Cucumber's secret: decoding the metabolic role of csnadp-me2
Nanjing Agricultural University The Academy of Science
image: Putative model of CsNADP-ME2 function in cucumber fruit. Based on gene expression, tissue-specific localization, activity assay of enzymes, and related physiological speculations, the role and active sites of NADP-ME (one of the decarboxylases), the TCA cycle and glycolysis in cucumber fruit are marked. Solid black arrows indicate metabolic flux. Dotted black arrows indicate that the process consists of multiple catalytic reactions. In CsNADP-ME2-OE plants (left) with upregulation of CsNADP-ME2 expression and enzyme activity (up arrow) when compared with WT plants, the content of substrate malate decreased (down arrows), then the increased transcript levels and maintained enzyme activities of PK (the primary regulation) and PFK (the secondary regulation) (up arrows) could result in a continuous bottom-up feedback-promotion of glycolysis. On the other hand, as the more intermediate products of the TCA cycle were likely used to produce energy by its own reaction, the availability of carbon skeleton for amino acid metabolism was suppressed. Compared with wild-type plants, in RNAi plants (right) characterized by the downregulation of CsNADP-ME2 expression and enzyme activity (down arrow), the substrate malate accumulated significantly (up arrows). Accumulated malate could feedback-inhibit the expressions and activities of PK and PFK (down arrows). In addition, downregulation of CsNADP-ME2 in the fruit of RNAi lines might slow down the rate of TCA cycle activity due to the accumulation of the substrate malate. Some intermediates in the TCA cycle can be more effectively used as a precursor for the production of other derivatives/amino acids, thus promoting nitrogen assimilation, such as amino acid synthesis, in the exocarp. F-1,6-BP, fructose-1,6-bisphosphate; F-6-P, fructose-6-phosphate; 2OG, 2-oxoglutarate; Mal, malate; OAA, oxaloacetate; PFK, ATP-dependent phosphofructokinase; PK, pyruvate kinase; PYR, pyruvic acid; Suc, sucrose.
Credit: Horticulture Research
A recent study has uncovered the pivotal role of the enzyme CsNADP-ME2 (NADP-dependent malic enzyme, NADP-ME) in cucumbers, controlling the delicate balance between carbon and amino acid metabolism within the fruit. This intricate metabolic process directly impacts fruit development, yield, and nutritional quality, highlighting CsNADP-ME2 as a promising target for enhancing crop performance and food quality through metabolic engineering.
Carbon and nitrogen are fundamental to plant growth and agricultural productivity, with their regulation often mediated by carboxylate metabolism enzymes. While previous research has identified the importance of malate-related enzymes in managing carbon and nitrogen metabolism in plants, their specific functions in fleshy fruits like cucumbers remain largely unexplored. Addressing this knowledge gap is crucial for understanding how these enzymes can be leveraged to boost fruit yield and quality.
Led by scientists from China Agricultural University and the Max Planck Institute of Molecular Plant Physiology, the study (DOI: 10.1093/hr/uhad216) was published on October 25, 2023, in Horticulture Research. It focuses on the CsNADP-ME2 (NADP-dependent malic enzyme, NADP-ME) enzyme in cucumbers, which plays a crucial role in regulating carbon and amino acid metabolism. By examining transgenic lines, the researchers revealed how varying levels of CsNADP-ME2 expression influence carbon flow and the metabolic balance of sugars and amino acids, providing new insights into improving fruit quality.
The study investigates how CsNADP-ME2 orchestrates carbon and nitrogen metabolism in cucumber fruits. Predominantly active in the exocarp and vascular bundles, CsNADP-ME2 regulates the conversion of malate into pyruvate and CO₂, key processes in glycolysis and the tricarboxylic acid (TCA) cycle. Overexpression of CsNADP-ME2 significantly boosted soluble sugars and starch, while its suppression led to malate and amino acid accumulation, underscoring its dual role in maintaining carbon-nitrogen balance. The findings highlight CsNADP-ME2’s potential as a target for metabolic engineering, promising enhanced cucumber growth and improved fruit quality.
Dr. Xiaolei Sui, a lead researcher in the study, commented, "Our research shows that CsNADP-ME2 is more than just a metabolic participant—it is a crucial regulator of the network that integrates sugar and amino acid synthesis in cucumber fruits. By decoding the feedback mechanisms and regulatory functions of this enzyme, we can develop new strategies to enhance the nutritional value and yield of cucumbers and other fleshy fruits."
The identification of CsNADP-ME2’s critical role in cucumber metabolism paves the way for innovative approaches to improve fruit quality and agricultural yields through genetic and metabolic engineering. Targeting this enzyme allows for precise adjustments in carbon and nitrogen balance, optimizing crop productivity. This study underscores the potential of manipulating key metabolic enzymes to meet global food security needs, enhancing plant growth and fruit development in sustainable agricultural practices.
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References
DOI
Original Source URL
https://doi.org/10.1093/hr/uhad216
Funding information
This work was supported by the National Natural Science Foundation of China (32272695 and 31972398 to X.S.), the National Key Research and Development Program of China (2019YFD1000300), the National Natural Science Foundation of China (31960591 to N.S.), the Max-Planck Society and European Union’s Horizon 2020 research and innovation programme, project PlantaSYST (SGA-CSA No. 664621 and No. 739582 under FPA No. 664620), the China Agriculture Research System of MOF and MARA (CARS-23), and the 111 Project of Ministry of Education of P.R.C. (B17043).
About Horticulture Research
Horticulture Research is an open access journal of Nanjing Agricultural University and ranked number two in the Horticulture category of the Journal Citation Reports ™ from Clarivate, 2023. The journal is committed to publishing original research articles, reviews, perspectives, comments, correspondence articles and letters to the editor related to all major horticultural plants and disciplines, including biotechnology, breeding, cellular and molecular biology, evolution, genetics, inter-species interactions, physiology, and the origination and domestication of crops.
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