Elsevier

Plant Science

Volume 181, Issue 4, October 2011, Pages 387-400
Plant Science

Review
Myo-inositol and beyond – Emerging networks under stress

https://doi.org/10.1016/j.plantsci.2011.07.009Get rights and content

Abstract

Myo-inositol is a versatile compound that generates diversified derivatives upon phosphorylation by lipid-dependent and -independent pathways. Phosphatidylinositols form one such group of myo-inositol derivatives that act both as membrane structural lipid molecules and as signals. The significance of these compounds lies in their dual functions as signals as well as key metabolites under stress. Several stress- and non-stress related pathways regulated by phosphatidylinositol isoforms and associated enzymes, kinases and phosphatases, appear to function in parallel to coordinatively adapt growth and stress responses in plants. Recent evidence also postulates their crucial roles in nuclear functions as they interact with the key players of chromatin structure, yet other nuclear functions remain largely unknown. Phosphatidylinositol monophosphate 5-kinase interacts with and represses a cytosolic neutral invertase, a key enzyme of sugar metabolism suggesting a crosstalk between lipid and sugar signaling. Besides phosphatidylinositol, myo-inositol derived galactinol and associated raffinose-family oligosaccharides are emerging as antioxidants and putative signaling compounds too. Importantly, myo-inositol polyphosphate 5-phosphatase (5PTase) acts, depending on sugar status, as a positive or negative regulator of a global energy sensor, SnRK1. This implies that both myo-inositol- and sugar-derived (e.g. trehalose 6-phosphate) molecules form part of a broad regulatory network with SnRK1 as the central regulator. Recently, it was shown that the transcription factor bZIP11 also takes part in this network. Moreover, a functional coordination between neutral invertase and hexokinase is emerging as a sweet network that contributes to oxidative stress homeostasis in plants. In this review, we focus on myo-inositol, its direct and more downstream derivatives (galactinol, raffinose), and the contribution of their associated networks to plant stress tolerance.

Highlights

► The role of myo-inositol and its derivatives in abiotic stress tolerance. ► Emerging links between phosphatidylinositol and sugar metabolism. ► A putative signaling role for galactinol and RFOs during stress tolerance. ► Mitochondrial ROS homeostasis by neutral invertase and hexokinase. ► Putative links between SnRK1, sugar and lipid metabolism.

Introduction

Since its first isolation [1], inositol (cyclohexanehexol) has become a crucial component in cellular biology. Nine different stereoisomeric forms can be distinguished. Seven of these are known to occur in nature, the exceptions being epi- and allo-inositol. Myo-, chiro- and scyllo-inositols constitute the major stereoisomers in plants (Fig. 1). However, muco- and neo-inositols were reported in some plant species as well [2]. Many eukaryotes use inositol-based cytosolic solutes as protective compounds under stress conditions. Furthermore, inositols are essential for growth in many yeast, fungi and plants [2]. Inositols and their phosphates lack a hydrolytically labile glycosidic linkage and therefore they are rather stable and less vulnerable to degradative enzymes in vivo.

Myo-inositol (hereafter referred to as ‘Ins’) is the most abundant isoform in biological systems and occupies a central position in inositol metabolism [3]. The six-carbon ring of Ins harbors one axial hydroxyl (at the D-2 position) and five equatorial hydroxyl groups (Fig. 1). Other biological inositols were proposed to be made from Ins by simple epimerization (inversion of the configuration) of some Ins hydroxyls [4]. However, a great diversity of Ins derivatives is generated by attaching multiple combinations of mono- and pyrophosphate groups to each of the hydroxyl moieties. Further complexity comes from the incorporation of these derivatives in lipid head groups. To date, more than 37 distinct Ins derivatives have been identified in biological systems exhibiting diversified functions, including roles in stress responses and cellular signaling [5].

Ins biosynthesis involves a highly conserved two-step biochemical pathway (also known as Loewus pathway [6]), in all living organisms and is catalyzed by a D-myo-inositol 3-phosphate synthase (MIPS) [7]. MIPS converts d-glucose-6-P to myo-inositol-3-phosphate (Ins3P). This is subsequently followed by dephosphorylation by a specific Mg2+-dependent inositol mono-phosphate phosphatase to form free Ins (Fig. 2A). MIPS enzymes have been reported from more than 70 different organisms and share an evolutionary conserved core catalytic domain across phyla [3]. Plants possess multiple MIPS genes [7], in contrast to yeast and animals that contain only one gene [8], suggesting functional divergence of MIPS genes in plants.

Ins can be used to generate: (1) phosphatidylinositol (PtdIns) and its derivatives (Fig. 2A); (2) Ins polyphosphates (InsPs; Fig. 2B) and (3) compatible solutes such as galactinol, raffinose-family oligosaccharides (RFOs), pinitol and cell wall polysaccharides (Fig. 2C). These Ins-derived compounds participate in several crucial plant cellular functions including: signal transduction [9], [10], membrane trafficking [11], mRNA export [12], stress tolerance [13], [14], and phosphorus storage [11], [15], [16]. In addition, the primary breakdown product of Ins, d-glucuronic acid, is utilized in the synthesis of various cell wall pectic and non-cellulosic compounds and ascorbic acid [6], [17], [18], [19]. Therefore, Ins takes a central position in cellular metabolism.

In this review, we discuss the roles of specific Ins derivatives linked to sugar metabolism and (a)biotic stress tolerance. To this end, we also provide putative roles for SnRK1 (sucrose non-fermenting-1-related protein kinase-1) linking Ins, sugar and energy metabolism in plants. For more comprehensive information on specific Ins derivatives, we suggest readers to go through some recent reviews [5], [7], [9], [10], [11], [18], [21], [24], [26], [29], [38], [46].

Section snippets

Phosphatidylinositol (PtdIns) derivatives

Ins derivatives (Fig. 2) represent a large family of molecules with diversified functions. They are present both as lipids and as water-soluble compounds. Phosphatidylinositol synthase (PIS) couples Ins (via its C1) to the backbone of a glycerophospholipid to create the simplest PtdIns (Fig. 2A). Next, distinct lipid kinases can phosphorylate three of five free hydroxyl groups of PtdIns (at the D-3, -4, and -5 positions) producing seven isomers with unique structural identity and functions,

Phosphatidylinositol 5-phosphate – a chromatin modifier under stress

Monophosphorylated isomers of PtdIns, such as PtdIns3P, PtsIns4P and PtdIns5P are implicated in growth and development of plants. These are widely distributed in various subcellular compartments [9], [67], [68], [52], [69] suggesting that these lipids might also be involved in distinct stress signaling pathways. All mono- and bisphosphorylated combinations represent less than 1% of the total phospholipids in a cell. Both PtdIns3P and PtdIns4P are involved in ABA-induced stomata closing via

Invertases and hexokinase – an emerging sweet link

Invertases hydrolyze sucrose into the hexose sugars glucose and fructose. Invertases are classified, based on their subcellular localization and pH optimum, into two isoforms: glycosylated acid-invertases of glycoside hydrolase family 32 (GH32), localized either in the apoplast (CWINVs) or in the vacuole (VINVs) and non-glycosylated alkaline/neutral INVs (A/N-INVs) of GH100 [128]. The A/N-INVs are unique to photosynthetic bacteria and plants [129], [130]. However, in silico and phylogenetic

SnRK1 – a central integrator linking sugar, Ins and energy metabolism

SnRK1 (Snf1-Related Protein Kinase-1) is a protein kinase possessing a catalytic domain mirroring the Snf1 (sucrose non-fermenting-1) of yeast and AMPK (AMP-activated protein kinase) of animals. They are well-conserved serine/threonine kinases acting as metabolic sensors [143], [144]. Three classes of SnRKs (1, 2 and 3) have been described in plants. SnRK2 and 3 do not complement yeast snf1 mutants [153], [156]. Two Arabidopsis protein kinases, KIN10 and KIN11 are the closest relatives of Snf1

Concluding remarks

Ins and its derivatives are an emerging family of compounds that are crucial for development and signaling in plants. They essentially function as either metabolic mediators or participate in various signaling pathways in response to stress, hormones, and nutrients, by transcriptional regulation of the stimuli-responsive genes. In addition, the downstream metabolites and the associated pathways are enormous, which function in a highly coordinated manner contributing to stress tolerance in

Acknowledgements

R. Valluru acknowledges postdoctoral fellowship from Institut National de la Recherche Agronomique (INRA), France

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