Pyrophosphate as an alternative energy currency in plants

Abstract

In the conditions of [Mg2+] elevation that occur, in particular, under low oxygen stress and are the consequence of the decrease in [ATP] and increase in [ADP] and [AMP], pyrophosphate (PPi) can function as an alternative energy currency in plant cells. In addition to its production by various metabolic pathways, PPi can be synthesized in the combined reactions of pyruvate, phosphate dikinase (PPDK) and pyruvate kinase (PK) by so-called PK/PPDK substrate cycle, and in the reverse reaction of membrane-bound H+-pyrophosphatase, which uses the energy of electrochemical gradients generated on tonoplast and plasma membrane. The PPi can then be consumed in its active forms of MgPPi and Mg2PPi by PPi-utilizing enzymes, which require an elevated [Mg2+]. This ensures a continuous operation of glycolysis in the conditions of suppressed ATP synthesis, keeping metabolism energy efficient and less dependent on ATP.

Catalytic Asymmetry in Homodimeric H+-Pumping Membrane Pyrophosphatase Demonstrated by Non-Hydrolyzable Pyrophosphate Analogs

“…All K + -independent mPPases are H + transporters, whereas the K + -dependent family is more diverse, and includes mPPases that, depending on Na + concentration, can transport either Na + or both Na + and H + [4]. An increasing body of evidence indicates that mPPases contribute to the tolerance of plants and the bacteria that live in harsh conditions to abiotic stress, such as salination, drought, cold, anoxia, and nutrient limitation [9][10][11][12]. mPPase functions in parallel with F-type ATPase, its highly evolved analog, which couples the same transport reactions with ATP synthesis/hydrolysis.…”

A Lumenal Loop Associated with Catalytic Asymmetry in Plant Vacuolar H+-Translocating Pyrophosphatase

“…The current view is that vacuolar mPPase does not act as a unidirectional H + pump-like V-ATPase but maintains a cytoplasmic PP i level by hydrolyzing or synthesizing it depending on the cell status [ 39 , 40 ]. PP i is a vital regulator and alternative energy source present in relatively high concentrations in plant cell cytosol [ 7 , 41 ]. By sensing PP i in the cytoplasm and H + in the lumen, loop 2–3 may work as a “clutch” that determines the direction in which mPPase works.…”

Effects of Magnesium, Pyrophosphate and Phosphonates on Pyrophosphorolytic Reaction of UDP-Glucose Pyrophosphorylase

“…PP i -dependent reactions are frequently more active, when cytosolic [Mg 2+ ] increases and when energy supply in the form of nucleoside triphosphates (e.g., ATP, UTP) is limited, as in anoxia/hypoxia [3,4,32]. An excess of [Mg 2+ ] over total [PP i ] appears to be a key requirement for the involvement of MgPPi, rather than free PP i , as substrate not only in the case of UGPase, but also for PP i -dependent phosphofructokinase [33], the latter being actually inhibited by free PP i [34].…”

“…MgPP i complexes are true substrates for both H + -pumping and non-proton-pumping pyrophosphatases [22,36]. Interactions between Mg 2+ and PP i /nucleotides and their role as substrates and regulators of cellular metabolism have been discussed in more detail in our recent works [4,7,14].…”

“…UDP-glucose (UDPG) pyrophosphorylase (UGPase) is a freely reversible enzyme that uses glucose-1-P (Glc-1-P) and uridine-triphosphate (UTP) in its forward (synthesis) reaction and UDPG and inorganic pyrophosphate (PP i ) in the reverse direction (pyrophosphorolysis) [1,2]. Both the synthesis and pyrophosphorolysis reactions of UGPase are deemed essential for plants, with the former providing UDPG for hundreds of glycosylation reactions, and the pyrophosphorolysis reaction involved in energy production (UTP) [3,4] and providing carbon skeletons in the sucrose-to-starch pathway in certain non-photosynthetic tissues [5][6][7]. For both directions of the reaction, it has been reported that magnesium is required for activity [1,[8][9][10].…”