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All sourcesNASA NTRSDOE OSTI
DOE OSTI2021

GTP binding by Arabidopsis extra-large G protein 2 is not essential for its functions

The extra-large guanosine-5'-triphosphate (GTP)-binding protein 2, XLG2, is an unconventional Gα subunit of the Arabidopsis (Arabidopsis thaliana) heterotrimeric GTP-binding protein complex with a major role in plant defense. In vitro biochemical analyses and molecular dynamic simulations show that affinity of XLG2 for GTP is two orders of magnitude lower than that of the conventional Gα, AtGPA1. Here we tested the physiological relevance of GTP binding by XLG2. We generated an XLG2(T476N) variant with abolished GTP binding, as confirmed by in vitro GTPγS binding assay. Yeast three-hybrid, bimolecular fluorescence complementation, and split firefly-luciferase complementation assays revealed that the nucleotide-depleted XLG2(T476N) retained wild-type XLG2-like interactions with the Gβγ dimer and defense-related receptor-like kinases. Both wild-type and nucleotide-depleted XLG2(T476N) restored the defense responses against Fusarium oxysporum and Pseudomonas syringae compromised in the xlg2 xlg3 double mutant. Additionally, XLG2(T476N) was fully functional restoring stomatal density, root growth, and sensitivity to NaCl, but failed to complement impaired germination and vernalization-induced flowering. We conclude that XLG2 is able to function in a GTP-independent manner and discuss its possible mechanisms of action.

Plant Sciences↗
DOE OSTI2021

Seawater exposure causes hydraulic damage in dying Sitka-spruce trees

Sea-level rise is one of the most critical challenges facing coastal ecosystems under climate change. Observations of elevated tree mortality in global coastal forests are increasing, but the mechanism of salinity-stress induced tree mortality is currently unknown. We monitored progressive mortality and associated gas exchange and hydraulic shifts in Sitka-spruce (Picea sitchensis) trees located within a salinity gradient under an ecosystem-scale change of seawater exposure in Washington State, USA. Percentage of live foliated crown (PLFC) decreased and tree mortality increased with increasing soil salinity during the study period. A strong reduction in gas exchange and xylem hydraulic conductivity (Ks) occurred during tree death, with an increase of the percentage loss of xylem conductivity (PLC) and turgor loss point (ptlp). Hydraulic and osmotic shifts reflected that hydraulic function declined from seawater exposure and dying trees were unable to support osmotic adjustment. Constrained gas exchange was strongly related to hydraulic damage at both stem and leaf levels. Significant correlations between foliar sodium (Na+) concentration and gas exchange and key hydraulic parameters (Ks, PLC and ptlp ) suggest that cellular injury related to the toxic effects of ion accumulation impacted the physiology of these dying trees. This study provides evidence of toxic effects on cellular function that become manifest in all aspects of plant functioning, leading to unfavourable osmotic and hydraulic conditions.

Zhang, Hongxia↗
DOE OSTI2021

Desiccation and rehydration dynamics in the epiphytic resurrection fern Pleopeltis polypodioides

The epiphytic resurrection—or desiccation-tolerant (DT)—fern Pleopeltis polypodioides can survive extreme desiccation and recover physiological activity within hours of rehydration. Yet, how epiphytic DT ferns coordinate between deterioration and recovery of their hydraulic and photosynthetic systems remains poorly understood. We examined the functional status of the leaf vascular system, chlorophyll fluorescence, and photosynthetic rate during desiccation and rehydration of P. polypodioides. Xylem tracheids in the stipe embolized within 3–4 h during dehydration. When the leaf and rhizome received water, tracheids refilled after ~24 h, which occurred along with dramatic structural changes in the stele. Photosynthetic rate and chlorophyll fluorescence recovered to predesiccation values within 12 h of rehydration, regardless of whether fronds were connected to their rhizome. Our data show that the epiphytic DT fern P. polypodioides can utilize foliar water uptake to rehydrate the leaf mesophyll and recover photosynthesis despite a broken hydraulic connection to the rhizome.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2022

Heinz-resistant tomato cultivars exhibit a lignin-based resistance to field dodder ( Cuscuta campestris ) parasitism

Cuscuta species (dodders) are agriculturally destructive, parasitic angiosperms. These parasitic plants use haustoria as physiological bridges to extract nutrients and water from hosts. Cuscuta campestris has a broad host range and wide geographical distribution. While some wild tomato relatives are resistant, cultivated tomatoes are generally susceptible to C. campestris infestations. However, some specific Heinz tomato (Solanum lycopersicum) hybrid cultivars exhibit resistance to dodders in the field, but their defense mechanism was previously unknown. Here, we discovered that the stem cortex in these resistant lines responds with local lignification upon C. campestris attachment, preventing parasite entry into the host. Lignin Induction Factor 1 (LIF1, an AP2-like transcription factor), SlMYB55, and Cuscuta R-gene for Lignin-based Resistance 1, a CC-NBS-LRR (CuRLR1) are identified as factors that confer host resistance by regulating lignification. SlWRKY16 is upregulated upon C. campestris infestation and potentially negatively regulates LIF1 function. Intriguingly, CuRLR1 may play a role in signaling or function as an intracellular receptor for receiving Cuscuta signals or effectors, thereby regulating lignification-based resistance. In summary, these four regulators control the lignin-based resistance response in specific Heinz tomato cultivars, preventing C. campestris from parasitizing resistant tomatoes. This discovery provides a foundation for investigating multilayer resistance against Cuscuta species and has potential for application in other essential crops attacked by parasitic plants.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2022

Altered properties and structures of root exudate polysaccharides in a root hairless mutant of barley

Root exudates and rhizosheaths of attached soil are important features of growing roots. To elucidate factors involved in rhizosheath formation, wild-type (WT) barley (Hordeum vulgare L. cv. Pallas) and a root hairless mutant, bald root barley (brb), were investigated with a combination of physiological, biochemical, and immunochemical assays. When grown in soil, WT barley roots bound ~5-fold more soil than brb per unit root length. High molecular weight (HMW) polysaccharide exudates of brb roots had less soil-binding capacity than those of WT root exudates. Carbohydrate and glycan monoclonal antibody analyses of HMW polysaccharide exudates indicated differing glycan profiles. Relative to WT plants, root exudates of brb had reduced signals for arabinogalactan-protein (AGP), extensin, and heteroxylan epitopes. In contrast, the root exudate of 2-week-old brb plants contained ~25-fold more detectable xyloglucan epitope relative to WT. Root system immunoprints confirmed the higher levels of release of the xyloglucan epitope from brb root apices and root axes relative to WT. Epitope detection with anion-exchange chromatography indicated that the increased detection of xyloglucan in brb exudates was due to enhanced abundance of a neutral polymer. Conversely, brb root exudates contained decreased amounts of an acidic polymer, with soil-binding properties, containing the xyloglucan epitope and glycoprotein and heteroxylan epitopes relative to WT. We, therefore, propose that, in addition to physically structuring soil particles, root hairs facilitate rhizosheath formation by releasing a soil-binding polysaccharide complex.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2022

Uncoupling differential water usage from drought resistance in a dwarf Arabidopsis mutant

Abstract Understanding the molecular and physiological mechanisms of how plants respond to drought is paramount to breeding more drought-resistant crops. Certain mutations or allelic variations result in plants with altered water-use requirements. To correctly identify genetic differences which confer a drought phenotype, plants with different genotypes must be subjected to equal levels of drought stress. Many reports of advantageous mutations conferring drought resistance do not control for soil water content (SWC) variations across genotypes and may therefore need to be re-examined. Here, we reassessed the drought phenotype of the Arabidopsis (Arabidopsis thaliana) dwarf mutant, chiquita1-1 (chiq1-1, also called constitutively stressed 1 (cost1)), by growing mutant seedlings together with the wild-type to ensure uniform soil water availability across genotypes. Our results demonstrate that the dwarf phenotype conferred by loss of CHIQ1 function results in constitutively lower water usage per plant, but not increased drought resistance. Our study provides an easily reproducible, low-cost method to measure and control for SWC and to compare drought-resistant genotypes more accurately.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2023

High-throughput, dynamic, multi-dimensional: an expanding repertoire of plant respiration measurements

A recent burst of technological innovation and adaptation has greatly improved our ability to capture respiration rate data from plant sources. At the tissue level, several independent respiration measurement options are now available, each with distinct advantages and suitability, including high-throughput sampling capacity. These advancements facilitate the inclusion of respiration rate data into large-scale biological studies such as genetic screens, ecological surveys, crop breeding trials, and multi-omics molecular studies. As a result, our understanding of the correlations of respiration with other biological and biochemical measurements is rapidly increasing. Difficult questions persist concerning the interpretation and utilization of respiration data; concepts such as allocation of respiration to growth versus maintenance, the unnecessary or inefficient use of carbon and energy by respiration, and predictions of future respiration rates in response to environmental change are all insufficiently grounded in empirical data. However, we emphasize that new experimental designs involving novel combinations of respiration rate data with other measurements will flesh-out our current theories of respiration. Furthermore, dynamic recordings of respiration rate, which have long been used at the scale of mitochondria, are increasingly being used at larger scales of size and time to reflect processes of cellular signal transduction and physiological response to the environment. Herein, we also highlight how respiratory methods are being better adapted to different plant tissues including roots and seeds, which have been somewhat neglected historically.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2023

Optimizing the electron transport chain to sustainably improve photosynthesis

Abstract Genetically improving photosynthesis is a key strategy to boosting crop production to meet the rising demand for food and fuel by a rapidly growing global population in a warming climate. Many components of the photosynthetic apparatus have been targeted for genetic modification for improving photosynthesis. Successful translation of these modifications into increased plant productivity in fluctuating environments will depend on whether the electron transport chain (ETC) can support the increased electron transport rate without risking overreduction and photodamage. At present atmospheric conditions, the ETC appears suboptimal and will likely need to be modified to support proposed photosynthetic improvements and to maintain energy balance. Here, I derive photochemical equations to quantify the transport capacity and the corresponding reduction level based on the kinetics of redox reactions along the ETC. Using these theoretical equations and measurements from diverse C3/C4 species across environments, I identify several strategies that can simultaneously increase the transport capacity and decrease the reduction level of the ETC. These strategies include increasing the abundances of reaction centers, cytochrome b6f complexes, and mobile electron carriers, improving their redox kinetics, and decreasing the fraction of secondary quinone–nonreducing photosystem II reaction centers. I also shed light on several previously unexplained experimental findings regarding the physiological impacts of the abundances of the cytochrome b6f complex and plastoquinone. The model developed, and the insights generated from it facilitate the development of sustainable photosynthetic systems for greater crop yields.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2024

Cynipid wasps systematically reprogram host metabolism and restructure cell walls in developing galls

Many insects have evolved the ability to manipulate plant growth to generate extraordinary structures called galls, in which insect larva can develop while being sheltered and feeding on the plant. In particular, cynipid (Hymenoptera: Cynipidae) wasps have evolved to form morphologically complex galls and generate an astonishing array of gall shapes, colors, and sizes. However, the biochemical basis underlying these remarkable cellular and developmental transformations remains poorly understood. A key determinant in plant cellular development is cell wall deposition that dictates the physical form and physiological function of newly developing cells, tissues, and organs. However, it is unclear to what degree cell walls are restructured to initiate and support the formation of new gall tissue. Here, we characterize the molecular alterations underlying gall development using a combination of metabolomic, histological, and biochemical techniques to elucidate how valley oak (Quercus lobata) leaf cells are reprogrammed to form galls. Strikingly, gall development involves an exceptionally coordinated spatial deposition of lignin and xylan to form de novo gall vasculature. Our results highlight how cynipid wasps can radically change the metabolite profile and restructure the cell wall to enable the formation of galls, providing insights into the mechanism of gall induction and the extent to which plants can be entirely reprogrammed to form unique structures and organs.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2024

Chloroplast phosphatases LPPγ and LPPε1 facilitate conversion of extraplastidic phospholipids to galactolipids

Abstract Galactolipids comprise the majority of chloroplast membranes in plants, and their biosynthesis requires dephosphorylation of phosphatidic acid at the chloroplast envelope membranes. In Arabidopsis (Arabidopsis thaliana), the lipid phosphate phosphatases LPPγ, LPPε1, and LPPε2 have been previously implicated in chloroplast lipid assembly, with LPPγ being essential, as null mutants were reported to exhibit embryo lethality. Here, we show that lppγ mutants are in fact viable and that LPPγ, LPPε1, and LPPε2 do not appear to have central roles in the plastid pathway of membrane lipid biosynthesis. Redundant LPPγ and LPPε1 activity at the outer envelope membrane is important for plant development, and the respective lppγ lppε1 double mutant exhibits reduced flux through the ER pathway of galactolipid synthesis. While LPPε2 is imported and associated with interior chloroplast membranes, its role remains elusive and does not include basal nor phosphate limitation-induced biosynthesis of glycolipids. The specific physiological roles of LPPγ, LPPε1, and LPPε2 are yet to be uncovered, as does the identity of the phosphatidic acid phosphatase required for plastid galactolipid biosynthesis.

Cook, Ron (ORCID:0000000198356205)↗
DOE OSTI2024

Packaging “vegetable oils”: Insights into plant lipid droplet proteins

Abstract Plant neutral lipids, also known as “vegetable oils”, are synthesized within the endoplasmic reticulum (ER) membrane and packaged into subcellular compartments called lipid droplets (LDs) for stable storage in the cytoplasm. The biogenesis, modulation, and degradation of cytoplasmic LDs in plant cells are orchestrated by a variety of proteins localized to the ER, LDs, and peroxisomes. Recent studies of these LD-related proteins have greatly advanced our understanding of LDs not only as steady oil depots in seeds but also as dynamic cell organelles involved in numerous physiological processes in different tissues and developmental stages of plants. In the past 2 decades, technology advances in proteomics, transcriptomics, genome sequencing, cellular imaging and protein structural modeling have markedly expanded the inventory of LD-related proteins, provided unprecedented structural and functional insights into the protein machinery modulating LDs in plant cells, and shed new light on the functions of LDs in nonseed plant tissues as well as in unicellular algae. Here, we review critical advances in revealing new LD proteins in various plant tissues, point out structural and mechanistic insights into key proteins in LD biogenesis and dynamic modulation, and discuss future perspectives on bridging our knowledge gaps in plant LD biology.

Cai, Yingqi (ORCID:0000000203575809)↗
DOE OSTI2024

Rooting for survival: how plants tackle a challenging environment through a diversity of root forms and functions

Abstract The current climate crisis has global impacts and will affect the physiology of plants across every continent. Ensuring resilience of our agricultural and natural ecosystems to the environmental stresses imposed by climate change will require molecular insight into the adaptations employed by a diverse array of plants. However, most current studies continue to focus on a limited set of model species or crops. Root systems are particularly understudied even though their functions in water and nutrient uptake are likely pivotal for plant stress resilience and sustainable agriculture. In this review, we highlight anatomical adaptations in roots that enable plant survival in different ecological niches. We then present the current state of knowledge for the molecular underpinnings of these adaptations. Finally, we identify areas where future research using a biodiversity approach can fill knowledge gaps necessary for the development of climate-resilient crops of the future.

Plant Sciences↗
DOE OSTI2024

Modeling with uncertainty quantification reveals the essentials of a non-canonical algal carbon-concentrating mechanism

The thermoacidophilic red alga Cyanidioschyzon merolae survives its challenging environment likely in part by operating a carbon-concentrating mechanism (CCM). Here, we demonstrated that C. merolae 's cellular affinity for CO 2 is stronger than the affinity of its rubisco for CO 2 . This finding provided additional evidence that C. merolae operates a CCM while lacking the structures and functions characteristic of CCMs in other organisms. To test how such a CCM could function, we created a mathematical compartmental model of a simple CCM, distinct from those we have seen previously described in detail. The results of our modeling supported the feasibility of this proposed minimal and non-canonical CCM in C. merolae . To facilitate the robust modeling of this process, we measured and incorporated physiological and enzymatic parameters into the model. Additionally, we trained a surrogate machine-learning model to emulate the mechanistic model and characterized the effects of model parameters on key outputs. This parameter exploration enabled us to identify model features that influenced whether the model met the experimentally derived criteria for functional carbon concentration and efficient energy usage. Such parameters included cytosolic pH, bicarbonate pumping cost and kinetics, cell radius, carboxylation velocity, number of thylakoid membranes, and CO 2 membrane permeability. Our exploration thus suggested that a non-canonical CCM could exist in C. merolae and illuminated the essential features generally necessary for CCMs to function.

Steensma, Anne K. [Michigan State Univ., East Lans↗
DOE OSTI2022

Latitudinal shifts of soil microbial biomass seasonality

Soil microbes ultimately drive the mineralization of soil organic carbon and thus ecosystem functions. We compiled a dataset of the seasonality of microbial biomass carbon (MBC) and developed a semi-mechanistic model to map monthly MBC across the globe. MBC exhibits an equatorially symmetric seasonality between the Northern and Southern Hemispheres. In the Northern Hemisphere, MBC peaks in autumn and is minimal in spring at low latitudes (<25°N), peaks in the spring and is minimal in autumn at mid-latitudes (25°N to 50°N), while peaks in autumn and is minimal in spring at high latitudes (>50°N). This latitudinal shift of MBC seasonality is attributed to an interaction of soil temperature, soil moisture, and substrate availability. The MBC seasonality is inconsistent with patterns of heterotrophic respiration, indicating that MBC as a proxy for microbial activity is inappropriate at this resolution. This study highlights the need to explicitly represent microbial physiology in microbial models. The interactive controls of environments and substrate on microbial seasonality provide insights for better representing microbial mechanisms in simulating ecosystem functions at the seasonal scale.

54 ENVIRONMENTAL SCIENCES↗
DOE OSTI2023

A subcellular biochemical model for T6SS dynamics reveals winning competitive strategies

Abstract The type VI secretion system (T6SS) is a broadly distributed interbacterial weapon that can be used to eliminate competing bacterial populations. Although unarmed target populations are typically used to study T6SS function in vitro, bacteria most likely encounter other T6SS-armed competitors in nature. However, the connection between subcellular details of the T6SS and the outcomes of such mutually lethal battles is not well understood. Here, we incorporate biological data derived from natural competitors of Vibrio fischeri light organ symbionts to build a biochemical model for T6SS at the single-cell level, which we then integrate into an agent-based model (ABM). Using the ABM, we isolate and experiment with strain-specific physiological differences between competitors in ways not possible with biological samples to identify winning strategies for T6SS-armed populations. Through in vitro experiments, we discover that strain-specific differences exist in T6SS activation speed. ABM simulations corroborate that faster activation is dominant in determining survival during competition. Once competitors are fully activated, the energy required for T6SS creates a tipping point where increased weapon building and firing becomes too costly to be advantageous. Through ABM simulations, we identify the threshold where this transition occurs in the T6SS parameter space. We also find that competitive outcomes depend on the geometry of the battlefield: unarmed target cells survive at the edges of a range expansion where unlimited territory can be claimed. Alternatively, competitions within a confined space, much like the light organ crypts where natural V. fischeri compete, result in the rapid elimination of the unarmed population.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2020

Genomics-enabled analysis of specialized metabolism in bioenergy crops: Current progress and challenges

Plants produce a staggering diversity of specialized small molecule metabolites that play vital roles in mediating environmental interactions and stress adaptation. This chemical diversity derives from dynamic biosynthetic pathway networks that are often species-specific and operate under tight spatiotemporal and environmental control. A growing divide between demand and environmental challenges in food and bioenergy crop production have intensified research on these complex metabolite networks and their contribution to crop fitness. High-throughput omics technologies provide access to ever-increasing data resources for investigating plant metabolism. However, the efficiency of using such system-wide data to decode the gene and enzyme functions controlling specialized metabolism has remained limited; due largely to the recalcitrance of many plants to genetic approaches and the lack of ‘user-friendly’ biochemical tools for studying the diverse enzyme classes involved in specialized metabolism. With emphasis on terpenoid metabolism in the bioenergy crop switchgrass as an example, this review aims to illustrate current advances and challenges in the application of DNA synthesis and synthetic biology tools for accelerating the functional discovery of genes, enzymes and pathways in plant specialized metabolism. These technologies have accelerated knowledge development on the biosynthesis and physiological roles of diverse metabolite networks across many ecologically and economically important plant species and can provide resources for application to precision breeding and natural product metabolic engineering.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2021

Mechanistic Evaluation of Black Cohosh Extract-Induced Genotoxicity in Human Cells

Abstract Black cohosh extract (BCE) is marketed to women as an alternative to hormone replacement therapy for alleviating menopausal symptoms. Previous studies by the National Toxicology Program revealed that BCE induced micronuclei (MN) and a nonregenerative macrocytic anemia in rats and mice, likely caused by disruption of the folate metabolism pathway. Additional work using TK6 cells showed that BCE induced aneugenicity by destabilizing microtubules. In the present study, BCE-induced MN were confirmed in TK6 and HepG2 cells. We then evaluated BCE-induced DNA damage using the comet assay at multiple time points (0.5–24 h). Following a 0.5-h exposure, BCE induced significant, concentration-dependent increases in %tail DNA in TK6 cells only. Although DNA damage decreased in TK6 cells over time, likely due to repair, small but statistically significant levels of DNA damage were observed after 2 and 4 h exposures to 250 µg/ml BCE. A G1/S arrest in TK6 cells exposed to 125 µg/ml BCE (24 h) was accompanied by apoptosis and increased expression of γH2A.X, p-Chk1, p-Chk2, p53, and p21. Conditioning TK6 cells to physiological levels of folic acid (120 nM) did not increase the sensitivity of cells to BCE-induced DNA damage. BCE did not alter global DNA methylation in TK6 and HepG2 cells cultured in standard medium. Our results suggest that BCE induces acute DNA strand breaks which are quickly repaired in TK6 cells, whereas DNA damage seen at 4 and 24 h may reflect apoptosis. The present study supports that BCE is genotoxic mainly by inducing MN with an aneugenic mode of action.

Seo, Ji-Eun↗
DOE OSTI2020

Transporters and ascorbate–glutathione metabolism for differential cadmium accumulation and tolerance in two contrasting willow genotypes

Salix matsudana Koidz is a low cadmium (Cd)-accumulating willow, whereas its cultivated variety, Salix matsudana var. matsudana f. umbraculifera Rehd., is a high Cd-accumulating and tolerant willow (HCW). The physiological and molecular mechanisms underlying differential Cd accumulation and tolerance in the two Salix species are poorly understood. In this study, we confirmed that the differential Cd translocation capacity from roots to the shoots leads to the differential Cd accumulation in their aboveground parts between these two willow genotypes. Cadmium accumulation happens preferentially in the transport pathway, and Cd is mainly located in the vacuolar, cell wall and intercellular space in HCW bark by cadmium location analysis at tissue and subcellular levels. Comparative transcriptome analysis revealed that higher expressions of several metal transporter genes (ATP-binding cassette transporters, K + transporters/channels, yellow stripe-like proteins, zinc-regulated transporter/iron-regulated transporter-like proteins, etc.) are involved in root uptake and translocation capacity in HCW; meanwhile, ascorbate–glutathione metabolic pathways play essential roles in Cd detoxification and higher tolerance of the Cd-accumulator HCW. These results lay the foundation for further understanding the molecular mechanisms of Cd accumulation in woody plants and provide new insights into molecular-assisted-screening woody plant varieties for phytoremediation.

59 BASIC BIOLOGICAL SCIENCES↗