Mechanisms and regulation of organic acid accumulation in plant vacuoles

Abstract

In fleshy fruits, organic acids are the main source of fruit acidity and play an important role in regulating osmotic pressure, pH homeostasis, stress resistance, and fruit quality. The transport of organic acids from the cytosol to the vacuole and their storage are complex processes. A large number of transporters carry organic acids from the cytosol to the vacuole with the assistance of various proton pumps and enzymes. However, much remains to be explored regarding the vacuolar transport mechanism of organic acids as well as the substances involved and their association. In this review, recent advances in the vacuolar transport mechanism of organic acids in plants are summarized from the perspectives of transporters, channels, proton pumps, and upstream regulators to better understand the complex regulatory networks involved in fruit acid formation.

Fig. 1. Vacuolar proteins that are involved in the transport of organic acids.

The vacuolar transport of organic acids is mainly mediated by channels, carriers, and proton pumps. Carriers catalyze either the transport of a single solute or the coupled transport of two solutes. Carrier proteins can be involved in promoting diffusion and secondary active transport of counter-electrochemical potential gradients by pro-electrochemical potential gradients. Channel proteins are another class of transporters that differ from carrier proteins in that they are simply gated membrane protein channels for diffusion. Channels act as selective holes through which molecules or ions can diffuse across the membrane. Proton pumps catalyze the coupled transport of a solute with a chemical reaction, which allows X- to utilize the energy released by the hydrolysis of ATP or PPi (ΔGATP (or PPi) <0). These mechanisms allow ionic material (X-) to pass through the biofilm and are governed by the general principle of thermodynamics that the change in free energy (ΔG1-2) of the transport reaction must be negative. During the vacuole transport of organic acids: (1) Diffusion includes simple diffusion mediated by channels (C) (used to transport some cations such as Na⁺, K⁺, and Ca²⁺) and facilitated diffusion mediated by carriers (A, B) (which is the main mode of transport of organic acids from the cytoplasm to the vacuole). (2) Primary active transport is mediated by three types of pumps (D, E, F) on the vacuole. Proton entry into the vacuole provides good conditions for the transport of organic acids: acidic vacuolar pH and a positive electric potential gradient. (3) Secondary active transport is mediated by symports (C), which are mainly involved in the transport of citrate out of the vacuole

Fig. 2. Upstream regulators that are involved in the vacuolar transport of malate and vacuolar acidification in apple parenchyma cells.

The graphs above the blue dotted line show the positive regulators of MYB-bHLH-WD40 (MBW) complexes, including MdMYB1-MdbHLH3-MdTTG1 and MdMYB73-MdCIbHLH1-WD40, that are involved in malate accumulation and vacuolar acidification; the stabilities of these two MBW complexes can be affected by posttranslational modifications, such as phosphorylation and ubiquitination, in response to environmental stimuli. The graphs below the blue dotted line reveal the negative regulators of the MBW complex or protein phosphatases and kinases involved in malate accumulation and vacuolar acidification

Fig. 3. Upstream regulators that are involved in vacuolar acidification in petunia petal, citrus and grapevine fruit cells.

The graph to the left of the black dotted line shows the WRKY- MYB-bHLH-WD40 (WMBW) complex and ERF transcription factor that are involved in vacuolar acidification in petunia petal and citrus fruit cells. The graph to the right of the black dotted line reveals the WMBW complex that is involved in vacuolar acidification in grapevine fruit cells