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Article|25 Oct 2023|OPEN
Cucumber malate decarboxylase, CsNADP-ME2, functions in the balance of carbon and amino acid metabolism in fruit
Nan Shan1,2 ,† , Youjun Zhang3 ,† , Yicong Guo1 ,† , Wenna Zhang1 , Jing Nie1 and Alisdair R. Fernie3,4 , , Xiaolei Sui,1,4 ,
1Beijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, College of Horticulture, China Agricultural University, Beijing 100193, China
2Jiangxi Province Key Laboratory of Root and Tuber Crops Biology (Jiangxi Agricultural University), Nanchang 330045, China
3Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm 14476 Germany
4Equal senior authors
*Corresponding author. E-mail: fernie@mpimp-golm.mpg.de,suixiaolei@cau.edu.cn
Nan Shan and Youjun Zhang,Yicong Guo contributed equally to the study.

Horticulture Research 11,
Article number: uhad216 (2024)
doi: https://doi.org/10.1093/hr/uhad216
Views: 50

Received: 20 Jul 2023
Accepted: 16 Oct 2023
Published online: 25 Oct 2023

Abstract

Central metabolism produces carbohydrates and amino acids that are tightly correlated to plant growth and thereby crop productivity. Malate is reported to link mitochondrial respiratory metabolism with cytosolic biosynthetic pathways. Although the function of malate metabolism-related enzymes in providing carbon has been characterized in some plants, evidence for this role in the fleshy fruit of cucumber is lacking. Here, radiolabeled bicarbonate fed into the xylem stream from the cucumber roots was incorporated into amino acids, soluble sugars, and organic acids in the exocarp and vasculature of fruits. The activities of decarboxylases, especially decarboxylation from NADP-dependent malic enzyme (NADP-ME), were higher in cucumber fruit than in the leaf lamina. Histochemical localization revealed that CsNADP-ME2 was mainly located in the exocarp and vascular bundle system of fruit. Radiotracer and gas-exchange analysis indicated that overexpression of CsNADP-ME2 could promote carbon flux into soluble sugars and starch in fruits. Further studies combined with metabolic profiling revealed that the downregulation of CsNADP-ME2 in RNA interference (RNAi) lines caused the accumulation of its substrate, malate, in the exocarp. In addition to inhibition of glycolysis-related gene expression and reduction of the activities of the corresponding enzymes, increased amino acid synthesis and decreased sugar abundance were also observed in these lines. The opposite effect was found in CsNADP-ME2-overexpressing lines, suggesting that there may be a continuous bottom-up feedback regulation of glycolysis in cucumber fruits. Overall, our studies indicate that CsNADP-ME2 may play potential roles in both central carbon reactions and amino acid metabolism in cucumber fruits.