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DOE OSTI2021

Arabidopsis thaliana zinc accumulation in leaf trichomes is correlated with zinc concentration in leaves

Zinc (Zn) is a key micronutrient for plants and animals, and understanding Zn homeostasis in plants can improve both agriculture and human health. While root Zn transporters in plant model species have been characterized in detail, comparatively little is known about shoot processes controlling Zn concentrations and spatial distribution. Previous work showed that Zn hyperaccumulator species such as Arabidopsis halleri accumulate Zn and other metals in leaf trichomes. To date there is no systematic study regarding Zn accumulation in the trichomes of the non-accumulating, genetic model species A. thaliana. Here, we used Synchrotron X-Ray Fluorescence mapping to show that Zn accumulates at the base of trichomes of A. thaliana. Using transgenic and natural accessions of A thaliana that vary in bulk leaf Zn concentration, we demonstrate that higher leaf Zn increases total Zn found at the base of trichome cells. Our data indicates that Zn accumulation in trichomes is a function of the Zn status of the plant, and provides the basis for future studies on a genetically tractable plant species to understand the molecular steps involved in Zn spatial distribution in leaves.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2023

Variable lignin structure revealed in Populus leaves

NMR analysis of Populus leaves revealed lignin traits such as condensed syringyl units and both erythron / threo conformations of the β-O-4 linkage. Lignin structure was also well correlated with certain metabolites such as salicin derivatives.

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗

DOE OSTI2020

Source of 12 C in Calvin–Benson cycle intermediates and isoprene emitted from plant leaves fed with 13 CO 2

Feeding 14 CO 2 was crucial to uncovering the path of carbon in photosynthesis. Feeding 13 CO 2 to photosynthesizing leaves emitting isoprene has been used to develop hypotheses about the sources of carbon for the methylerythritol 4-phosphate pathway, which makes the precursors for terpene synthesis in chloroplasts and bacteria. Both photosynthesis and isoprene studies found that products label very quickly (<10 min) up to 80–90% but the last 10–20% of labeling requires hours indicating a source of 12 C during photosynthesis and isoprene emission. Furthermore, studies with isoprene showed that the proportion of slow label could vary significantly. This was interpreted as a variable contribution of carbon from sources other than the Calvin–Benson cycle (CBC) feeding the methylerythritol 4-phosphate pathway. Here, we measured the degree of label in isoprene and photosynthetic metabolites 20 min after beginning to feed 13 CO 2 . Isoprene labeling was the same as labeling of photosynthesis intermediates. High temperature reduced the label in isoprene and photosynthesis intermediates by the same amount indicating no role for alternative carbon sources for isoprene. A model assuming glucose, fructose, and/or sucrose reenters the CBC as ribulose 5-phosphate through a cytosolic shunt involving glucose 6-phosphate dehydrogenase was consistent with the observations.

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗

DOE OSTI2024

Triacylglycerol stability limits futile cycles and inhibition of carbon capture in oil-accumulating leaves

Engineering plant vegetative tissue to accumulate triacylglycerols (TAG, e.g. oil) can increase the amount of oil harvested per acre to levels that exceed current oilseed crops. Engineered tobacco (Nicotiana tabacum) lines that accumulate 15% to 30% oil of leaf dry weight resulted in starkly different metabolic phenotypes. In-depth analysis of the leaf lipid accumulation and 14 CO 2 tracking describe metabolic adaptations to the leaf oil engineering. An oil-for-membrane lipid tradeoff in the 15% oil line (referred to as HO) was surprisingly not further exacerbated when lipid production was enhanced to 30% (LEAFY COTYLEDON 2 (LEC2) line). The HO line exhibited a futile cycle that limited TAG yield through exchange with starch, altered carbon flux into various metabolite pools and end products, and suggested interference of the glyoxylate cycle with photorespiration that limited CO 2 assimilation by 50%. In contrast, inclusion of the LEC2 transcription factor in tobacco improved TAG stability, alleviated the TAG-to-starch futile cycle, and recovered CO 2 assimilation and plant growth comparable to wild type but with much higher lipid levels in leaves. Thus, the unstable production of storage reserves and futile cycling limit vegetative oil engineering approaches. The capacity to overcome futile cycles and maintain enhanced stable TAG levels in LEC2 demonstrated the importance of considering unanticipated metabolic adaptations while engineering vegetative oil crops.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2021

CO2 refixation is higher in leaves of woody species with high mesophyll and stomatal resistances to CO2 diffusion

Abstract The percentage of respiratory and photorespiratory CO2 refixed in leaves (Pr) represents part of the CO2 used in photosynthesis. The importance of Pr as well as differences between species and functional types are still not well investigated. In this study, we examine how Pr differs between six temperate and boreal woody species: Betula pendula, Quercus robur, Larix decidua, Pinus sylvestris, Picea abies and Vaccinium vitis-idaea. The study covers early and late successional species, deciduous broadleaves, deciduous conifers, evergreen conifers and evergreen broadleaves. We investigated whether some species or functional types had higher refixation percentages than others, whether leaf traits could predict higher Pr and whether these traits and their impact on Pr changed during growing seasons. Photosynthesis CO2 response (A/Ci)-curves, measured early, mid and late season, were used to estimate and compare Pr, mesophyll resistance (rm) and stomatal resistance (rs) to CO2 diffusion. Additionally, light images and transmission electron microscope images were used to approximate the fraction of intercellular airspace and cell wall thickness. We found that evergreens, especially late successional species, refixed a significantly higher amount of CO2 than the other species throughout the entire growing season. In addition, rm, rs and leaf mass per area, traits that typically are higher in evergreen species, were also significantly, positively correlated with Pr. We suggest that this is due to higher rm decreasing diffusion of (photo) respiratory CO2 out of the leaf. Cell wall thickness had a positive effect on Pr and rm, while the fraction of intercellular airspace had no effect. Both were significantly different between evergreen conifers and other types. Our findings suggest that species with a higher rm use a greater fraction of mitochondria-derived CO2, especially when stomatal conductance is low. This should be taken into account when modeling the overall CO2 fertilization effect for terrestrial ecosystems dominated by high rm species.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2021

Maximum CO 2 diffusion inside leaves is limited by the scaling of cell size and genome size

Maintaining high rates of photosynthesis in leaves requires efficient movement of CO 2 from the atmosphere to the mesophyll cells inside the leaf where CO 2 is converted into sugar. CO 2 diffusion inside the leaf depends directly on the structure of the mesophyll cells and their surrounding airspace, which have been difficult to characterize because of their inherently three-dimensional organization. Yet faster CO 2 diffusion inside the leaf was probably critical in elevating rates of photosynthesis that occurred among angiosperm lineages. Here we characterize the three-dimensional surface area of the leaf mesophyll across vascular plants. We show that genome size determines the sizes and packing densities of cells in all leaf tissues and that smaller cells enable more mesophyll surface area to be packed into the leaf volume, facilitating higher CO 2 diffusion. Measurements and modelling revealed that the spongy mesophyll layer better facilitates gaseous phase diffusion while the palisade mesophyll layer better facilitates liquid-phase diffusion. Our results demonstrate that genome downsizing among the angiosperms was critical to restructuring the entire pathway of CO 2 diffusion into and through the leaf, maintaining high rates of CO 2 supply to the leaf mesophyll despite declining atmospheric CO 2 levels during the Cretaceous.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2023

Climate change increases carbon allocation to leaves in early leaf green-up

Global greening, characterized by an increase in leaf area index (LAI), implies an increase in foliar carbon (C). Whether this increase in foliar C under climate change is due to higher photosynthesis or to higher allocation of C to leaves remains unknown. Here, we explored the trends in foliar C accumulation and allocation during leaf green-up from 2000 to 2017 using satellite-derived LAI and solar-induced chlorophyll fluorescence (SIF) across the Northern Hemisphere. The accumulation of foliar C accelerated in the early green-up period due to both increased photosynthesis and higher foliar C allocation driven by climate change. In the late stage of green-up, however, we detected decreasing trends in foliar C accumulation and foliar C allocation. Such stage-dependent trends in the accumulation and allocation of foliar C are not represented in current terrestrial biosphere models. Further, our results highlight that a better representation of C allocation should be incorporated into models.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2022

Utilisation of flavonoids from Lycium barbarum L. leaves cross‐linked with whey protein for the stabilisation and delivery of β ‐carotene emulsions

Summary Although β ‐carotene is an essential nutrient for the maintenance of human health, it is insoluble in water and extremely unstable, which limits its application. Here, we prepared a stable emulsification system of whey protein (WP)‐ Lycium barbarum L. leaves flavonoids (LBLF) complex as a carrier to load β ‐carotene. The rheological properties, antioxidant properties and stability of emulsion were studied, and the effects of emulsion on the biological retention of β ‐carotene and stability were investigated. The results indicate that, compared with WP, the WP‐LBLF emulsion has smaller particles, a smaller creaming index, and significantly enhanced chemical stability under light and heat treatment conditions. The thiobarbituric acid value of the WP‐LBLF emulsion (0.031 ± 0.016 mg/kg) was dramatically lower than that of the WP emulsion (0.045 ± 0.012 mg/kg) ( P < 0.05). In the simulated gastrointestinal digestion experiment, the retention rate of β ‐carotene was higher in WP‐LBLF emulsion. Additionally, the WP‐LBLF emulsion loaded with β ‐carotene has good salt tolerance and heat stability. In our study, WP‐LBLF was used as an emulsifier to load β ‐carotene emulsion to improve its bioavailability and stability, which provides a new preparation and application method for a complex functional emulsifier.

Fan, Yanli↗

DOE OSTI2020

Is the Kok effect a respiratory phenomenon? Metabolic insight using 13 C labeling in Helianthus annuus leaves

The Kok effect is a well-known phenomenon in which the quantum yield of photosynthesis changes abruptly at low light. This effect has often been interpreted as a shift in leaf respiratory metabolism and thus used widely to measure day respiration. However, there is still no formal evidence that the Kok effect has a respiratory origin. Here, both gas exchange and isotopic labeling were carried out on sunflower leaves, using glucose that was 13 C-enriched at specific C-atom positions. Position-specific decarboxylation measurements and NMR analysis of metabolites were used to trace the fate of C-atoms in metabolism. Decarboxylation rates were significant at low light (including above the Kok break point) and increased with decreasing irradiance below 100 µmol photons m –2 s –1 . The variation in several metabolite pools such as malate, fumarate or citrate, and flux calculations suggest the involvement of several decarboxylating pathways in the Kok effect, including the malic enzyme. Our results show that day respiratory CO 2 evolution plays an important role in the Kok effect. Furthermore, the increase in the apparent quantum yield of photosynthesis below the Kok break point is also probably related to malate metabolism, which participates in maintaining photosynthetic linear electron flow.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2024

The expression of genes encoding novel Sesame oleosin variants facilitates enhanced triacylglycerol accumulation in Arabidopsis leaves and seeds

Summary Triacylglycerols (TAG), accumulate within lipid droplets (LD), predominantly surrounded by OLEOSINs (OLE), that protect TAG from hydrolysis. We tested the hypothesis that identifying and removing degradation signals from OLE would promote its abundance, preventing TAG degradation and enhancing TAG accumulation. We tested whether mutating potential ubiquitin‐conjugation sites in a previously reported improved Sesamum indicum OLE ( SiO ) variant, o3‐3 Cys‐OLE ( SiCO herein), would stabilize it and increase its lipogenic potential. SiCOv1 was created by replacing all five lysines in SiCO with arginines. Separately, six cysteine residues within SiCO were deleted to create SiCOv2. SiCOv1 and SiCOv2 mutations were combined to create SiCOv3. Transient expression of SiCOv3 in Nicotiana benthamiana increased TAG by two‐fold relative to SiCO. Constitutive expression of SiCOv3 or SiCOv5 , containing the five predominant TAG‐increasing mutations from SiCOv3 , in Arabidopsis along with mouse DGAT2 ( mD ) increased TAG accumulation by 54% in leaves and 13% in seeds compared with control lines coexpressing SiCO and mD. Lipid synthesis rates increased, consistent with an increase in lipid sink strength that sequesters newly synthesized TAG, thereby relieving the constitutive BADC‐dependent inhibition of ACCase reported for WT Arabidopsis. These OLE variants represent novel factors for potentially increasing TAG accumulation in a variety of oil crops.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2024

Data for the Expression of Genes Encoding Novel Sesame Oleosin Variants Facilitates Enhanced Triacylglycerol Accumulation in Arabidopsis Leaves and Seeds

Triacylglycerols (TAG), accumulate within lipid droplets (LD), predominantly surrounded by OLEOSINs (OLE), that protect TAG from hydrolysis. We tested the hypothesis that identifying and removing degradation signals from OLE would promote its abundance, preventing TAG degradation and enhancing TAG accumulation. We tested whether mutating potential ubiquitin-conjugation sites in a previously reported improved Sesamum indicum OLE ( SiO ) variant, o3-3 Cys-OLE ( SiCO herein), would stabilize it and increase its lipogenic potential. SiCOv1 was created by replacing all five lysines in SiCO with arginines. Separately, six cysteine residues within SiCO were deleted to create SiCOv2. SiCOv1 and SiCOv2 mutations were combined to create SiCOv3. Transient expression of SiCOv3 in Nicotiana benthamiana increased TAG by two-fold relative to SiCO. Constitutive expression of SiCOv3 or SiCOv5 , containing the five predominant TAG-increasing mutations from SiCOv3 , in Arabidopsis along with mouse DGAT2 ( mD ) increased TAG accumulation by 54% in leaves and 13% in seeds compared with control lines coexpressing SiCO and mD . Lipid synthesis rates increased, consistent with an increase in lipid sink strength that sequesters newly synthesized TAG, thereby relieving the constitutive BADC-dependent inhibition of ACCase reported for WT Arabidopsis. These OLE variants represent novel factors for potentially increasing TAG accumulation in a variety of oil crops.

Feedstock Production↗

DOE OSTI2023

Anomaly Detection and Identification Using a Leave-One-Variable-Out Method

At nuclear power plants (NPPs), anomaly detection and identification (i.e., determining the causes of anomalies) are important tasks for ensuring the safe and efficient operation of NPPs. These tasks are currently labor-intensive and costly, and are made more difficult by the size and complexity of NPP systems. An alternative approach to conducting these tasks is to automate them, such as via the reconstruction-based contribution method, which is a well-researched unsupervised machine learning method that uses a data-driven model of anomaly-free behavior to detect events and then identify each variable’s contributions to those events. The present effort developed a novel contribution approach that utilized a leave-one-variable-out (LOVO) model, with which each variable is predicted using all the other variables. The novelty lay in transforming this model into a reconstruction model and modifying the identification algorithm to work with the new reconstruction model. To evaluate this method in a controlled environment, a synthetic dataset based on spring-mass-damper (SMD) systems (commonly found in mechanical engineering references) was used, with known anomalies introduced into the system. The proposed method successfully detected the anomalies and afforded insights into their causes, thus enabling the appropriate identifications to be made.

46 INSTRUMENTATION RELATED TO NUCLEAR SCIENCE AND ↗

DOE OSTI2025

Comparing the predictive capabilities of subjective crackle metrics using leave-one-out cross validation

Leave-one-out cross validation was used to show the capability to predict crackling sound quality based on the use of the standard deviation of the time-varying sharpness and the skewness of the derivative of the pressure waveform. The predictive output of this method implies that the more sophisticated fits used to describe this data were not overfit, but instead exhibited substantial predictive value.

Swift, Stephen Hales [Sandia National Laboratories↗

DOE OSTI2026

Data from "What regulates decomposition in agroecosystems? Insights from reading the tea leaves"

Agricultural land management↗

DOE OSTI2024

Elemental profiling and genome-wide association studies reveal genomic variants modulating ionomic composition in Populus trichocarpa leaves

The ionome represents elemental composition in plant tissues and can be an indicator of nutrient status as well as overall plant performance. Thus, identifying genetic determinants governing elemental uptake and storage is an important goal for breeding and engineering biomass feedstocks with improved performance. In this study, we coupled high-throughput ionome characterization of leaf tissues with high-resolution genome-wide association studies (GWAS) to uncover genetic loci that modulate ionomic composition in leaves of poplar ( Populus trichocarpa ). Significant agreement was observed across the three ionomic profiling platforms tested: inductively coupled plasma-mass spectrometry (ICP-MS), neutron activation analysis (NAA) and laser-induced breakdown spectroscopy (LIBS). Relative quantification of 20 elements using ICP-MS across a population of 584 genotypes, revealed larger variation in micro-nutrients and trace elements content than for macro-nutrients across genotypes. The GWAS performed using a set of high-density (>8.2 million) single nucleotide polymorphisms, identified over 600 loci significantly associated with variations in these mineral elements, pointing to numerous uncharacterized candidate genes. A significant enrichment for genes related to ion homeostasis and transport was observed, including several members of the cation-proton antiporters (CPA) family and MATE efflux transporters, previously reported to be critical for plant growth and fitness in other species. Our results also included a polymorphic copy of the high-affinity molybdenum transporter MOT1 found directly associated to molybdenum content. For the first time in a perennial plant, our results provide evidence of genetic control of mineral content in a model tree species.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2025

What regulates decomposition in agroecosystems? Insights from reading the tea leaves

Litter decomposition is a critical Earth process, recycling nutrients and setting a portion of plant tissue on a path toward soil organic matter. Despite this importance, we still lack a good understanding of local factors that regulate decomposition, especially in agroecosystems where management plays an outsized role. Using a narrow range of climate and soils, we buried 1,308 pre-manufactured “litter bags” of differing residue quality (i.e., green and rooibos tea leaves) in 109 plots across several management practices to (1) explore the local controls on decomposition in agroecosystems and (2) test the robustness of the Tea Bag Index (TBI). We found that management practices intended to increase soil ecosystem services, that is, soil health, altered the decomposition of both teas. For example, adding nitrogen fertilizer and implementing perennial cropping decreased the extent of green tea decomposition (carbon-to-nitrogen ratio, or C:N = 12.8). No-tillage increased, but perennial cropping decreased, the rate of rooibos tea decomposition (C:N = 50.1). Cropped prairie accelerated green tea decomposition and increased the extent of red tea decomposition. A random forest regression model showed that soil temperature was the strongest predictor of green tea decomposition, but a soil health score also played a significant role in predicting the mass remaining. Soil texture and nutrient availability best predicted rooibos tea decomposition. Finer textured soils seemed to decelerate rooibos decomposition but increased the extent of decomposition. Furthermore, we demonstrated that the TBI metrics correlated somewhat well with empirically derived decomposition constants and were similarly sensitive to the effects of management. Still, the green tea stabilization factor had a substantial prediction bias. Our study increased our basic understanding of what regulates decomposition in agroecosystems. It also showed that the TBI can be a scientifically rigorous citizen science approach to monitoring changes in soil health.

60 APPLIED LIFE SCIENCES↗

DOE OSTI2021

Ectopic Expression of OLEOSIN 1 and Inactivation of GBSS1 Have a Synergistic Effect on Oil Accumulation in Plant Leaves

During the transformation of wild-type (WT) Arabidopsis thaliana, a T-DNA containing OLEOSIN-GFP (OLE1-GFP) was inserted by happenstance within the GBSS1 gene, resulting in significant reduction in amylose and increase in leaf oil content in the transgenic line (OG). The synergistic effect on oil accumulation of combining gbss1 with the expression of OLE1-GFP was confirmed by transforming an independent gbss1 mutant (GABI_914G01) with OLE1-GFP. The resulting OLE1-GFP/gbss1 transgenic lines showed higher leaf oil content than the individual OLE1-GFP/WT or single gbss1 mutant lines. Further stacking of the lipogenic factors WRINKLED1, Diacylglycerol O-Acyltransferase (DGAT1), and Cys-OLEOSIN1 (an engineered sesame OLEOSIN1) in OG significantly elevated its oil content in mature leaves to 2.3% of dry weight, which is 15 times higher than that in WT Arabidopsis. Inducible expression of the same lipogenic factors was shown to be an effective strategy for triacylglycerol (TAG) accumulation without incurring growth, development, and yield penalties.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2024

Challenges and Solutions for Leave-One-Out Biosensor Design in the Context of a Rugged Fitness Landscape

The leave-one-out (LOO) green fluorescent protein (GFP) approach to biosensor design combines computational protein design with split protein reconstitution. LOO-GFPs reversibly fold and gain fluorescence upon encountering the target peptide, which can be redefined by computational design of the LOO site. Such an approach can be used to create reusable biosensors for the early detection of emerging biological threats. Enlightening biophysical inferences for nine LOO-GFP biosensor libraries are presented, with target sequences from dengue, influenza, or HIV, replacing beta strands 7, 8, or 11. An initially low hit rate was traced to components of the energy function, manifesting in the over-rewarding of over-tight side chain packing. Also, screening by colony picking required a low library complexity, but designing a biosensor against a peptide of at least 12 residues requires a high-complexity library. This double-bind was solved using a “piecemeal” iterative design strategy. Also, designed LOO-GFPs fluoresced in the unbound state due to unwanted dimerization, but this was solved by fusing a fully functional prototype LOO-GFP to a fiber-forming protein, Drosophila ultrabithorax, creating a biosensor fiber. One influenza hemagglutinin biosensor is characterized here in detail, showing a shifted excitation/emission spectrum, a micromolar affinity for the target peptide, and an unexpected photo-switching ability.

Chemistry↗