Changes and response mechanism of sugar and organic acids in fruits under water deficit stress

Abstract

The content and the ratio of soluble sugars and organic acids in fruits are significant indicators for fruit quality. They are affected by multiple environmental factors, in which water-deficient is the most concern. Previous studies found that the content of soluble sugars and organic acids in fruit displayed great differences under varied water stress. It is important to clarify the mechanism of such difference and to provide researchers with systematic knowledge about the response to drought stress and the mechanism of sugar and acid changes in fruits, so that they can better carry out the study of fruit quality under drought stress. Therefore, the researchers studied dozens of research articles about the content of soluble sugar and organic acid, the activity of related metabolic enzymes, and the expression of related metabolic genes in fruits under water stress, and the stress response of plants to water stress. We found that after plants perceived and transmitted the signal of water deficit, the expression of genes related to the metabolism of soluble sugars and organic acids changed. It was then affected the synthesis of metabolic enzymes and changed their metabolic rate, ultimately leading to changes in soluble sugar and organic acid content. Based on the literature review, we described the pathway diagrams of sugar metabolism, organic acid metabolism, mainly malic acid, tartaric acid, and citric acid metabolism, and of the response to drought stress. From many aspects including plants' perception of water stress signal, signal conversion and transmission, induced gene expression, the changes in soluble sugar and the enzyme activities of organic acids, as well as the final sugar and acid content in fruits, this thesis summarized previous studies on the influence of water stress on soluble sugars and the metabolism of organic acids in fruits.

Keywords: Enzyme activity; Gene expression; Signal transduction; Sugar and acid metabolism; Water stress.

Figure 1. Sugar metabolism in fruit cell under water stress.

The red circles indicate elevated fructose and glucose content (Rahmati et al., 2015; Alcobendas et al., 2013; Wang et al., 2019), while the green arrows represent enhanced activity of SS, SPS, vAINV, NAD⁺-SDH and SOX under water stress (Hockema & Etxeberria, 2001; Lu, Li & Jiang, 2009; Li et al., 2019; Wang et al., 2019). With enhanced SS activity, the rate of sucrose-fructose interconversion was accelerated (Hockema & Etxeberria, 2001), but SPP catalyzed irreversible reactions leading to sucrose-to-fructose conversion (Huber & Huber, 1996); with enhanced NAD⁺-SDH activity, the rate of sorbitol conversion to fructose was accelerated (Li & Li, 2005); with enhanced SPS activity, the rate of Sucrose-6-phosphate synthesis and decomposition was accelerated (Yang et al., 2002; Cornic, Ghashghaie & Fresneau, 2007), and due to enhanced SS activity, the rate of Sucrose-6-phosphate to sucrose, resulting in SPS-catalyzed Sucrose-6-phosphate synthesis, and the above reasons led to the increase of fructose content. The sorbitol transported into the fruit, due to the enhanced activity of SOX and NADP⁺-SDH (Li & Li, 2005; Wang et al., 2019), the conversion of sorbitol to glucose and the increase of glucose content.

Figure 2. The synthesis of tartaric acid in grape.

The initial substrate of tartaric acid synthesis is ascorbic acid, and the synthesis reaction takes place in the fragment of ascorbic acid C4-C5, and tartaric acid in grapes is synthesized through the intermediate metabolic pathways (Jia et al., 2019). The related enzymes mainly include 2-KGR, L-IDN DH, TK and TSAD, among which L-IDN DH is the rate-limiting enzyme. The process of 2-KGA synthesis by AsA is not clear. 2-KGA is reduced to L-Idn by 2-KGR (Jia et al., 2019), then L-IDO is oxidized to 5-KGA by L-Idn DH (Debolt, 2006). TK catalyzes the cleavage of 5-KGA between C4 and C5 to produce L-TT and Gly. Finally, L-TT generates TA by the catalysis of TSAD (Debolt, 2006).

Figure 3. Malate metabolism in fruit cell under water stress.

The red font: material accumulation (Jiang et al., 2014). Dark blue dashed arrows: omission of the multiple reaction process of the substrate formation product; red arrow: inhibition of related metabolic enzyme activities. Under water stress, ACO, IDH and MDH enzyme activities are inhibited and citrate, isocitrate and malate metabolism rates are reduced (Jiang et al., 2014), leading to accumulation. Malate was translocated to vacuole storage and its content increases.

Figure 4. Cirrate metabolism in fruit cell under water stress.

The red font: material accumulation (Jiang et al., 2014). Dark blue dashed arrows: omission of the multiple reaction process of the substrate formation product; red arrow: inhibition of related metabolic enzyme activities; red dashed arrows: multiple reaction processes in which the substrate forms a product are omitted and the catalyticase activity of at least one step of the reaction is inhibited. Under water stress, ACO, IDH and MDH enzyme activities are inhibited and citrate, isocitrate and malate metabolism rates are reduced (Jiang et al., 2014), leading to accumulation. Citrate was transported to the cytoplasm for metabolism.

Figure 5. Signal transduction from root to fruit and water stress response in the root cell.

Water stress is translated into osmotic stress, mechanical stress and oxidative stress (Gong et al., 2020; Niedzwiedz-Siegien et al., 2004; Cao et al., 2015). Mechanical stress triggered by cellular water loss is recognized by phospholipase C (PLC) and stretch channels and on the plasma membrane, and osmotic stress is recognized by mitogen-activated protein kinase (MAPK), leading to an increase in intracellular free Ca²⁺ concentration and the production of reactive oxygen species (ROS) (Gong et al., 2020; Dastogeer et al., 2017). In addition, water stress increases intracellular inositol (1,4,5)-trisphosphate (IP3) and ABA synthesis, which induces endoplasmic reticulum Ca²⁺ entry into the cytoplasm. High intracellular concentrations of ABA and Ca²⁺-receiving calmodulin caused reversible phosphorylation of proteins (Iwata et al., 1998), induced gene expression, and caused changes in sugar and acids metabolism.