Inositol phosphate kinases in the eukaryote landscape.

Debabrata Laha,Yann Desfougères,Adolfo Saiardi,Paloma Portela-Torres

doi:10.1016/j.jbior.2020.100782

Abstract

Inositol phosphate encompasses a large multifaceted family of signalling molecules that originate from the combinatorial attachment of phosphate groups to the inositol ring. To date, four distinct inositol kinases have been identified, namely, IPK, ITPK, IPPK (IP5–2K), and PPIP5K. Although, ITPKs have recently been identified in archaea, eukaryotes have taken advantage of these enzymes to create a sophisticated signalling network based on inositol phosphates. However, it remains largely elusive what fundamental biochemical principles control the signalling cascade. Here, we present an evolutionary approach to understand the development of the ‘inositol phosphate code’ in eukaryotes. Distribution analyses of these four inositol kinase groups throughout the eukaryotic landscape reveal the loss of either ITPK, or of PPIP5K proteins in several species. Surprisingly, the loss of IPPK, an enzyme thought to catalyse the rate limiting step of IP6 (phytic acid) synthesis, was also recorded. Furthermore, this study highlights a noteworthy difference between animal (metazoan) and plant (archaeplastida) lineages. While metazoan appears to have a substantial amplification of IPK enzymes, archaeplastida genomes show a considerable increase in ITPK members. Differential evolution of IPK and ITPK between plant and animal lineage is likely reflective of converging functional adaptation of these two types of inositol kinases. Since, the IPK family comprises three sub-types IPMK, IP6K, and IP3–3K each with dedicated enzymatic specificity in metazoan, we propose that the amplified ITPK group in plant could be classified in sub-types with distinct enzymology.

Highlights

Living organisms took advantage of the metabolic stability and ease of synthesis of inositol to use it as osmolyte (Novak et al, 1999), and to create a vast family of intracellular messengers including the lipid-bound phosphoinositides (PIPs) and the soluble inositol phosphates (IPs)
Recent findings demonstrating the ability of isyna1− /− null cell to synthesize inositol suggest the existence of ISYNA1 independent pathway of inositol synthesis (Qiu et al, 2020)
We will briefly highlight the fate of the two sources of cellular inositol since it will give insight on phosphorylation events that are independent of IP kinases

Summary

Introduction

Living organisms took advantage of the metabolic stability and ease of synthesis of inositol to use it as osmolyte (Novak et al, 1999), and to create a vast family of intracellular messengers including the lipid-bound phosphoinositides (PIPs) and the soluble inositol phosphates (IPs). The molecular complexity of IPs signalling network is further augmented with the possibility to have pyro-phosphate group(s) attached to the inositol ring (Shah et al, 2017; Wilson et al, 2013) such as in IP7 and IP8, referred to as inositol pyrophosphates These highly polar and energy-rich species occupy the center stage of IPs research due to their key role in regulating a large array of fundamental cellular functions including energy metabolism, phosphate homeostasis and immune responses in yeasts, metazoans and plants (Azevedo and Saiardi, 2017; Dong et al, 2019; Laha et al, 2015; Li et al, 2020; Lopez-Sanchez et al, 2020; Wilson et al, 2019; Zhu et al, 2019). A major focus in the field is to establish novel methods allowing us to map the subcellular concentration as well as the molecular identity of different IPs (Qiu et al., 2020; Harmel et al, 2019; Ito et al, 2018; Losito et al, 2009; Wilson et al, 2015)

Methods

Results

Conclusion