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Synchronization of developmental, molecular and metabolic aspects of source-sink interactions.
Fernie, AR, Bachem, CWB, Helariutta, Y, Neuhaus, HE, Prat, S, Ruan, YL, Stitt, M, Sweetlove, LJ, Tegeder, M, Wahl, V, et al
Nature plants. 2020;(2):55-66
Abstract
Plants have evolved a multitude of strategies to adjust their growth according to external and internal signals. Interconnected metabolic and phytohormonal signalling networks allow adaption to changing environmental and developmental conditions and ensure the survival of species in fluctuating environments. In agricultural ecosystems, many of these adaptive responses are not required or may even limit crop yield, as they prevent plants from realizing their fullest potential. By lifting source and sink activities to their maximum, massive yield increases can be foreseen, potentially closing the future yield gap resulting from an increasing world population and the transition to a carbon-neutral economy. To do so, a better understanding of the interplay between metabolic and developmental processes is required. In the past, these processes have been tackled independently from each other, but coordinated efforts are required to understand the fine mechanics of source-sink relations and thus optimize crop yield. Here, we describe approaches to design high-yielding crop plants utilizing strategies derived from current metabolic concepts and our understanding of the molecular processes determining sink development.
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Lighting Up Live-Cell and In Vivo Central Carbon Metabolism with Genetically Encoded Fluorescent Sensors.
Zhang, Z, Cheng, X, Zhao, Y, Yang, Y
Annual review of analytical chemistry (Palo Alto, Calif.). 2020;(1):293-314
Abstract
As the core component of cell metabolism, central carbon metabolism, consisting of glycolysis, the pentose phosphate pathway, and the tricarboxylic acid cycle converts nutrients into metabolic precursors for biomass and energy to sustain the life of virtually all extant species. The metabolite levels or distributions in central carbon metabolism often change dynamically with cell fates, development, and disease progression. However, traditional biochemical methods require cell lysis, making it challenging to obtain spatiotemporal information about metabolites in living cells and in vivo. Genetically encoded fluorescent sensors allow the rapid, sensitive, specific, and real-time readout of metabolite dynamics in living organisms, thereby offering the potential to fill the gap in current techniques. In this review, we introduce recent progress made in the development of genetically encoded fluorescent sensors for central carbon metabolism and discuss their advantages, disadvantages, and applications. Moreover, several future directions of metabolite sensors are also proposed.
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Wasteful, essential, evolutionary stepping stone? The multiple personalities of the photorespiratory pathway.
Fernie, AR, Bauwe, H
The Plant journal : for cell and molecular biology. 2020;(4):666-677
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Abstract
The photorespiratory pathway, in short photorespiration, is a metabolic repair system that enables the CO2 fixation enzyme Rubisco to sustainably operate in the presence of oxygen, that is, during oxygenic photosynthesis of plants and cyanobacteria. Photorespiration is necessary because an auto-inhibitory metabolite, 2-phosphoglycolate (2PG), is produced when Rubisco binds oxygen instead of CO2 as a substrate and must be removed, to avoid collapse of metabolism, and recycled as efficiently as possible. The basic principle of recycling 2PG very likely evolved several billion years ago in connection with the evolution of oxyphotobacteria. It comprises the multi-step combination of two molecules of 2PG to form 3-phosphoglycerate. The biochemistry of this process dictates that one out of four 2PG carbons is lost as CO2 , which is a long-standing plant breeders' concern because it represents by far the largest fraction of respiratory processes that reduce gross-photosynthesis of major crops down to about 50% and less, lowering potential yields. In addition to the ATP needed for recycling of the 2PG carbon, extra energy is needed for the refixation of liberated equal amounts of ammonia. It is thought that the energy costs of photorespiration have an additional negative impact on crop yields in at least some environments. This paper discusses recent advances concerning the origin and evolution of photorespiration, and gives an overview of contemporary and envisioned strategies to engineer the biochemistry of, or even avoid, photorespiration.
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Pseudomonad reverse carbon catabolite repression, interspecies metabolite exchange, and consortial division of labor.
Park, H, McGill, SL, Arnold, AD, Carlson, RP
Cellular and molecular life sciences : CMLS. 2020;(3):395-413
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Abstract
Microorganisms acquire energy and nutrients from dynamic environments, where substrates vary in both type and abundance. The regulatory system responsible for prioritizing preferred substrates is known as carbon catabolite repression (CCR). Two broad classes of CCR have been documented in the literature. The best described CCR strategy, referred to here as classic CCR (cCCR), has been experimentally and theoretically studied using model organisms such as Escherichia coli. cCCR phenotypes are often used to generalize universal strategies for fitness, sometimes incorrectly. For instance, extremely competitive microorganisms, such as Pseudomonads, which arguably have broader global distributions than E. coli, have achieved their success using metabolic strategies that are nearly opposite of cCCR. These organisms utilize a CCR strategy termed 'reverse CCR' (rCCR), because the order of preferred substrates is nearly reverse that of cCCR. rCCR phenotypes prefer organic acids over glucose, may or may not select preferred substrates to optimize growth rates, and do not allocate intracellular resources in a manner that produces an overflow metabolism. cCCR and rCCR have traditionally been interpreted from the perspective of monocultures, even though most microorganisms live in consortia. Here, we review the basic tenets of the two CCR strategies and consider these phenotypes from the perspective of resource acquisition in consortia, a scenario that surely influenced the evolution of cCCR and rCCR. For instance, cCCR and rCCR metabolism are near mirror images of each other; when considered from a consortium basis, the complementary properties of the two strategies can mitigate direct competition for energy and nutrients and instead establish cooperative division of labor.
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Review: Crucial role of inorganic pyrophosphate in integrating carbon metabolism from sucrose breakdown to starch synthesis in rice endosperm.
Lee, SK, Jeon, JS
Plant science : an international journal of experimental plant biology. 2020;:110572
Abstract
The endosperm is a primary constituent of mature seeds in rice as well as in other cereal crops, serving as the major storage reserve of starch. Observations indicate that the central part of the endosperm is subject to hypoxic conditions, which require a switch of energy metabolism owing to limited mitochondrial respiration. Uniquely, this endosperm generates a large source of inorganic pyrophosphate (PPi) as a byproduct of the reaction of ADP glucose pyrophosphorylase in the cytosol. Recent results derived from examination of the mutants of cereal crops, especially rice, for PPi-utilizing enzymes clearly suggest an important role of PPi as an alternative energy currency for integrating carbon metabolism from sucrose breakdown to starch synthesis in the endosperm. Thus, the present review provides an outline of the interlaced PPi-dependent metabolic pathways, which are critical for starch synthesis in the endosperm in terms of energy metabolism, along with its application to enhance yield potential.
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Mechanisms for Induction of Microbial Extracellular Proteases in Response to Exterior Proteins.
Zhang, YZ, Zhang, WX, Chen, XL
Applied and environmental microbiology. 2020;(19)
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Abstract
Proteins are a main organic nitrogen source for microorganisms. Many heterotrophic microorganisms secrete extracellular proteases (ex-proteases) to efficiently decompose proteins into oligopeptides and amino acids when exterior proteins are required for growth. These ex-proteases not only play important roles in microbial nutrient acquisition or host infection but also contribute greatly to the global recycling of carbon and nitrogen. Moreover, may microbial ex-proteases have important applications in industrial, medical, and biotechnological areas. Therefore, uncovering the mechanisms by which microorganisms initiate the expression of ex-protease genes in response to exterior proteins is of great significance. In this review, the progress made in understanding the induction mechanisms of microbial ex-proteases in response to exterior proteins is summarized, with a focus on the inducer molecules, membrane sensors, and downstream pathways. Problems to be solved for better understanding of the induction mechanisms of microbial ex-proteases are also discussed.
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Constraining estimates of terrestrial carbon uptake: new opportunities using long-term satellite observations and data assimilation.
Smith, WK, Fox, AM, MacBean, N, Moore, DJP, Parazoo, NC
The New phytologist. 2020;(1):105-112
Abstract
The response of terrestrial carbon uptake to increasing atmospheric [CO2 ], that is the CO2 fertilization effect (CFE), remains a key area of uncertainty in carbon cycle science. Here we provide a perspective on how satellite observations could be better used to understand and constrain CFE. We then highlight data assimilation (DA) as an effective way to reconcile different satellite datasets and systematically constrain carbon uptake trends in Earth System Models. As a proof-of-concept, we show that joint DA of multiple independent satellite datasets reduced model ensemble error by better constraining unobservable processes and variables, including those directly impacted by CFE. DA of multiple satellite datasets offers a powerful technique that could improve understanding of CFE and enable more accurate forecasts of terrestrial carbon uptake.
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Regulatory RNA at the crossroads of carbon and nitrogen metabolism in photosynthetic cyanobacteria.
Muro-Pastor, AM, Hess, WR
Biochimica et biophysica acta. Gene regulatory mechanisms. 2020;(1):194477
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Abstract
Cyanobacteria are photosynthetic bacteria that populate widely different habitats. Accordingly, cyanobacteria exhibit a wide spectrum of lifestyles, physiologies, and morphologies and possess genome sizes and gene numbers which may vary by up to a factor of ten within the phylum. Consequently, large differences exist between individual species in the size and complexity of their regulatory networks. Several non-coding RNAs have been identified that play crucial roles in the acclimation responses of cyanobacteria to changes in the environment. Some of these regulatory RNAs are conserved throughout the cyanobacterial phylum, while others exist only in a few taxa. Here we give an overview on characterized regulatory RNAs in cyanobacteria, with a focus on regulators of photosynthesis, carbon and nitrogen metabolism. However, chances are high that these regulators represent just the tip of the iceberg.
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tRNA wobble-uridine modifications as amino acid sensors and regulators of cellular metabolic state.
Gupta, R, Laxman, S
Current genetics. 2020;(3):475-480
Abstract
Cells must appropriately sense available nutrients and accordingly regulate their metabolic outputs, to survive. This mini-review considers the idea that conserved chemical modifications of wobble (U34) position tRNA uridines enable cells to sense nutrients and regulate their metabolic state. tRNA wobble uridines are chemically modified at the 2- and 5- positions, with a thiol (s2), and (commonly) a methoxycarbonylmethyl (mcm5) modification, respectively. These modifications reflect sulfur amino acid (methionine and cysteine) availability. The loss of these modifications has minor translation defects. However, they result in striking phenotypes consistent with an altered metabolic state. Using yeast, we recently discovered that the s2 modification regulates overall carbon and nitrogen metabolism, dependent on methionine availability. The loss of this modification results in rewired carbon (glucose) metabolism. Cells have reduced carbon flux towards the pentose phosphate pathway and instead increased flux towards storage carbohydrates-primarily trehalose, along with reduced nucleotide synthesis, and perceived amino acid starvation signatures. Remarkably, this metabolic rewiring in the s2U mutants is caused by mechanisms leading to intracellular phosphate limitation. Thus this U34 tRNA modification responds to methionine availability and integratively regulates carbon and nitrogen homeostasis, wiring cells to a 'growth' state. We interpret the importance of U34 modifications in the context of metabolic sensing and anabolism, emphasizing their intimate coupling to methionine metabolism.
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Seed quality and carbon primary metabolism.
Domergue, JB, Abadie, C, Limami, A, Way, D, Tcherkez, G
Plant, cell & environment. 2019;(10):2776-2788
Abstract
Improving seed quality is amongst the most important challenges of contemporary agriculture. In fact, using plant varieties with better germination rates that are more tolerant to stress during seedling establishment may improve crop yield considerably. Therefore, intense efforts are currently being devoted to improve seed quality in many species, mostly using genomics tools. However, despite its considerable importance during seed imbibition and germination processes, primary carbon metabolism in seeds is less studied. Our knowledge of the physiology of seed respiration and energy generation and the impact of these processes on seed performance have made limited progress over the past three decades. In particular, (isotope-assisted) metabolomics of seeds has only been assessed occasionally, and there is limited information on possible quantitative relationships between metabolic fluxes and seed quality. Here, we review the recent literature and provide an overview of potential links between metabolic efficiency, metabolic biomarkers, and seed quality and discuss implications for future research, including a climate change context.