Inositol Pyrophosphate Pathways and Mechanisms: What Can We Learn from Plants?

Abstract

The ability of an organism to maintain homeostasis in changing conditions is crucial for growth and survival. Eukaryotes have developed complex signaling pathways to adapt to a readily changing environment, including the inositol phosphate (InsP) signaling pathway. In plants and humans the pyrophosphorylated inositol molecules, inositol pyrophosphates (PP-InsPs), have been implicated in phosphate and energy sensing. PP-InsPs are synthesized from the phosphorylation of InsP6, the most abundant InsP. The plant PP-InsP synthesis pathway is similar but distinct from that of the human, which may reflect differences in how molecules such as Ins(1,4,5)P3 and InsP6 function in plants vs. animals. In addition, PP-InsPs can potentially interact with several major signaling proteins in plants, suggesting PP-InsPs play unique signaling roles via binding to protein partners. In this review, we will compare the biosynthesis and role of PP-InsPs in animals and plants, focusing on three central themes: InsP6 synthesis pathways, synthesis and regulation of the PP-InsPs, and function of a specific protein domain called the Syg1, Pho1, Xpr1 (SPX ) domain in binding PP-InsPs and regulating inorganic phosphate (Pi) sensing. This review will provide novel insights into the biosynthetic pathway and bioactivity of these key signaling molecules in plant and human systems.

Inositol polyphosphates and target of rapamycin kinase signalling govern photosystem II protein phosphorylation and photosynthetic function under light stress in Chlamydomonas

“…Although PP‐InsPs have been previously linked to the control of intracellular ATP in yeast kcs1Δ mutants (Szijgyarto et al ., 2011), vip1 mutants have not previously been directly connected with this phenotype. While no IP6K homologue is found in algae or plants, the detection of InsP 8 (1,5(PP) 2 ‐InsP 4 ) suggests the presence of a functional IP6K enzyme (Desai et al ., 2014; Laha et al ., 2015; Couso et al ., 2016), or a noncanonical ITPK function (Cridland & Gillaspy, 2020) that could be regulating ATP levels in coordination with VIP1. Recently, VIP1 was also reported to have a bifunctional kinase/pyrophosphatase activity that produces and destroys 1‐PP‐InsPs at the expense of consuming ATP in yeast (Dollins et al ., 2020).…”

“…S1), in reactions catalysed by two distinct classes of enzymes: diphosphoinositol pentakisphosphate kinase (PPIP5K, known as VIH in plants and VIP1 in budding yeast and algae) and inositol hexakisphosphate kinase (IP6K, known as KCS1 in budding yeast) (Saiardi et al ., 1999; Saiardi, 2004; Mulugu et al ., 2007; Laha et al ., 2015; Couso et al ., 2016; Shears & Wang, 2019). IP6K is not conserved in green organisms; however ITPKs, which are responsible for the conversion of InsP 3 into InsP 5 , has recently been suggested to phosphorylate InsP 6 in vitro in Arabidopsis (Cridland & Gillaspy, 2020). Although, PP‐InsPs constitute a minor portion of the InsPs pool, they are suggested to play a fundamental role in controlling metabolism, interacting with SPX domain‐containing proteins that are connected to polyphosphate (Poly‐P) synthesis (Wild et al ., 2016; Gerasimaite et al ., 2017) and phosphate signalling in yeast, mammals, and plants (Saiardi, 2012a; Secco et al ., 2012; Livermore et al ., 2016; Wild et al ., 2016; Jung et al ., 2018; Zhu et al ., 2019; Li et al ., 2020; Ried et al ., 2021).…”

Globoids and Phytase: The Mineral Storage and Release System in Seeds

“…The synthesis of PP-InsP 6 can occur through an auxiliary catalytic activity of ITPK, which also participates in phytate biosynthesis (see Section 2.1 ). PP-InsP 6 is receiving increasing attention as a signal molecule in plants; for instance, in phosphate sensing [ 102 ]. The cofactor requirements of V-PPase further support a close association with the globoid content.…”

Bioactivity of Inositol Phosphates

“…IPs may also have distinctive properties in energy production, which is finely tuned to the metabolism and is known to be modulated by several signaling pathways, such as Akt/mTOR, in which IPs are key players [ 3 ]. Comparing plants and humans, Cridland and Gillaspy underline lessons we have learned from plants [ 4 ]. While eukaryotes have developed complex signaling pathways to adapt to a readily changing environment, in plants and humans, IPs have been implicated in phosphate and energy sensing.…”

“…The plant PP-IP synthesis pathway is similar, but distinct from that of the human, reflecting differences in how molecules such as IP 3 and IP 6 function in plants vs. animals. In this review, they compare IP 6 synthesis pathways, synthesis and regulation of the PP-IPs, and function of a specific protein domain called the Syg1, Pho1, Xpr1 (SPX) domain in binding PP-IPs and regulating inorganic phosphate sensing, providing novel insights into the biosynthetic pathway and bioactivity of these key signaling molecules in plant and human systems [ 4 ]. Of course, phosphorus (P) in plants is an essential nutrient, and IPs, particularly IP 6 , are important stores of P in plants.…”