Publications by authors named "Albert Batushansky"

28 Publications

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Fundamentals of OA. An initiative of Osteoarthritis and Cartilage. Chapter 9: Obesity and metabolic factors in OA.

Osteoarthritis Cartilage 2021 Sep 16. Epub 2021 Sep 16.

Aging and Metabolism Research Program, Oklahoma Medical Research Foundation, Oklahoma City, OK, USA, 73104; Reynolds Oklahoma Center on Aging, Department of Biochemistry and Molecular Biology, Department of Physiology, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA, 73104; Veterans Affairs Medical Center, Oklahoma City, OK, USA, 73104. Electronic address:

Objective: Obesity was once considered a risk factor for knee osteoarthritis (OA) primarily for biomechanical reasons. Here we provide an additional perspective by discussing how obesity also increases OA risk by altering metabolism and inflammation.

Design: This narrative review is presented in four sections: 1) metabolic syndrome and OA, 2) metabolic biomarkers of OA, 3) evidence for dysregulated chondrocyte metabolism in OA, and 4) metabolic inflammation: joint tissue mediators and mechanisms.

Results: Metabolic syndrome and its components are strongly associated with OA. However, evidence for a causal relationship is context dependent, varying by joint, gender, diagnostic criteria, and demographics, with additional environmental and genetic interactions yet to be fully defined. Importantly, some aspects of the etiology of obesity-induced OA appear to be distinct between men and women, especially regarding the role of adipose tissue. Metabolomic analyses of serum and synovial fluid have identified potential diagnostic biomarkers of knee OA and prognostic biomarkers of disease progression. Connecting these biomarkers to cellular pathophysiology will require future in vivo studies of joint tissue metabolism. Such studies will help reveal when a metabolic process or a metabolite itself is a causal factor in disease progression. Current evidence points towards impaired chondrocyte metabolic homeostasis and metabolic-immune dysregulation as likely factors connecting obesity to the increased risk of OA.

Conclusions: A deeper understanding of how obesity alters metabolic and inflammatory pathways in synovial joint tissues is expected to provide new therapeutic targets and an improved definition of "metabolic" and "obesity" OA phenotypes.
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http://dx.doi.org/10.1016/j.joca.2021.06.013DOI Listing
September 2021

PFKFB3-dependent glucose metabolism regulates 3T3-L1 adipocyte development.

FASEB J 2021 07;35(7):e21728

Department of Biochemistry & Molecular Biology, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA.

Proliferation and differentiation of preadipocytes, and other cell types, is accompanied by an increase in glucose uptake. Previous work showed that a pulse of high glucose was required during the first 3 days of differentiation in vitro, but was not required after that. The specific glucose metabolism pathways required for adipocyte differentiation are unknown. Herein, we used 3T3-L1 adipocytes as a model system to study glucose metabolism and expansion of the adipocyte metabolome during the first 3 days of differentiation. Our primary outcome measures were GLUT4 and adiponectin, key proteins associated with healthy adipocytes. Using complete media with 0 or 5 mM glucose, we distinguished between developmental features that were dependent on the differentiation cocktail of dexamethasone, insulin, and isobutylmethylxanthine alone or the cocktail plus glucose. Cocktail alone was sufficient to activate the capacity for 2-deoxglucose uptake and glycolysis, but was unable to support the expression of GLUT4 and adiponectin in mature adipocytes. In contrast, 5 mM glucose in the media promoted a transient increase in glucose uptake and glycolysis as well as a significant expansion of the adipocyte metabolome and proteome. Using genetic and pharmacologic approaches, we found that the positive effects of 5 mM glucose on adipocyte differentiation were specifically due to increased expression of 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase 3 (PFKFB3), a key regulator of glycolysis and the ancillary glucose metabolic pathways. Our data reveal a critical role for PFKFB3 activity in regulating the cellular metabolic remodeling required for adipocyte differentiation and maturation.
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http://dx.doi.org/10.1096/fj.202100381RRDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8205188PMC
July 2021

Sirt5 Deficiency Causes Posttranslational Protein Malonylation and Dysregulated Cellular Metabolism in Chondrocytes Under Obesity Conditions.

Cartilage 2021 Feb 11:1947603521993209. Epub 2021 Feb 11.

Aging and Metabolism Research Program, Oklahoma Medical Research Foundation, Oklahoma City, OK, USA.

Objective: Obesity accelerates the development of osteoarthritis (OA) during aging and is associated with altered chondrocyte cellular metabolism. Protein lysine malonylation (MaK) is a posttranslational modification (PTM) that has been shown to play an important role during aging and obesity. The objective of this study was to investigate the role of sirtuin 5 (Sirt5) in regulating MaK and cellular metabolism in chondrocytes under obesity-related conditions.

Methods: MaK and SIRT5 were immunostained in knee articular cartilage of obese mice and different aged C57BL6 mice with or without destabilization of the medial meniscus surgery to induce OA. Primary chondrocytes were isolated from 7-day-old WT and mice and treated with varying concentrations of glucose and insulin to mimic obesity. Sirt5-dependent effects on MaK and metabolism were evaluated by western blot, Seahorse Respirometry, and gas/chromatography-mass/spectrometry (GC-MS) metabolic profiling.

Results: MaK was significantly increased in cartilage of mice and in chondrocytes treated with high concentrations of glucose and insulin (GluIns). Sirt5 was increased in an age-dependent manner following joint injury, and Sirt5 deficient primary chondrocytes had increased MaK, decreased glycolysis rate, and reduced basal mitochondrial respiration. GC-MS identified 41 metabolites. Sirt5 deficiency altered 13 distinct metabolites under basal conditions and 18 metabolites under GluIns treatment. Pathway analysis identified a wide range of Sirt5-dependent altered metabolic pathways that include amino acid metabolism, TCA cycle, and glycolysis.

Conclusion: This study provides the first evidence that Sirt5 broadly regulates chondrocyte metabolism. We observed changes in SIRT5 and MaK levels in cartilage with obesity and joint injury, suggesting that the Sirt5-MaK pathway may contribute to altered chondrocyte metabolism that occurs during OA development.
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http://dx.doi.org/10.1177/1947603521993209DOI Listing
February 2021

Proximal colon-derived O-glycosylated mucus encapsulates and modulates the microbiota.

Science 2020 10;370(6515):467-472

Cardiovascular Biology Research Program, Oklahoma Medical Research Foundation, Oklahoma City, OK 73104, USA.

Colon mucus segregates the intestinal microbiota from host tissues, but how it organizes to function throughout the colon is unclear. In mice, we found that colon mucus consists of two distinct O-glycosylated entities of Muc2: a major form produced by the proximal colon, which encapsulates the fecal material including the microbiota, and a minor form derived from the distal colon, which adheres to the major form. The microbiota directs its own encapsulation by inducing Muc2 production from proximal colon goblet cells. In turn, O-glycans on proximal colon-derived Muc2 modulate the structure and function of the microbiota as well as transcription in the colon mucosa. Our work shows how proximal colon control of mucin production is an important element in the regulation of host-microbiota symbiosis.
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http://dx.doi.org/10.1126/science.aay7367DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8132455PMC
October 2020

A Shift in Glycerolipid Metabolism Defines the Follicular Fluid of IVF Patients with Unexplained Infertility.

Biomolecules 2020 07 31;10(8). Epub 2020 Jul 31.

The Institute for Drug Research, The Hebrew University of Jerusalem, Jerusalem 9112102, Israel.

Follicular fluid (FF) constitutes the microenvironment of the developing oocyte. We recently characterized its lipid composition and found lipid signatures of positive pregnancy outcome after in vitro fertilization (IVF). In the current study, we aimed to test the hypothesis that unexplained female infertility is related to lipid metabolism, given the lipid signature of positive-outcome IVF patients we previously found. Assuming that FF samples from IVF patients with male factor infertility can represent a non-hindered metabolic microenvironment, we compared them to FF taken from women with unexplained infertility. FF from patients undergoing IVF was examined for its lipid composition. We found highly increased triacylglycerol levels, with a lower abundance of monoacylglycerols, phospholipids and sphingolipids in the FF of patients with unexplained infertility. The alterations in the lipid class accumulation were independent of the body mass index (BMI) and were altogether kept across the age groups. Potential lipid biomarkers for pregnancy outcomes showed a highly discriminative abundance in the FF of unexplained infertility patients. Lipid abundance distinguished IVF patients with unrecognized infertility and provided a potential means for the evaluation of female fertility.
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http://dx.doi.org/10.3390/biom10081135DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7465802PMC
July 2020

Correlation network analysis shows divergent effects of a long-term, high-fat diet and exercise on early stage osteoarthritis phenotypes in mice.

J Sport Health Sci 2020 03 24;9(2):119-131. Epub 2019 May 24.

Aging and Metabolism Research Program, Oklahoma Medical Research Foundation (OMRF), Oklahoma City, OK 73104, USA.

Background: Obesity increases knee osteoarthritis (OA) risk through metabolic, inflammatory, and biomechanical factors, but how these systemic and local mediators interact to drive OA pathology is not well understood. We tested the effect of voluntary running exercise after chronic diet-induced obesity on knee OA-related cartilage and bone pathology in mice. We then used a correlation-based network analysis to identify systemic and local factors associated with early-stage knee OA phenotypes among the different diet and exercise groups.

Methods: Male C57BL/6J mice were fed a defined control (10% kcal fat) or high fat (HF) (60% kcal fat) diet from 6 to 37 weeks of age. At 25 weeks, one-half of the mice from each diet group were housed in cages with running wheels for the remainder of the study. Histology, micro computed tomography, and magnetic resonance imaging were used to evaluate changes in joint tissue structure and OA pathology. These local variables were then compared to systemic metabolic (body mass, body fat, and glucose tolerance), inflammatory (serum adipokines and inflammatory mediators), and functional (mechanical tactile sensitivity and grip strength) outcomes using a correlation-based network analysis. Diet and exercise effects were evaluated by two-way analysis of variance.

Results: An HF diet increased the infrapatellar fat pad size and posterior joint osteophytes, and wheel running primarily altered the subchondral cortical and trabecular bone. Neither HF diet nor exercise altered average knee cartilage OA scores compared to control groups. However, the coefficient of variation was ≥25% for many outcomes, and some mice in both diet groups developed moderate OA (≥33% maximum score). This supported using correlation-based network analyses to identify systemic and local factors associated with early-stage knee OA phenotypes. In wheel-running cohorts, an HF diet reduced the network size compared to the control diet group despite similar running distances, suggesting that diet-induced obesity dampens the effects of exercise on systemic and local OA-related factors. Each of the 4 diet and activity groups showed mostly unique networks of local and systemic factors correlated with early-stage knee OA.

Conclusion: Despite minimal group-level effects of chronic diet-induced obesity and voluntary wheel running on knee OA pathology under the current test durations, diet and exercise substantially altered the relationships among systemic and local variables associated with early-stage knee OA. These results suggest that distinct pre-OA phenotypes may exist prior to the development of disease.
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http://dx.doi.org/10.1016/j.jshs.2019.05.008DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7031811PMC
March 2020

Can metabolic tightening and expansion of co-expression network play a role in stress response and tolerance?

Plant Sci 2020 Apr 10;293:110409. Epub 2020 Jan 10.

Division of Biological Sciences, Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, MO, 65201, USA. Electronic address:

Plants respond and adapt to changes in their environment by employing a wide variety of genetic, molecular, and biochemical mechanisms. When so doing, they trigger large-scale rearrangements at the metabolic and transcriptional levels. The dynamics and patterns of these rearrangements and how they govern a stress response is not clear. In this opinion, we discuss a plant's response to stress from the perspective of the metabolic gene co-expression network and its rearrangement upon stress. As a case study, we use publicly available expression data of Arabidopsis thaliana plants exposed to heat and drought stress to evaluate and compare the co-expression networks of metabolic genes. The analysis highlights that stress conditions can lead to metabolic tightening and expansion of the co-expression network. We argue that this rearrangement could play a role in a plant's response to stress and thus may be an additional tool to assess and understand stress tolerance/sensitivity. Additional studies are needed to evaluate the metabolic network in response to multiple stresses at various intensities and across different genetic backgrounds (e.g., intra- and inter-species, sensitive and tolerant eco/genotypes).
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http://dx.doi.org/10.1016/j.plantsci.2020.110409DOI Listing
April 2020

The complex response of free and bound amino acids to water stress during the seed setting stage in Arabidopsis.

Plant J 2020 05 5;102(4):838-855. Epub 2020 Feb 5.

Division of Biological Sciences, Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, MO, 65211, USA.

Free amino acids (FAAs) and protein-bound amino acids (PBAAs) in seeds play an important role in seed desiccation, longevity, and germination. However, the effect that water stress has on these two functional pools, especially when imposed during the crucial seed setting stage is unclear. To better understand these effects, we exposed Arabidopsis plants at the seed setting stage to a range of water limitation and water deprivation conditions and then evaluated physiological, metabolic, and proteomic parameters, with special focus on FAAs and PBAAs. We found that in response to severe water limitation, seed yield decreased, while seed weight, FAA, and PBAA content per seed increased. Nevertheless, the composition of FAAs and PBAAs remained unaltered. In response to severe water deprivation, however, both seed yield and weight were reduced. In addition, major alterations were observed in both FAA and proteome compositions, which indicated that both osmotic adjustment and proteomic reprogramming occurred in these naturally desiccation-tolerant organs. However, despite the major proteomic alteration, the PBAA composition did not change, suggesting that the proteomic reprogramming was followed by a proteomic rebalancing. Proteomic rebalancing has not been observed previously in response to stress, but its occurrence under stress strongly suggests its natural function. Together, our data show that the dry seed PBAA composition plays a key role in seed fitness and therefore is rigorously maintained even under severe water stress, while the FAA composition is more plastic and adaptable to changing environments, and that both functional pools are distinctly regulated.
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http://dx.doi.org/10.1111/tpj.14668DOI Listing
May 2020

Enhancing cardiac glycolysis causes an increase in PDK4 content in response to short-term high-fat diet.

J Biol Chem 2019 11 27;294(45):16831-16845. Epub 2019 Sep 27.

Aging and Metabolism Research Program, Oklahoma Medical Research Foundation, Oklahoma City, Oklahoma 73104

The healthy heart has a dynamic capacity to respond and adapt to changes in nutrient availability. Metabolic inflexibility, such as occurs with diabetes, increases cardiac reliance on fatty acids to meet energetic demands, and this results in deleterious effects, including mitochondrial dysfunction, that contribute to pathophysiology. Enhancing glucose usage may mitigate metabolic inflexibility and be advantageous under such conditions. Here, we sought to identify how mitochondrial function and cardiac metabolism are affected in a transgenic mouse model of enhanced cardiac glycolysis (Glyco) basally and following a short-term (7-day) high-fat diet (HFD). Glyco mice constitutively express an active form of phosphofructokinase-2, resulting in elevated levels of the PFK-1 allosteric activator fructose 2,6-bisphosphate. We report that basally Glyco mitochondria exhibit augmented pyruvate-supported respiration relative to fatty acids. Nevertheless, both WT and Glyco mitochondria had a similar shift toward increased rates of fatty acid-supported respiration following HFD. Metabolic profiling by GC-MS revealed distinct features based on both genotype and diet, with a unique increase in branched-chain amino acids in the Glyco HFD group. Targeted quantitative proteomics analysis also supported both genotype- and diet-dependent changes in protein expression and uncovered an enhanced expression of pyruvate dehydrogenase kinase 4 (PDK4) in the Glyco HFD group. These results support a newly identified mechanism whereby the levels of fructose 2,6-bisphosphate promote mitochondrial PDK4 levels and identify a secondary adaptive response that prevents excessive mitochondrial pyruvate oxidation when glycolysis is sustained after a high-fat dietary challenge.
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http://dx.doi.org/10.1074/jbc.RA119.010371DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6851294PMC
November 2019

GC-MS metabolic profiling reveals fructose-2,6-bisphosphate regulates branched chain amino acid metabolism in the heart during fasting.

Metabolomics 2019 01 28;15(2):18. Epub 2019 Jan 28.

Aging and Metabolism Research Program, Oklahoma Medical Research Foundation, Oklahoma City, OK, 73104, US.

Introduction: As an insulin sensitive tissue, the heart decreases glucose usage during fasting. This response is mediated, in part, by decreasing phosphofructokinase-2 (PFK-2) activity and levels of its product fructose-2,6-bisphosphate. However, the importance of fructose-2,6-bisphosphate in the fasting response on other metabolic pathways has not been evaluated.

Objectives: The goal of this study is to determine how sustaining cardiac fructose-2,6-bisphosphate levels during fasting affects the metabolomic profile.

Methods: Control and transgenic mice expressing a constitutively active form of PFK-2 (Glyco) were subjected to either 12-h fasting or regular feeding. Animals (n = 4 per group) were used for whole-heart extraction, followed by gas chromatography-mass spectrometry metabolic profiling and multivariate data analysis.

Results: Principal component analysis displayed differences between Control and Glyco groups under both fasting and fed conditions while a clear response to fasting was observed only for Control animals. However, pathway analysis revealed that these smaller changes in the Glyco group were significantly associated with branched-chain amino acid (BCAA) metabolism (~ 40% increase in all BCAAs). Correlation network analysis demonstrated clear differences in response to fasting between Control and Glyco groups amongst most parameters. Notably, fasting caused an increase in network density in the Control group from 0.12 to 0.14 while the Glyco group responded oppositely (0.17-0.15).

Conclusions: Elevated cardiac PFK-2 activity during fasting selectively increases BCAAs levels and decreases global changes in metabolism.
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http://dx.doi.org/10.1007/s11306-019-1478-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6478396PMC
January 2019

Adaptive responses of amino acid metabolism to the combination of desiccation and low nitrogen availability in Sporobolus stapfianus.

Planta 2019 May 6;249(5):1535-1549. Epub 2019 Feb 6.

Division of Biological Sciences, Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, MO, 65311, USA.

Main Conclusion: Depending on nitrogen availability, S. stapfianus uses different amino acid metabolism strategies to cope with desiccation stress. The different metabolic strategies support essential processes for the desiccation tolerance phenotype. To provide a comprehensive assessment of the role played by amino acids in the adaptation of Sporobolus stapfianus to a combination of desiccation and nitrogen limitation, we used an absolute quantification of free and protein-bound amino acids (FAAs and PBAAs) as well as their gamma-glutamyl (gg-AA) derivatives in four different tissues grown under high- and low-nitrogen regimes. We demonstrate that although specific FAAs and gg-AAs increased in desiccating immature leaves under both nitrogen regimes, the absolute change in the total amount of either is small or negligible, negating their proposed role in nitrogen storage. FAAs and PBAAs decrease in underground tissues during desiccation, when nitrogen is abundant. In contrast, PBAAs are drastically reduced from the mature leaves, when nitrogen is limiting. Nevertheless, the substantial reduction in PBAA and FAA fractions in both treatments is not manifested in the immature leaves, which strongly suggests that these amino acids are further metabolized to fuel central metabolism or other metabolic adjustments that are essential for the acquisition of desiccation tolerance (DT).
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http://dx.doi.org/10.1007/s00425-019-03105-6DOI Listing
May 2019

Independent effects of dietary fat and sucrose content on chondrocyte metabolism and osteoarthritis pathology in mice.

Dis Model Mech 2018 08 31;11(9). Epub 2018 Aug 31.

Aging and Metabolism Research Program, Oklahoma Medical Research Foundation (OMRF), Oklahoma City, OK 73104, USA

Obesity is one of the most significant risk factors for knee osteoarthritis. However, therapeutic strategies to prevent or treat obesity-associated osteoarthritis are limited because of uncertainty about the etiology of disease, particularly with regard to metabolic factors. High-fat-diet-induced obese mice have become a widely used model for testing hypotheses about how obesity increases the risk of osteoarthritis, but progress has been limited by variation in disease severity, with some reports concluding that dietary treatment alone is insufficient to induce osteoarthritis in mice. We hypothesized that increased sucrose content of typical low-fat control diets contributes to osteoarthritis pathology and thus alters outcomes when evaluating the effects of a high-fat diet. We tested this hypothesis in male C57BL/6J mice by comparing the effects of purified diets that independently varied sucrose or fat content from 6 to 26 weeks of age. Outcomes included osteoarthritis pathology, serum metabolites, and cartilage gene and protein changes associated with cellular metabolism and stress-response pathways. We found that the relative content of sucrose versus cornstarch in low-fat iso-caloric purified diets caused substantial differences in serum metabolites, joint pathology, and cartilage metabolic and stress-response pathways, despite no differences in body mass or body fat. We also found that higher dietary fat increased fatty acid metabolic enzymes in cartilage. The findings indicate that the choice of control diets should be carefully considered in mouse osteoarthritis studies. Our study also indicates that altered cartilage metabolism might be a contributing factor to how diet and obesity increase the risk of osteoarthritis.
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http://dx.doi.org/10.1242/dmm.034827DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6176996PMC
August 2018

Topological Data Analysis as a Morphometric Method: Using Persistent Homology to Demarcate a Leaf Morphospace.

Front Plant Sci 2018 25;9:553. Epub 2018 Apr 25.

Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT, United States.

Current morphometric methods that comprehensively measure shape cannot compare the disparate leaf shapes found in seed plants and are sensitive to processing artifacts. We explore the use of persistent homology, a topological method applied as a filtration across simplicial complexes (or more simply, a method to measure topological features of spaces across different spatial resolutions), to overcome these limitations. The described method isolates subsets of shape features and measures the spatial relationship of neighboring pixel densities in a shape. We apply the method to the analysis of 182,707 leaves, both published and unpublished, representing 141 plant families collected from 75 sites throughout the world. By measuring leaves from throughout the seed plants using persistent homology, a defined morphospace comparing all leaves is demarcated. Clear differences in shape between major phylogenetic groups are detected and estimates of leaf shape diversity within plant families are made. The approach predicts plant family above chance. The application of a persistent homology method, using topological features, to measure leaf shape allows for a unified morphometric framework to measure plant form, including shapes, textures, patterns, and branching architectures.
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http://dx.doi.org/10.3389/fpls.2018.00553DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5996898PMC
April 2018

Paclobutrazol induces tolerance in tomato to deficit irrigation through diversified effects on plant morphology, physiology and metabolism.

Sci Rep 2016 12 22;6:39321. Epub 2016 Dec 22.

Jacob Blaustein Institutes for Desert Research, Sede Boqer Campus, Ben-Gurion University of the Negev, Israel.

Dwindling water resources combined with meeting the demands for food security require maximizing water use efficiency (WUE) both in rainfed and irrigated agriculture. In this regard, deficit irrigation (DI), defined as the administration of water below full crop-water requirements (evapotranspiration), is a valuable practice to contain irrigation water use. In this study, the mechanism of paclobutrazol (Pbz)-mediated improvement in tolerance to water deficit in tomato was thoroughly investigated. Tomato plants were subjected to normal irrigated and deficit irrigated conditions plus Pbz application (0.8 and 1.6 ppm). A comprehensive morpho-physiological, metabolomics and molecular analysis was undertaken. Findings revealed that Pbz application reduced plant height, improved stem diameter and leaf number, altered root architecture, enhanced photosynthetic rates and WUE of tomato plants under deficit irrigation. Pbz differentially induced expression of genes and accumulation of metabolites of the tricarboxylic acid (TCA) cycle, γ-aminobutyric acid (GABA-shunt pathway), glutathione ascorbate (GSH-ASC)-cycle, cell wall and sugar metabolism, abscisic acid (ABA), spermidine (Spd) content and expression of an aquaporin (AP) protein under deficit irrigation. Our results suggest that Pbz application could significantly improve tolerance in tomato plants under limited water availability through selective changes in morpho-physiology and induction of stress-related molecular processes.
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http://dx.doi.org/10.1038/srep39321DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5177942PMC
December 2016

Environmental and genetic effects on tomato seed metabolic balance and its association with germination vigor.

BMC Genomics 2016 12 19;17(1):1047. Epub 2016 Dec 19.

The French Associates Institute for Agriculture and Biotechnology of Dryland, the Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede Boqer Campus, Midreshet Ben Gurion, 84990, Israel.

Background: The metabolite content of a seed and its ability to germinate are determined by genetic makeup and environmental effects during development. The interaction between genetics, environment and seed metabolism and germination was studied in 72 tomato homozygous introgression lines (IL) derived from Solanum pennelli and S. esculentum M82 cultivar. Plants were grown in the field under saline and fresh water irrigation during two consecutive seasons, and collected seeds were subjected to morphological analysis, gas chromatograph-mass spectrometry (GC-MS) metabolic profiling and germination tests.

Results: Seed weight was under tight genetic regulation, but it was not related to germination vigor. Salinity significantly reduced seed number but had little influence on seed metabolites, affecting only 1% of the statistical comparisons. The metabolites negatively correlated to germination were simple sugars and most amino acids, while positive correlations were found for several organic acids and the N metabolites urea and dopamine. Germination tests identified putative loci for improved germination as compared to M82 and in response to salinity, which were also characterized by defined metabolic changes in the seed.

Conclusions: An integrative analysis of the metabolite and germination data revealed metabolite levels unambiguously associated with germination percentage and rate, mostly conserved in the different tested seed development environments. Such consistent relations suggest the potential for developing a method of germination vigor prediction by metabolic profiling, as well as add to our understanding of the importance of primary metabolic processes in germination.
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http://dx.doi.org/10.1186/s12864-016-3376-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5168813PMC
December 2016

Network-Guided GWAS Improves Identification of Genes Affecting Free Amino Acids.

Plant Physiol 2017 01 21;173(1):872-886. Epub 2016 Nov 21.

Division of Biological Sciences, University of Missouri, Columbia, Missouri 65211 (R.A., A.B.).

Amino acids are essential for proper growth and development in plants. Amino acids serve as building blocks for proteins but also are important for responses to stress and the biosynthesis of numerous essential compounds. In seed, the pool of free amino acids (FAAs) also contributes to alternative energy, desiccation, and seed vigor; thus, manipulating FAA levels can significantly impact a seed's nutritional qualities. While genome-wide association studies (GWAS) on branched-chain amino acids have identified some regulatory genes controlling seed FAAs, the genetic regulation of FAA levels, composition, and homeostasis in seeds remains mostly unresolved. Hence, we performed GWAS on 18 FAAs from a 313-ecotype Arabidopsis (Arabidopsis thaliana) association panel. Specifically, GWAS was performed on 98 traits derived from known amino acid metabolic pathways (approach 1) and then on 92 traits generated from an unbiased correlation-based metabolic network analysis (approach 2), and the results were compared. The latter approach facilitated the discovery of additional novel metabolic interactions and single-nucleotide polymorphism-trait associations not identified by the former approach. The most prominent network-guided GWAS signal was for a histidine (His)-related trait in a region containing two genes: a cationic amino acid transporter (CAT4) and a polynucleotide phosphorylase resistant to inhibition with fosmidomycin. A reverse genetics approach confirmed CAT4 to be responsible for the natural variation of His-related traits across the association panel. Given that His is a semiessential amino acid and a potent metal chelator, CAT4 orthologs could be considered as candidate genes for seed quality biofortification in crop plants.
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http://dx.doi.org/10.1104/pp.16.01287DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5210728PMC
January 2017

Correlation-Based Network Generation, Visualization, and Analysis as a Powerful Tool in Biological Studies: A Case Study in Cancer Cell Metabolism.

Biomed Res Int 2016 19;2016:8313272. Epub 2016 Oct 19.

The Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, 84990 Midreshet Ben-Gurion, Israel.

In the last decade vast data sets are being generated in biological and medical studies. The challenge lies in their summary, complexity reduction, and interpretation. Correlation-based networks and graph-theory based properties of this type of networks can be successfully used during this process. However, the procedure has its pitfalls and requires specific knowledge that often lays beyond classical biology and includes many computational tools and software. Here we introduce one of a series of methods for correlation-based network generation and analysis using freely available software. The pipeline allows the user to control each step of the network generation and provides flexibility in selection of correlation methods and thresholds. The pipeline was implemented on published metabolomics data of a population of human breast carcinoma cell lines MDA-MB-231 under two conditions: normal and hypoxia. The analysis revealed significant differences between the metabolic networks in response to the tested conditions. The network under hypoxia had 1.7 times more significant correlations between metabolites, compared to normal conditions. Unique metabolic interactions were identified which could lead to the identification of improved markers or aid in elucidating the mechanism of regulation between distantly related metabolites induced by the cancer growth.
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http://dx.doi.org/10.1155/2016/8313272DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5090126PMC
March 2017

Effects of Parental Temperature and Nitrate on Seed Performance are Reflected by Partly Overlapping Genetic and Metabolic Pathways.

Plant Cell Physiol 2016 Mar 6;57(3):473-87. Epub 2016 Jan 6.

Wageningen Seed Lab, Laboratory of Plant Physiology, Wageningen University, Droevendaalsesteeg 1, NL-6708 PB Wageningen, The Netherlands Department of Molecular Plant Physiology, Utrecht University, NL-3584 CH Utrecht, The Netherlands

Seed performance is affected by the seed maturation environment, and previously we have shown that temperature, nitrate and light intensity were the most influential environmental factors affecting seed performance. Seeds developed in these environments were selected to assess the underlying metabolic pathways, using a combination of transcriptomics and metabolomics. These analyses revealed that the effects of the parental temperature and nitrate environments were reflected by partly overlapping genetic and metabolic networks, as indicated by similar changes in the expression levels of metabolites and transcripts. Nitrogen metabolism-related metabolites (asparagine, γ-aminobutyric acid and allantoin) were significantly decreased in both low temperature (15 °C) and low nitrate (N0) maturation environments. Correspondingly, nitrogen metabolism genes (ALLANTOINASE, NITRATE REDUCTASE 1, NITRITE REDUCTASE 1 and NITRILASE 4) were differentially regulated in the low temperature and nitrate maturation environments, as compared with control conditions. High light intensity during seed maturation increased galactinol content, and displayed a high correlation with seed longevity. Low light had a genotype-specific effect on cell surface-encoding genes in the DELAY OF GERMINATION 6-near isogenic line (NILDOG6). Overall, the integration of phenotypes, metabolites and transcripts led to new insights into the regulation of seed performance.
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http://dx.doi.org/10.1093/pcp/pcv207DOI Listing
March 2016

The transporter GAT1 plays an important role in GABA-mediated carbon-nitrogen interactions in Arabidopsis.

Front Plant Sci 2015 29;6:785. Epub 2015 Sep 29.

The Albert Katz International School for Desert Studies, The Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Midreshet Ben-Gurion Beer Sheva, Israel.

Glutamate derived γ-aminobutyric acid (GABA) is synthetized in the cytosol prior to delivery to the mitochondria where it is catabolized via the TCA cycle. GABA accumulates under various environmental conditions, but an increasing number of studies show its involvement at the crossroad between C and N metabolism. To assess the role of GABA in modulating cellular metabolism, we exposed seedlings of A. thaliana GABA transporter gat1 mutant to full nutrition medium and media deficient in C and N combined with feeding of different concentrations (0.5 and 1 mM) of exogenous GABA. GC-MS based metabolite profiling showed an expected effect of medium composition on the seedlings metabolism of mutant and wild type alike. That being said, a significant interaction between GAT1 deficiency and medium composition was determined with respect to magnitude of change in relative amino acid levels. The effect of exogenous GABA treatment on metabolism was contingent on both the medium and the genotype, leading for instance to a drop in asparagine under full nutrition and low C conditions and glucose under all tested media, but not to changes in GABA content. We additionally assessed the effect of GAT1 deficiency on the expression of glutamate metabolism related genes and genes involved in abiotic stress responses. These results suggest a role for GAT1 in GABA-mediated metabolic alterations in the context of the C-N equilibrium of plant cells.
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http://dx.doi.org/10.3389/fpls.2015.00785DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4586413PMC
October 2015

Metabolic and Physiological Responses of Shiraz and Cabernet Sauvignon (Vitis vinifera L.) to Near Optimal Temperatures of 25 and 35 °C.

Int J Mol Sci 2015 Oct 14;16(10):24276-94. Epub 2015 Oct 14.

The French Associates Institute for Agriculture and Biotechnology of Drylands (FAAB), the Jacob Blaustein Institute for Desert Research, Ben Gurion University of the Negev, 84990 Sede Boqer, Israel.

Shiraz and Cabernet Sauvignon (Cs) grapevines were grown at near optimal temperatures (25 or 35 °C). Gas exchange, fluorescence, metabolic profiling and correlation based network analysis were used to characterize leaf physiology. When grown at 25 °C, the growth rate and photosynthesis of both cultivars were similar. At 35 °C Shiraz showed increased respiration, non-photochemical quenching and reductions of photosynthesis and growth. In contrast, Cs maintained relatively stable photosynthetic activity and growth regardless of the condition. In both cultivars, growth at 35 °C resulted in accumulations of secondary sugars (raffinose, fucose and ribulose) and reduction of primary sugars concentration (glucose, fructose and sucrose), more noticeably in Shiraz than Cs. In spite of similar patterns of metabolic changes in response to growth at 35 °C, significant differences in important leaf antioxidants and antioxidant precursors (DHA/ascorbate, quinates, cathechins) characterized the cultivar response. Correlation analysis reinforced Shiraz sensitivity to the 35 °C, showing higher number of newly formed edges at 35 °C and higher modularity in Shiraz as compared to Cs. The results suggest that the optimal growth temperatures of grapevines are cultivar dependent, and allow a first insight into the variability of the metabolic responses of grapevines under varied temperatures.
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http://dx.doi.org/10.3390/ijms161024276DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4632749PMC
October 2015

Sulfite Oxidase Activity Is Essential for Normal Sulfur, Nitrogen and Carbon Metabolism in Tomato Leaves.

Plants (Basel) 2015 Aug 14;4(3):573-605. Epub 2015 Aug 14.

French Associates Institute for Agriculture and Biotechnology of Drylands, Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede Boqer Campus 84990, Israel.

Plant sulfite oxidase [SO; E.C.1.8.3.1] has been shown to be a key player in protecting plants against exogenous toxic sulfite. Recently we showed that SO activity is essential to cope with rising dark-induced endogenous sulfite levels in tomato plants (Lycopersicon esculentum/Solanum lycopersicum Mill. cv. Rheinlands Ruhm). Here we uncover the ramifications of SO impairment on carbon, nitrogen and sulfur (S) metabolites. Current analysis of the wild-type and SO-impaired plants revealed that under controlled conditions, the imbalanced sulfite level resulting from SO impairment conferred a metabolic shift towards elevated reduced S-compounds, namely sulfide, S-amino acids (S-AA), Co-A and acetyl-CoA, followed by non-S-AA, nitrogen and carbon metabolite enhancement, including polar lipids. Exposing plants to dark-induced carbon starvation resulted in a higher degradation of S-compounds, total AA, carbohydrates, polar lipids and total RNA in the mutant plants. Significantly, a failure to balance the carbon backbones was evident in the mutants, indicated by an increase in tricarboxylic acid cycle (TCA) cycle intermediates, whereas a decrease was shown in stressed wild-type plants. These results indicate that the role of SO is not limited to a rescue reaction under elevated sulfite, but SO is a key player in maintaining optimal carbon, nitrogen and sulfur metabolism in tomato plants.
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http://dx.doi.org/10.3390/plants4030573DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4844397PMC
August 2015

Combined correlation-based network and mQTL analyses efficiently identified loci for branched-chain amino acid, serine to threonine, and proline metabolism in tomato seeds.

Plant J 2015 Jan 16;81(1):121-33. Epub 2014 Dec 16.

The Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, 84990, Midreshet Ben-Gurion, Israel.

Correlation-based network analysis (CNA) of the metabolic profiles of seeds of a tomato introgression line mapping population revealed a clique of proteinogenic amino acids: Gly, Ile, Pro, Ser, Thr, and Val. Correlations between profiles of these amino acids exhibited a statistically significant average correlation coefficient of 0.84 as compared with an average correlation coefficient of 0.39 over the 16 119 other metabolite cliques containing six metabolites. In silico removal of cliques was used to quantify their importance in determining seminal network properties, highlighting the strong effects of the amino acid clique. Quantitative trait locus analysis revealed co-localization for the six amino acids on chromosome 2, 4 and 10. Sequence analysis identified a unique set of 10 genes on chromosome 2 only, which were associated with amino acid metabolism and specifically the metabolism of Ser-Gly and their conversion into branched-chain amino acids. Metabolite profiling of a set of sublines, with introgressions on chromosome 2, identified a significant change in the abundance of the six amino acids in comparison with M82. Expression analysis of candidate genes affecting Ser metabolism matched the observation from the metabolite data, suggesting a coordinated behavior of the level of these amino acids at the genetic level. Analysis of transcription factor binding sites in the promoter regions of the identified genes suggested combinatorial response to light and the circadian clock.
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http://dx.doi.org/10.1111/tpj.12717DOI Listing
January 2015

Metabolite profiling and integrative modeling reveal metabolic constraints for carbon partitioning under nitrogen starvation in the green algae Haematococcus pluvialis.

J Biol Chem 2014 Oct 2;289(44):30387-30403. Epub 2014 Sep 2.

French Associates Institute for Agriculture and Biotechnology, the Jacob Blaustein Institutes for Desert Research, Ben Gurion University of the Negev, Sede Boker 84990, Israel.

The green alga Hematococcus pluvialis accumulates large amounts of the antioxidant astaxanthin under inductive stress conditions, such as nitrogen starvation. The response to nitrogen starvation and high light leads to the accumulation of carbohydrates and fatty acids as well as increased activity of the tricarboxylic acid cycle. Although the behavior of individual pathways has been well investigated, little is known about the systemic effects of the stress response mechanism. Here we present time-resolved metabolite, enzyme activity, and physiological data that capture the metabolic response of H. pluvialis under nitrogen starvation and high light. The data were integrated into a putative genome-scale model of the green alga to in silico test hypotheses of underlying carbon partitioning. The model-based hypothesis testing reinforces the involvement of starch degradation to support fatty acid synthesis in the later stages of the stress response. In addition, our findings support a possible mechanism for the involvement of the increased activity of the tricarboxylic acid cycle in carbon repartitioning. Finally, the in vitro experiments and the in silico modeling presented here emphasize the predictive power of large scale integrative approaches to pinpoint metabolic adjustment to changing environments.
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http://dx.doi.org/10.1074/jbc.M114.555144DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4215223PMC
October 2014

Metabolite and transcript profiling of berry skin during fruit development elucidates differential regulation between Cabernet Sauvignon and Shiraz cultivars at branching points in the polyphenol pathway.

BMC Plant Biol 2014 Jul 26;14:188. Epub 2014 Jul 26.

The French Associates Institute for Agriculture and Biotechnology of Drylands, the Jacob Blaustein Institute for Desert Research, Ben-Gurion University of the Negev, Sede Boqer 84990, Israel.

Background: Grapevine berries undergo complex biochemical changes during fruit maturation, many of which are dependent upon the variety and its environment. In order to elucidate the varietal dependent developmental regulation of primary and specialized metabolism, berry skins of Cabernet Sauvignon and Shiraz were subjected to gas chromatography-mass spectrometry (GC-MS) and liquid chromatography-mass spectrometry (LC-MS) based metabolite profiling from pre-veraison to harvest. The generated dataset was augmented with transcript profiling using RNAseq.

Results: The analysis of the metabolite data revealed similar developmental patterns of change in primary metabolites between the two cultivars. Nevertheless, towards maturity the extent of change in the major organic acid and sugars (i.e. sucrose, trehalose, malate) and precursors of aromatic and phenolic compounds such as quinate and shikimate was greater in Shiraz compared to Cabernet Sauvignon. In contrast, distinct directional projections on the PCA plot of the two cultivars samples towards maturation when using the specialized metabolite profiles were apparent, suggesting a cultivar-dependent regulation of the specialized metabolism. Generally, Shiraz displayed greater upregulation of the entire polyphenol pathway and specifically higher accumulation of piceid and coumaroyl anthocyanin forms than Cabernet Sauvignon from veraison onwards. Transcript profiling revealed coordinated increased transcript abundance for genes encoding enzymes of committing steps in the phenylpropanoid pathway. The anthocyanin metabolite profile showed F3'5'H-mediated delphinidin-type anthocyanin enrichment in both varieties towards maturation, consistent with the transcript data, indicating that the F3'5'H-governed branching step dominates the anthocyanin profile at late berry development. Correlation analysis confirmed the tightly coordinated metabolic changes during development, and suggested a source-sink relation between the central and specialized metabolism, stronger in Shiraz than Cabernet Sauvignon. RNAseq analysis also revealed that the two cultivars exhibited distinct pattern of changes in genes related to abscisic acid (ABA) biosynthesis enzymes.

Conclusions: Compared with CS, Shiraz showed higher number of significant correlations between metabolites, which together with the relatively higher expression of flavonoid genes supports the evidence of increased accumulation of coumaroyl anthocyanins in that cultivar. Enhanced stress related metabolism, e.g. trehalose, stilbene and ABA in Shiraz berry-skin are consistent with its relatively higher susceptibility to environmental cues.
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http://dx.doi.org/10.1186/s12870-014-0188-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4222437PMC
July 2014

Combined transcriptomics and metabolomics of Arabidopsis thaliana seedlings exposed to exogenous GABA suggest its role in plants is predominantly metabolic.

Mol Plant 2014 Jun 19;7(6):1065-1068. Epub 2014 Feb 19.

The Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev Sede Boqer Campus 84990, Israel. Electronic address:

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http://dx.doi.org/10.1093/mp/ssu017DOI Listing
June 2014

The investment in scent: time-resolved metabolic processes in developing volatile-producing Nigella sativa L. seeds.

PLoS One 2013 3;8(9):e73061. Epub 2013 Sep 3.

The Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Midreshet Ben-Gurion, Israel.

The interplay of processes in central and specialized metabolisms during seed development of Nigella sativa L. was studied by using a high-throughput metabolomics technology and network-based analysis. Two major metabolic shifts were identified during seed development: the first was characterized by the accumulation of storage lipids (estimated as total fatty acids) and N-compounds, and the second by the biosynthesis of volatile organic compounds (VOCs) and a 30% average decrease in total fatty acids. Network-based analysis identified coordinated metabolic processes during development and demonstrated the presence of five network communities. Enrichment analysis indicated that different compound classes, such as sugars, amino acids, and fatty acids, are largely separated and over-represented in certain communities. One community displayed several terpenoids and the central metabolites, shikimate derived amino acids, raffinose, xylitol and glycerol-3-phosphate. The latter are related to precursors of the mevalonate-independent pathway for VOC production in the plastid; also plastidial fatty acid 18∶3n-3 abundant in "green" seeds grouped with several major terpenes. The findings highlight the interplay between the components of central metabolism and the VOCs. The developmental regulation of Nigella seed metabolism during seed maturation suggests a substantial re-allocation of carbon from the breakdown of fatty acids and from N-compounds, probably towards the biosynthesis of VOCs.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0073061PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3760832PMC
May 2014

Growth, lipid production and metabolic adjustments in the euryhaline eustigmatophyte Nannochloropsis oceanica CCALA 804 in response to osmotic downshift.

Appl Microbiol Biotechnol 2013 Sep 25;97(18):8291-306. Epub 2013 Jul 25.

French Associates Institute of Agriculture and Biotechnology of Drylands, J. Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Midreshet Ben-Gurion, 84990, Israel.

We investigated the effects of osmotic downshift induced by the transfer of Nannochloropsis oceanica CCALA 804 from artificial seawater medium (27 g L(-1) NaCl) to the same medium without NaCl or freshwater modified BG-11 medium (mBG-11) as a function of photosynthetically active radiation (170, 350, or 700 μmol photon m(-2) s(-1)). Alterations in growth, total fatty acid (FA) content and FA composition of individual lipid classes, and in relative contents of metabolites relevant to osmotic adjustments were studied. Cells displayed remarkable tolerance to the osmotic downshift apart from some swelling, with no substantial lag or decline in cell division rate. Biomass accumulation and chlorophyll a content were enhanced upon downshifting, especially under the highest irradiance. The highest chlorophyll a and eicosapentaenoic acid (EPA) biomass and culture contents were determined in the cultures grown in mBG-11. Two days after transfer to 0 g L(-1) NaCl, the proportion in total acyl lipids of the major chloroplast galactolipid monogalactosyldiacylglycerol, a major depot of EPA, increased twofold, along with a modest change in the proportion of digalactosyldiacylglycerol (DGDG). EPA percentage decreased in DGDG and increased in the extraplastidial lipid phosphatidylethanolamine. Metabolite profiling by GC-MS analysis revealed a sharp decrease in metabolites potentially involved in osmoregulation, such as mannitol and proline, while proline-cycle intermediates and some free sugars increased. The stress-induced polyamine spermidine decreased ca. one order of magnitude, while its catabolic product-the non-protein amino acid γ-amino butyric acid-increased twofold, as did the stress-related sugars trehalose and talose. Biochemical mechanisms governing osmotic plasticity and implications for optimization of EPA production by N. oceanica CCALA 804 under variable cultivation conditions are discussed.
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http://dx.doi.org/10.1007/s00253-013-5092-6DOI Listing
September 2013

Growth platform-dependent and -independent phenotypic and metabolic responses of Arabidopsis and its halophytic relative, Eutrema salsugineum, to salt stress.

Plant Physiol 2013 Jul 4;162(3):1583-98. Epub 2013 Jun 4.

French Associates Institute for Biotechnology and Agriculture of Drylands, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Midreshet Ben Gurion 84990, Israel.

Comparative studies of the stress-tolerant Arabidopsis (Arabidopsis thaliana) halophytic relative, Eutrema salsugineum, have proven a fruitful approach to understanding natural stress tolerance. Here, we performed comparative phenotyping of Arabidopsis and E. salsugineum vegetative development under control and salt-stress conditions, and then compared the metabolic responses of the two species on different growth platforms in a defined leaf developmental stage. Our results reveal both growth platform-dependent and -independent phenotypes and metabolic responses. Leaf emergence was affected in a similar way in both species grown in vitro but the effects observed in Arabidopsis occurred at higher salt concentrations in E. salsugineum. No differences in leaf emergence were observed on soil. A new effect of a salt-mediated reduction in E. salsugineum leaf area was unmasked. On soil, leaf area reduction in E. salsugineum was mainly due to a fall in cell number, whereas both cell number and cell size contributed to the decrease in Arabidopsis leaf area. Common growth platform-independent leaf metabolic signatures such as high raffinose and malate, and low fumarate contents that could reflect core stress tolerance mechanisms, as well as growth platform-dependent metabolic responses were identified. In particular, the in vitro growth platform led to repression of accumulation of many metabolites including sugars, sugar phosphates, and amino acids in E. salsugineum compared with the soil system where these same metabolites accumulated to higher levels in E. salsugineum than in Arabidopsis. The observation that E. salsugineum maintains salt tolerance despite growth platform-specific phenotypes and metabolic responses suggests a considerable degree of phenotypic and metabolic adaptive plasticity in this extremophile.
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http://dx.doi.org/10.1104/pp.113.217844DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3707563PMC
July 2013
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