susceptible strains, or vice versa, as well as genes whose responses are reversed between tolerant and susceptible strains. We mapped regulatory mechanisms of transcriptomic responses via motif analysis as well as differential network reconstruction, identifying several transcription factors, including Stb5, Mac1, and Rtg1/Rtg3, some of which are known for their roles in acid response in Saccharomyces cerevisiae. Functional genomics analysis of short-listed genes and transcription factors suggested significant roles for energy metabolism and translation-related processes, as well as the cell wall integrity pathway and RTG-dependent retrograde signaling pathway. Finally, we conducted additional experiments for two organic acids, 3-hydroxypropionate and citramalate, to eliminate acid-specific effects and found potential roles for glycolysis and trehalose biosynthesis specifically for response to low pH. In summary, our approach of comparative transcriptomics and phenotypic contrasting, along with a multi-pronged bioinformatics analysis, suggests specific mechanisms of tolerance to low pH in I. orientalis that merit further validation through experimental perturbation and engineering.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2023

Data for A Transcriptomic Atlas of Acute Stress Response to Low pH in Multiple Issatchenkia orientalis Strains

Because of its natural stress tolerance to low pH, Issatchenkia orientalis (a.k.a. Pichia kudriavzevii ) is a promising non-model yeast for bio-based production of organic acids. Yet, this organism is relatively unstudied, and specific mechanisms of its tolerance to low pH are poorly understood, limiting commercial use. In this study, we selected 12 I. orientalis strains with varying acid stress tolerance (six tolerant and six susceptible) and profiled their transcriptomes in different pH conditions to study potential mechanisms of pH tolerance in this species. We identified hundreds of genes whose expression response is shared by tolerant strains but not by susceptible strains, or vice versa, as well as genes whose responses are reversed between tolerant and susceptible strains. We mapped regulatory mechanisms of transcriptomic responses via motif analysis as well as differential network reconstruction, identifying several transcription factors, including Stb5, Mac1, and Rtg1/Rtg3, some of which are known for their roles in acid response in Saccharomyces cerevisiae . Functional genomics analysis of short-listed genes and transcription factors suggested significant roles for energy metabolism and translation-related processes, as well as the cell wall integrity pathway and RTG-dependent retrograde signaling pathway. Finally, we conducted additional experiments for two organic acids, 3-hydroxypropionate and citramalate, to eliminate acid-specific effects and found potential roles for glycolysis and trehalose biosynthesis specifically for response to low pH. In summary, our approach of comparative transcriptomics and phenotypic contrasting, along with a multi-pronged bioinformatics analysis, suggests specific mechanisms of tolerance to low pH in I. orientalis that merit further validation through experimental perturbation and engineering.

Conversion↗

DOE OSTI2023

The reference genome and abiotic stress responses of the model perennial grass Brachypodium sylvaticum

Abstract Perennial grasses are important forage crops and emerging biomass crops and have the potential to be more sustainable grain crops. However, most perennial grass crops are difficult experimental subjects due to their large size, difficult genetics, and/or their recalcitrance to transformation. Thus, a tractable model perennial grass could be used to rapidly make discoveries that can be translated to perennial grass crops. Brachypodium sylvaticum has the potential to serve as such a model because of its small size, rapid generation time, simple genetics, and transformability. Here, we provide a high-quality genome assembly and annotation for B. sylvaticum, an essential resource for a modern model system. In addition, we conducted transcriptomic studies under 4 abiotic stresses (water, heat, salt, and freezing). Our results indicate that crowns are more responsive to freezing than leaves which may help them overwinter. We observed extensive transcriptional responses with varying temporal dynamics to all abiotic stresses, including classic heat-responsive genes. These results can be used to form testable hypotheses about how perennial grasses respond to these stresses. Taken together, these results will allow B. sylvaticum to serve as a truly tractable perennial model system.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2020

Phloem Exudate Protein Profiles during Drought and Recovery Reveal Abiotic Stress Responses in Tomato Vasculature

Drought is the leading cause of agricultural yield loss among all abiotic stresses, and the link between water deficit and phloem protein contents is relatively unexplored. Here we collected phloem exudates from Solanum lycopersicum leaves during periods of drought stress and recovery. Our analysis identified 2558 proteins, the most abundant of which were previously localized to the phloem. Independent of drought, enrichment analysis of the total phloem exudate protein profiles from all samples suggests that the protein content of phloem sap is complex, and includes proteins that function in chaperone systems, branched-chain amino acid synthesis, trehalose metabolism, and RNA silencing. We observed 169 proteins whose abundance changed significantly within the phloem sap, either during drought or recovery. Proteins that became significantly more abundant during drought include members of lipid metabolism, chaperone-mediated protein folding, carboxylic acid metabolism, abscisic acid signaling, cytokinin biosynthesis, and amino acid metabolism. Conversely, proteins involved in lipid signaling, sphingolipid metabolism, cell wall organization, carbohydrate metabolism, and a mitogen-activated protein kinase are decreased during drought. Our experiment has achieved an in-depth profiling of phloem sap protein contents during drought stress and recovery that supports previous findings and provides new evidence that multiple biological processes are involved in drought adaptation.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2023

Stressing the importance of plant specialized metabolites: omics-based approaches for discovering specialized metabolism in plant stress responses

Plants produce a diverse range of specialized metabolites that play pivotal roles in mediating environmental interactions and stress adaptation. These unique chemical compounds also hold significant agricultural, medicinal, and industrial values. Despite the expanding knowledge of their functions in plant stress interactions, understanding the intricate biosynthetic pathways of these natural products remains challenging due to gene and pathway redundancy, multifunctionality of proteins, and the activity of enzymes with broad substrate specificity. In the past decade, substantial progress in genomics, transcriptomics, metabolomics, and proteomics has made the exploration of plant specialized metabolism more feasible than ever before. Notably, recent advances in integrative multi-omics and computational approaches, along with other technologies, are accelerating the discovery of plant specialized metabolism. In this review, we present a summary of the recent progress in the discovery of plant stress-related specialized metabolites. Emphasis is placed on the application of advanced omics-based approaches and other techniques in studying plant stress-related specialized metabolism. Additionally, we discuss the high-throughput methods for gene functional characterization. These advances hold great promise for harnessing the potential of specialized metabolites to enhance plant stress resilience in the future.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2022

Comparative transcriptomics and metabolomics reveal specialized metabolite drought stress responses in switchgrass ( Panicum virgatum )

Summary Switchgrass ( Panicum virgatum ) is a bioenergy model crop valued for its energy efficiency and drought tolerance. The related monocot species rice ( Oryza sativa ) and maize ( Zea mays ) deploy species‐specific, specialized metabolites as core stress defenses. By contrast, specialized chemical defenses in switchgrass are largely unknown. To investigate specialized metabolic drought responses in switchgrass, we integrated tissue‐specific transcriptome and metabolite analyses of the genotypes Alamo and Cave‐in‐Rock that feature different drought tolerance. The more drought‐susceptible Cave‐in‐Rock featured an earlier onset of transcriptomic changes and significantly more differentially expressed genes in response to drought compared to Alamo. Specialized pathways showed moderate differential expression compared to pronounced transcriptomic alterations in carbohydrate and amino acid metabolism. However, diterpenoid‐biosynthetic genes showed drought‐inducible expression in Alamo roots, contrasting largely unaltered triterpenoid and phenylpropanoid pathways. Metabolomic analyses identified common and genotype‐specific flavonoids and terpenoids. Consistent with transcriptomic alterations, several root diterpenoids showed significant drought‐induced accumulation, whereas triterpenoid abundance remained predominantly unchanged. Structural analysis verified select drought‐responsive diterpenoids as oxygenated furanoditerpenoids. Drought‐dependent transcriptome and metabolite profiles provide the foundation to understand the molecular mechanisms underlying switchgrass drought responses. Accumulation of specialized root diterpenoids and corresponding pathway transcripts supports a role in drought stress tolerance.

transcriptomics↗

DOE OSTI2020

Transcriptional Regulatory Networks Involved in C3–C4 Alcohol Stress Response and Tolerance in Yeast

Alcohol toxicity significantly impacts the titer and productivity of industrially produced biofuels. To overcome this limitation, we must find and use strategies to improve stress tolerance in production strains. Previously, we developed a multiplex navigation of a global regulatory network (MINR) library that targeted 25 regulatory genes that are predicted to modify global regulation in yeast under different stress conditions. Herein, we expanded this concept to target the active sites of 47 transcriptional regulators using a saturation mutagenesis library. The 47 targeted regulators interact with more than half of all yeast genes. We then screened and selected for C3–C4 alcohol tolerance. We identified specific mutants that have resistance to isopropanol and isobutanol. Notably, the WAR1_K110N variant improved tolerance to both isopropanol and isobutanol. In addition, we investigated the mechanisms for improvement of isopropanol and isobutanol stress tolerance and found that genes related to glycolysis play a role in tolerance to isobutanol, while changes in ATP synthesis and mitochondrial respiration play a role in tolerance to both isobutanol and isopropanol. Overall, this work sheds light on basic mechanisms for isopropanol and isobutanol toxicity and demonstrates a promising strategy to improve tolerance to C3–C4 alcohols by perturbing the transcriptional regulatory network.

09 BIOMASS FUELS↗