Abstract
Inositol polyphosphates are ubiquitous molecular signals in metazoans, as are their pyrophosphorylated derivatives that bear a so-called ‘high-energy’ phosphoanhydride bond. A structural rationale is provided for the ability of Arabidopsis inositol tris/tetrakisphosphate kinase 1 to discriminate between symmetric and enantiomeric substrates in the production of diverse symmetric and asymmetric myo-inositol phosphate and diphospho-myo-inositol phosphate (inositol pyrophosphate) products. Simple tools are applied to chromatographic resolution and detection of known and novel diphosphoinositol phosphates without resort to radiolabeling approaches. It is shown that inositol tris/tetrakisphosphate kinase 1 and inositol pentakisphosphate 2-kinase comprise a reversible metabolic cassette converting Ins(3,4,5,6)P4 into 5-InsP7 and back in a nucleotide-dependent manner. Thus, inositol tris/tetrakisphosphate kinase 1 is a nexus of bioenergetics status and inositol polyphosphate/diphosphoinositol phosphate metabolism. As such, it commands a role in plants that evolution has assigned to a different class of enzyme in mammalian cells. The findings and the methods described will enable a full appraisal of the role of diphosphoinositol phosphates in plants and particularly the relative contribution of reversible inositol phosphate hydroxykinase and inositol phosphate phosphokinase activities to plant physiology.
Highlights
Myo-inositol hexakisphosphate (InsP6) is the predominant form of phosphorus storage molecule in plants, where in storage organs and tissues it may accumulate to several percent of dry weight [1]
In light of the consistent pattern of phosphorylation of 3- and 1- hydroxyls of Ins(1,4,1D-myo-inositol 3 (6)P3)/Ins(1,4,5,6)P4 and Ins(3,4,6)P3/Ins(3,4,5,6)P4 pairs, respectively, we modeled the binding of the enantiomers Ins(1,4,5,6)P4 and Ins(3,4,5,6)P4 (to ITPK1 (Figure 4))
Because diphosphoinositol phosphates have garnered attention as a cellular signal of eukaryotic energy status, reviewed [42,57,58], the recent works [12,13] focus attention on 5-InsP7 as an agent of energy signaling in plants
Summary
Myo-inositol hexakisphosphate (InsP6) is the predominant form of phosphorus storage molecule in plants, where in storage organs and tissues it may accumulate to several percent of dry weight [1]. The enzymology of InsP6 synthesis extends to families of enzymes collectively capable of phosphorylating all six hydroxyls of the inositol ring [2]. These include inositol kinase [3] and assorted inositol phosphate (hydroxy) kinases, including inositol 1,3,4-trisphosphate 5/6-kinases, known as inositol tris/tetrakisphosphate kinases, ITPKs [4,5,6]; inositol polyphosphate kinases [7], commonly called IPK2 after the yeast ortholog [8] and inositol pentakisphosphate 2-kinases [9], commonly called IPK1, again after the yeast ortholog [8]. Ins(3,4,5,6)P4 is the dominant InsP4 isomer in Atipk mutants which over-accumulate phosphate [11]. Others have shown that synthesis of 1,5-InsP8
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