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At least 91 records · Page 5
All sourcesNASA NTRSDOE OSTI
DOE OSTI2020

Phonon-mediated lipid raft formation in biological membranes

Short-wavelength collective molecular motions, also known as phonons, have recently attracted much interest in revealing dynamic properties of biological membranes through the use of neutron and x-ray scattering, infrared and Raman spectroscopies, and molecular dynamics simulations. Experimentally detecting unique vibrational patterns such as, shear phonon excitations, viscoelastic crossovers, transverse acoustic phonon gaps, and continuous and truncated optical phonon modes in cellular membranes, to name a few, has proven non-trivial. Here, we review recent advances in liquid thermodynamics that have resulted in the development of the phonon theory of 1 liquids. The theory has important predictions regarding the shear vibrational spectra of fluids, namely the emergence of viscoelastic crossovers and transverse acoustic phonon gaps. Furthermore, we show that these vibrational patterns are common in soft (non-crystalline) materials, including, but not limited to liquids, colloids, liquid crystals (mesogens), block copolymers, and biological membranes. The existence of viscoelastic crossovers and acoustic phonon gaps define the self-diffusion properties of cellular membranes and provide a molecular picture of the transient nature of lipid rafts.1 Importantly, the timescales (picoseconds) for the formation and dissolution of transient lipid rafts match the lifetime of the formation and breakdown of interfacial water hydrogen bonds. Apart from acoustic propagating phonon modes, biological membranes can also support more energetic non-propagating optical phonon excitations, also known as standing waves or breathing modes. Importantly, optical phonons can be truncated due to the existence of finite size nanodomains made up of strongly correlated lipid-cholesterol molecular pairs. These strongly coupled molecular pairs can serve as nucleation centers for the formation of stable rafts at larger length scales, due to correlations of spontaneous fluctuations (Onsager’s regression hypothesis). Finally and importantly, molecular level viscoelastic crossovers, acoustic phonon gaps, and continuous and truncated optical phonon modes may offer insights as to how lipid-lipid and lipid-protein interactions enable biological function.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2022

Caulobacter lipid A is conditionally dispensable in the absence of fur and in the presence of anionic sphingolipids

Lipid A, the membrane-anchored portion of lipopolysaccharide (LPS), is an essential component of the outer membrane (OM) of nearly all Gram-negative bacteria. Here we identify regulatory and structural factors that together render lipid A nonessential in Caulobacter crescentus. Mutations in the ferric uptake regulator fur allow Caulobacter to survive in the absence of either LpxC, which catalyzes an early step of lipid A synthesis, or CtpA, a tyrosine phosphatase homolog we find is needed for wild-type lipid A structure and abundance. Alterations in Fur-regulated processes, rather than iron status per se, underlie the ability to survive when lipid A synthesis is blocked. Fitness of lipid A-deficient Caulobacter requires an anionic sphingolipid, ceramide phosphoglycerate (CPG), which also mediates sensitivity to the antibiotic colistin. Our results demonstrate that, in an altered regulatory landscape, anionic sphingolipids can support the integrity of a lipid A-deficient OM.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2021

Curvature Energetics Determined by Alchemical Simulation on Four Topologically Distinct Lipid Phases

The relative curvature energetics of two lipids are tested using thermodynamic integration (TI) on four topologically distinct lipid phases. Simulations use TI to switch between choline headgroup lipids (POPC; that prefers to be flat) and ethanolamine headgroup lipids (POPE; that prefer, for example, the inner monolayer of vesicles). Here, the thermodynamical moving of the lipids between planar, inverse hexagonal (H II ), cubic (Q II ; Pn3m space group), and vesicle topologies reveals differences in material parameters that were previously challenging to access. The methodology allows for predictions of two important lipid material properties: the difference in POPC/POPE monolayer intrinsic curvature (ΔJ 0 ) and the difference in POPC/POPE monolayer Gaussian curvature modulus (Δ$\bar{κ_m}$), both of which are connected to the energetics of topological variation. Analysis of the TI data indicates that, consistent with previous experiment and simulation, the J 0 of POPE is more negative than POPC (ΔJ 0 = –0.018 ± 0.001 Å –1 ). The theoretical framework extracts significant differences in $\bar{κ_m}$ of which POPE is less negative than POPC by 2.0 to 4.0 kcal/mol. The range of these values is determined by considering subsets of the simulations, and disagreement between these subsets suggests separate mechanical parameters at very high curvature. Finally, the fit of the TI data to the model indicates that the position of the pivotal plane of curvature is not constant across topologies at high curvature. Overall, the results offer insights into lipid material properties, the limits of a single HC model, and how to test them using simulation.

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗
DOE OSTI2025

The Martini 3 Lipidome: Expanded and Refined Parameters Improve Lipid Phase Behavior

Lipid membranes are central to cellular life. Complementing experiments, computational modeling has been essential in unraveling complex lipid-biomolecule interactions, crucial in both academia and industry. The Martini model, a coarse-grained force field for efficient molecular dynamics simulations, is widely used to study membrane phenomena but has faced limitations, particularly in capturing realistic lipid phase behavior. Here, we present refined Martini 3 lipid models with a mapping scheme that distinguishes lipid tails that differ by just two carbon atoms, enhancing the structural resolution and thermodynamic accuracy of model membrane systems including ternary mixtures. The expanded Martini lipid library includes thousands of models, enabling simulations of complex and biologically relevant systems. These advancements establish Martini as a robust platform for lipid-based simulations across diverse fields.

Lipids↗
DOE OSTI2020

Halogenation-Dependent Effects of the Chlorosulfolipids of Ochromonas danica on Lipid Bilayers

The chlorosulfolipids are amphiphilic natural products with stereochemically complex patterns of chlorination and sulfation. Despite their role in toxic shellfish poisoning, potential pharmacological activities, and unknown biological roles, they remain understudied due to the difficulties in purifying them from natural sources. The structure of these molecules, with a charged sulfate group in the middle of the hydrophobic chain, appears incompatible with the conventional lipid bilayer structure. Questions about chlorosulfolipids remain unanswered partly due to the unavailability of structural analogues with which to conduct structure–function studies. Here, we approach this problem by combining enantioselective total synthesis and membrane biophysics. Using a combination of Langmuir pressure–area isotherms of lipid monolayers, fluorescence imaging of vesicles, mass spectrometry imaging, natural product isolation, small-angle X-ray scattering, and cryogenic electron microscopy, we show that danicalipin A (1) likely inserts into lipid bilayers in the headgroup region and alters their structure and phase behavior. Specifically, danicalipin A (1) thins the bilayer and fluidizes it, allowing even saturated lipid to form fluid bilayers. Lipid monolayers show similar fluidizing upon insertion of danicalipin A (1). Furthermore, we show that the halogenation of the molecule is critical for its membrane activity, likely due to sterically controlled conformational changes. Synthetic unchlorinated and monochlorinated analogues do not thin and fluidize lipid bilayers to the same extent as the natural product. Overall, this study sheds light on how amphiphilic small molecules interact with lipid bilayers and the importance of stereochemistry and halogenation for this interaction.

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗
DOE OSTI2023

LipidOz enables automated elucidation of lipid carbon–carbon double bond positions from ozone-induced dissociation mass spectrometry data

Lipids play essential roles in many biological processes and disease pathology, but unambiguous identification of lipids is complicated by the presence of multiple isomeric species differing by fatty acyl chain length, stereospecifically numbered (sn) position, and position/stereochemistry of double bonds. Conventional liquid chromatography-mass spectrometry (LC-MS/MS) analyses enable the determination of fatty acyl chain lengths (and in some cases sn position) and number of double bonds, but not carbon-carbon double bond positions. Ozone-induced dissociation (OzID) is a gas-phase oxidation reaction that produces characteristic fragments from lipids containing double bonds. OzID can be incorporated into ion mobility spectrometry (IMS)-MS instruments for the structural characterization of lipids, including additional isomer separation and confident assignment of double bond positions. The complexity and repetitive nature of OzID data analysis and lack of software tool support have limited the application of OzID for routine lipidomics studies. Here, we present an open-source Python tool, LipidOz, for the automated determination of lipid double bond positions from OzID-IMS-MS data, which employs a combination of traditional automation and deep learning approaches. Our results demonstrate the ability of LipidOz to robustly assign double bond positions for lipid standard mixtures and complex lipid extracts, enabling practical application of OzID for future lipidomics.

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗
DOE OSTI2021

Mechanisms and functions of membrane lipid remodeling in plants

Lipid remodeling, defined herein as post-synthetic structural modifications of membrane lipids, play crucial roles in regulating the physicochemical properties of cellular membranes and hence their many functions. Processes affected by lipid remodeling include lipid metabolism, membrane repair, cellular homeostasis, fatty acid trafficking, cellular signaling and stress tolerance. Glycerolipids are the major structural components of cellular membranes and their composition can be adjusted by modifying their head groups, their acyl chain lengths and the number and position of double bonds. This focused review summarizes recent advances in our understanding of mechanisms of membrane lipid remodeling with emphasis on the lipases and acyltransferases involved in the modification of phosphatidylcholine and monogalactosyldiacylglycerol, the major membrane lipids of extraplastidic and photosynthetic membranes, respectively. We also discuss the role of triacylglycerol metabolism in membrane acyl chain remodeling. Finally, we discuss emerging data concerning the functional roles of glycerolipid remodeling in plant stress responses. Illustrating the molecular basis of lipid remodeling may lead to novel strategies for crop improvement and other biotechnological applications such as bioenergy production.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2021

Catalytic Hydroprocessing of Single-Cell Oils to Hydrocarbon Fuels : Converting microbial lipids to fuels is a promising approach to replace fossil fuels

Microbial lipids hold great promise as biofuel precursors, and research efforts to convert such lipids to renewable diesel fuels have been increasing in recent years. In contrast to the numerous literature reviews on growing, characterising and extracting lipids from oleaginous microbes, and on converting vegetable oils to hydrocarbon fuels, this review aims to provide insight into aspects that are specific to hydroprocessing microbial lipids. While standard hydrotreating catalysts generally perform well with terrestrial oils, differences in lipid speciation and the presence of co-extracted compounds, such as chlorophyll and sterols, introduce additional complexities into the process for microbial lipids. Lipid cleanup steps can be introduced to produce suitable feedstocks for catalytic upgrading.

09 BIOMASS FUELS↗
DOE OSTI2023

Do betaine lipids replace phosphatidylcholine as fatty acid editing hubs in microalgae?

Acyl editing refers to a deacylation and reacylation cycle on a lipid, which allows for fatty acid desaturation and modification prior to being removed and incorporated into other pools. Acyl editing is an important determinant of glycerolipid synthesis and has been well-characterized in land plants, thus this review begins with an overview of acyl editing in plants. Much less is known about acyl editing in algae, including the extent to which acyl editing impacts lipid synthesis and on which lipid substrate(s) it occurs. This review compares what is known about acyl editing on its major hub phosphatidylcholine (PC) in land plants with the evidence for acyl editing of betaine lipids such as diacylglyceryltrimethylhomoserine (DGTS), the structural analog that replaces PC in several species of microalgae. In land plants, PC is also known to be a major source of fatty acids and diacylglycerol (DAG) for synthesis of the neutral lipid triacylglycerol (TAG). We review the evidence that DGTS contributes substantially to TAG accumulation in algae as a source of fatty acids, but not as a precursor to DAG. We conclude with evidence of acyl editing on other membrane lipid substrates in plants and algae apart from PC or DGTS, and discuss future analyses to elucidate the role of DGTS and other betaine lipids in acyl editing in microalgae.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2022

Complex Changes in Membrane Lipids Associated with the Modification of Autophagy in Arabidopsis

Autophagy is a conserved mechanism among eukaryotes that degrades and recycles cytoplasmic components. Autophagy is known to influence the plant metabolome, including lipid content; however, its impact on the plant lipidome is not fully understood, and most studies have analyzed a single or few mutants defective in autophagy. To gain more insight into the effect of autophagy on lipid concentrations and composition, we quantitatively profiled glycerolipids from multiple Arabidopsis thaliana mutants altered in autophagy and compared them with wild-type seedlings under nitrogen replete (+N; normal growth) and nitrogen starvation (−N; autophagy inducing) conditions. Mutants include those in genes of the core autophagy pathway, together with other genes that have been reported to affect autophagy. Using Matrix-Assisted Laser Desorption/Ionization—Mass Spectrometry (MALDI-MS), we imaged the cellular distribution of specific lipids in situ and demonstrated that autophagy and nitrogen treatment did not affect their spatial distribution within Arabidopsis seedling leaves. We observed changes, both increases and decreases, in the relative amounts of different lipid species in the mutants compared to WT both in +N and −N conditions, although more changes were seen in −N conditions. The relative amounts of polyunsaturated and very long chain lipids were significantly reduced in autophagy-disrupted mutants compared to WT plants. Collectively, our results provide additional evidence that autophagy affects plant lipid content and that autophagy likely affects lipid properties such as chain length and unsaturation.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2023

PLAT domain protein 1 (PLAT1/PLAFP) binds to the Arabidopsis thaliana plasma membrane and inserts a lipid

Robust agricultural yields depend on the plant's ability to fix carbon amid variable environmental conditions. Over seasonal and diurnal cycles, the plant must constantly adjust its metabolism according to available resources or external stressors. The metabolic changes that a plant undergoes in response to stress are well understood, but the long-distance signaling mechanisms that facilitate communication throughout the plant are less studied. The phloem is considered the predominant conduit for the bidirectional transport of these signals in the form of metabolites, nucleic acids, proteins, and lipids. Lipid trafficking through the phloem in particular attracted our attention due to its reliance on soluble lipid-binding proteins (LBP) that generate and solubilize otherwise membrane-associated lipids. The Phloem Lipid-Associated Family Protein (PLAFP) from Arabidopsis thaliana is generated in response to abiotic stress as is its lipid-ligand phosphatidic acid (PA). PLAFP is proposed to transport PA through the phloem in response to drought stress. To understand the interactions between PLAFP and PA, nearly 100 independent systems comprised of the protein and one PA, or a plasma membrane containing varying amounts of PA, were simulated using atomistic classical molecular dynamics methods. In these simulations, PLAFP is found to bind to plant plasma membrane models independent of the PA concentration. When bound to the membrane, PLAFP adopts a binding pose where W41 and R82 penetrate the membrane surface and anchor PLAFP. This triggers a separation of the two loop regions containing W41 and R82. Subsequent simulations indicate that PA insert into the β -sandwich of PLAFP, driven by interactions with multiple amino acids besides the W41 and R82 identified during the insertion process. Finally, fine-tuning the protein-membrane and protein-PA interface by mutating a selection of these amino acids may facilitate engineering plant signaling processes by modulating the binding response.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2021

Preserved and variable spatial‐chemical changes of lipids across tomato leaves in response to central vein wounding reveals potential origin of linolenic acid in signal transduction cascade

Abstract Membrane lipids serve as substrates for the generation of numerous signaling lipids when plants are exposed to environmental stresses, and jasmonic acid, an oxidized product of 18‐carbon unsaturated fatty acids (e.g., linolenic acid), has been recognized as the essential signal in wound‐induced gene expression. Yet, the contribution of individual membrane lipids in linolenic acid generation is ill‐defined. In this work, we performed spatial lipidomic experiments to track lipid changes that occur locally at the sight of leaf injury to better understand the potential origin of linolenic and linoleic acids from individual membrane lipids. The central veins of tomato leaflets were crushed using surgical forceps, leaves were cryosectioned and analyzed by two orthogonal matrix‐assisted laser desorption/ionization mass spectrometry imaging platforms for insight into lipid spatial distribution. Significant changes in lipid composition are only observed 30 min after wounding, while after 60 min lipidome homeostasis has been re‐established. Phosphatidylcholines exhibit a variable pattern of spatial behavior in individual plants. Among lysolipids, lysophosphatidylcholines strongly co‐localize with the injured zone of wounded leaflets, while, for example, lysophosphatidylglycerol (LPG) (16:1) accumulated preferentially toward the apex in the injured zone of wounded leaflets. In contrast, two other LPGs (LPG [18:3] and LPG [18:2]) are depleted in the injured zone. Our high‐resolution co‐localization imaging analyses suggest that linolenic acids are predominantly released from PCs with 16_18 fatty acid composition along the entire leaf, while it seems that in the apex zone PG (16:1_18:3) significantly contributes to the linolenic acid pool. These results also indicate distinct localization and/or substrate preferences of phospholipase isoforms in leaf tissue.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2020

Improving biomass and lipid yields of Desmodesmus armatus and Chlorella vulgaris through mutagenesis and high-throughput screening

Advancement of microalgae for use as biofuel feedstock depends on bioprospecting novel strains and then applying classical strain improvement techniques to enhance desirable traits. Here we successfully demonstrate this approach using two novel strains of green algae, identified as Desmodesmus armatus and Chlorella vulgaris, to improve biomass and lipid yields. UV irradiation was utilized to generate random mutations and the resulting populations were analyzed via flow cytometry to quantify lipid fluorescence while enriching for high lipid variants using fluorescence activated cell sorting. Secondary screening was performed via in situ fluorescence staining to identify the single highest lipid producing mutants from each strain. This approach produced a Desmodesmus armatus mutant that exhibited both increased biomass productivity and higher lipid content, which doubled lipid yield from the culture. The resulting Chlorella vulgaris mutant exhibited an increase in growth only, resulting in a 33% increase in lipid yield.

09 BIOMASS FUELS↗
DOE OSTI2026

KRAS4a and KRAS4b show distinct lipid-dependent regulation of RAS-RAF membrane dynamics

KRAS4a and KRAS4b are important regulators of signaling, and their interactions with the plasma membrane are dynamic and influenced by lipid composition. KRAS 4a and 4b have nearly identical globular domains but differ in their membrane-associated hyper variable region (HVR). The functional distinctions between these isoforms remain unclear, particularly with regards to their dependence on specific lipids and the membrane environment. Previous work showed that the membrane orientation of KRAS4b affects its ability to bind to RAF kinase RBDCRD and that the KRAS–RBDCRD complex adopts different poses on the membrane as well as influences the size and composition of the lipid environment. To model differences between KRAS 4a and 4b protein–lipid interactions, we extended the Multiscale Machine-Learned Modeling Infrastructure (MuMMI) to incorporate continuum simulations in the grand canonical ensemble, enabling sampling across macroscopic, coarse-grained, and all-atom resolutions. Using this framework, we systematically altered PIP2 concentrations, KRAS 4a versus 4b, and RAF RBDCRD complexation to assess impacts on membrane–protein interactions and dynamics. Our results reveal that reducing PIP2 shifts and broadens the membrane orientational preference of both KRAS 4b and 4a, with stronger effects on 4b HVR localization versus 4a. We demonstrate that with depletion of the strong negatively charged PIP2 lipid, the less charged phosphatidylserine replaces PIP2. Our findings highlight similarities and distinctions in the dynamics and lipid dependency of KRAS isoforms and suggest that ordering of the local lipid composition by HVRs is a shared property and key modulator of RAS-mediated signaling at the plasma membrane.

Biological and medical sciences↗
DOE OSTI2024

Improved lipid analysis using a 2D-LC-MS system with a novel injection procedure

The aim of this study was to improve analysis of nonpolar lipidomics sample extracts using reversed phase (RP) chromatography. A 4/3/3 (v/v/v) mixture of methanol/methyl tert-butyl ether/chloroform (MeOH/MTBE/CHCl 3 , MMC) was chosen for sample extraction solvent based on its proven extraction capability for several lipid classes. To avoid carry over, loss of analytes and peak distortion the loops and all capillaries of the presented LC system were flushed and filled up with methanol until the analytical column. Here, the choice of methanol was due to its weak elution strength and being infinitely miscible with MMC and several other nonpolar solvents. This allowed injection of a 100 μl sample that was 20 μl nonpolar extraction solvent diluted fivefold with methanol. All lipids of 25 lipid classes were transferred quantitatively to the column head where the online dilution of methanol was carried out with aqueous eluent for focusing the lipid analytes. The weak elution strength of methanol prevented peak distortions. The consecutive reversed phase elution resulted in remarkably narrow peaks (full width at half maximum was 0.07–0.08 min typically) and enhanced sensitivity (limit of detection usually in sub nM region) because of increased sample injection volume and narrow peaks. Calibration and quality control samples made by diluting commercial lipid standards 200–50000 times confirmed the applicability of this approach both for targeted lipid quantification and for untargeted quantitative comparison of lipids from different sources.

46 INSTRUMENTATION RELATED TO NUCLEAR SCIENCE AND ↗
DOE OSTI2024

Economic and environmental bottlenecks in the industrial‐scale production of lipid‐derived biofuels from oleaginous yeasts: A review of the current trends and future prospects

Abstract Concerns about climate change and the reliance on fossil fuel reserves have motivated researchers to identify new renewable sources of energy. Biomass holds the potential to replace fossil‐derived products with biofuels and bio‐based chemicals. Plant‐derived lipids are promising sources of biofuels; however, the production of plant oil often leads to the release of massive amounts of carbon dioxide due to deforestation and land‐use change. The production of biofuels via plant oils (such as soybean) also competes with food production and in turn, impacts biodiversity. To mitigate these issues, the production of lipids from oleaginous yeasts could be an excellent alternative by incorporating these microbes into biorefineries utilizing agricultural or forest residues. Eventually, these microbial lipids could be potential sources for producing lipid‐derived biofuels. However, the current conventional methods for the production and recovery of lipids from oleaginous microbes suffer from economic and ecological challenges that affect its industrial‐scale expansion. This review highlights the major economic and environmental bottlenecks for the production of lipid‐derived biofuels from oleaginous yeasts. It also provides perspectives on the strategies that could be adapted on economic and ecological fronts to assist the expansion of the production of microbial lipid‐derived biofuels at an industrial scale.

Agriculture↗
DOE OSTI2021

Electromechanics of lipid-modulated gating of potassium channels

Experimental studies reveal that the anionic lipid phosphatidic acid (POPA), non-phospholipid cholesterol, and cationic lipid DOTAP inhibit the gating of voltage-sensitive potassium (Kv) channels. In this work, we develop a continuum electromechanical model to investigate the interaction of these lipids with the ion channel. Our model suggests that: (i) POPA lipids may restrict the vertical motion of the voltage-sensor domain through direct electrostatic interactions; (ii) cholesterol may oppose the radial motion of the pore domain of the channel by increasing the mechanical rigidity of the membrane; and (iii) DOTAP can reduce the effect of electrostatic forces by regulating the dielectric constant at the channel–lipid interface. The electromechanical model predictions for the three lipid types match well with the experimental observations and provide mechanistic insights into lipid-dependent gating of Kv channels.

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗
DOE OSTI2023

Data for Application of Time-Domain 1H NMR for Investigating Dynamics of Vegetative Lipids in Bioenergy Crops at Different Developmental Stages

Sweet sorghum is typically cultivated for the food and fodder market. Recently, sweet sorghum varieties are being metabolically transitioned to enhance energy density by accumulating oil droplets in their vegetative tissues for bioenergy applications. Owing to the high biomass yield of sorghum, the transgenic lines can compete with oil-seed crops for biodiesel yield per unit area. In the initial phase of transgenic development, a high-throughput phenotyping method can bridge the gap between the production pipeline and analysis to improve the efficiency of the process. To meet the requirement, the present study extends the application of time-domain 1H-NMR spectroscopy for rapid quantification and characterization of the total in-situ lipids of sweet sorghum ‘ramada’ to lay the groundwork for analyzing the upcoming large quantity of transgenic samples. NMR technology has been successfully established for analyzing lipid contents of vegetative tissues of non-transgenic variety. The multiexponential analysis of spin-lattice (T1) relaxation spectra obtained from TD-NMR aided the investigation of the dynamics of the free and bound lipid fraction with plant development. The total lipid concentration of bagasse and leaves of non-transgenic sweet sorghum remained unchanged throughout the plant development. Leaves displayed a higher percentage of bound lipids as compared to bagasse. A significant variation in the lipid concentration of juice was observed at the different growth stages with a maximum lipid accumulation of 1.21 ± 0.04% w/w at the boot stage that decreased with further maturity of the plant.

Biomass Analytics↗