Magnesium Signaling in Plants

Abstract

Free magnesium (Mg²⁺) is a signal of the adenylate (ATP+ADP+AMP) status in the cells. It results from the equilibrium of adenylate kinase (AK), which uses Mg-chelated and Mg-free adenylates as substrates in both directions of its reaction. The AK-mediated primary control of intracellular [Mg²⁺] is finely interwoven with the operation of membrane-bound adenylate- and Mg²⁺-translocators, which in a given compartment control the supply of free adenylates and Mg²⁺ for the AK-mediated equilibration. As a result, [Mg²⁺] itself varies both between and within the compartments, depending on their energetic status and environmental clues. Other key nucleotide-utilizing/producing enzymes (e.g., nucleoside diphosphate kinase) may also be involved in fine-tuning of the intracellular [Mg²⁺]. Changes in [Mg²⁺] regulate activities of myriads of Mg-utilizing/requiring enzymes, affecting metabolism under both normal and stress conditions, and impacting photosynthetic performance, respiration, phloem loading and other processes. In compartments controlled by AK equilibrium (cytosol, chloroplasts, mitochondria, nucleus), the intracellular [Mg²⁺] can be calculated from total adenylate contents, based on the dependence of the apparent equilibrium constant of AK on [Mg²⁺]. Magnesium signaling, reflecting cellular adenylate status, is likely widespread in all eukaryotic and prokaryotic organisms, due simply to the omnipresent nature of AK and to its involvement in adenylate equilibration.

Keywords: adenylate energy charge; adenylate kinase; cellular magnesium; free magnesium; nucleoside diphosphate kinase; thermodynamic buffering.

Figure 1

Effects of Mg²⁺ on Mg-chelation with adenylates and PP_i. (A) The ratios of free and Mg-bound adenylates, depending on [Mg²⁺]. (B) The percentage of free and Mg-chelated PP_i, depending on [Mg²⁺]. All lines were drawn according to the values of stability constants for chelation of adenylates and PP_i with Mg [15], using Origin software (OriginLab Corporation, Northampton, MA, USA).

Figure 2

Effects of [Mg²⁺] on K_app and K_true of AK. The K_app peaks at ca. 0.2 mM Mg²⁺. Please note that the scale on X-axis is logarithmic. The lines for K_app (blue) and K_true (red) were computed as described in ref 55, using Origin software (OriginLab Corporation, Northampton, MA, USA).

Figure 3

Distribution of Mg²⁺ transporters in membranes in plants. All transporters shown here have been identified in Arabidopsis [83]. The light-grey area corresponds to compartments where AK equilibrium is established. Numbers correspond to: (1) MGT5; (2) MGT10; (3) MGT1, MGT5, MGT6, MGT9; (4) MGT4, MGT7; (5) MGT2, MGT3; and (6) MHX. Question marks refer to transporters involved in Mg²⁺ export from a given compartment/cell; their nature remains unclear. Abbreviations: C, cytosol; CW, cell wall; ER, endoplasmic reticulum; M, mitochondrion; N, nucleus; P, plastid; PM, plasma membrane; V, vacuole.

Figure 4

Distribution of major adenylate carriers in membranes in plants. The names of the transporters and major transported molecules are as they are given by da Fonseca-Pereira et al. [99]. The light-grey area corresponds to compartments where AK equilibrium is established. Numbers correspond to: (1) AtBT1, Arabidopsis thaliana ATP/ADP/AMP carrier; (2) ATP/ADP carrier; (3) TAAC/PAPST1; (4) ZmBT1, maize (Zea mays) plastid ADP-Glucose/ADP carrier; (5) NTT1-2, ATP/ADP carriers; (6) PM-ANT1; (7) PNC1-2, ATP/ADP carrier; (8) AAC1-3, ATP/ADP carriers; (9) APC1-3, MgATP/P_i carriers; (10) ZmBT1, maize mitochondrial transporter, the substrate and transport mode of which are unclear; (11) ADNT1, AMP/ATP carrier; (12) AtBT1, ATP/ADP/AMP carrier; and (13) ER-ANT1, ATP/ADP carrier. Abbreviations: C, cytosol; CW, cell wall; ER, endoplasmic reticulum; M, mitochondrion; N, nucleus; P, plastid; PAP, 3’-phosphoadenosine 5’-phosphate; PAPS, 3’-phosphoadenosine 5’-phosphosulfate; PM, plasma membrane; Px, peroxisome.

Figure 5

A simplified view of the Mg²⁺ role as enzyme substrate/cofactor and as a signal arising from adenylate pools. Abbreviations: AK, adenylate kinase; Δμ_H+, membrane electrochemical potential; ETC, electron transport chain. Red dotted arrows refer to feedback control by Mg²⁺.