Plant phosphoinositide signaling - dynamics on demand

doi:10.1016/j.bbalip.2016.02.013

Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids

Volume 1861, Issue 9, Part B, September 2016, Pages 1345-1351

https://doi.org/10.1016/j.bbalip.2016.02.013 Get rights and content

Highlights

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Plant phosphoinositides (PIs) are subject to dynamic control.
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A dynamic balance of biosynthesis and degradation of PIs can be rapidly perturbed.
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The subcellular distribution of plant PIs can be dynamic.
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Key steps of plant PI-metabolism might be regulated at the post-translational level.
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There is little evidence for rapid transcriptional control of plant PI-metabolism.

Abstract

Eukaryotic membranes contain small amounts of lipids with regulatory roles. An important class of such regulatory lipids are phosphoinositides (PIs). Within membranes, PIs serve as recruitment signals, as regulators of membrane protein function or as precursors for second messenger production, thereby influencing a multitude of cellular processes with key importance for plant function and development. Plant PIs occur locally and transiently within membrane microdomains, and their abundance is strictly controlled. To understand the functions of the plant PI-network it is important to understand not only downstream PI-effects, but also to identify and characterize factors contributing to dynamic PI formation. This article is part of a Special Issue entitled: Plant Lipid Biology edited by Kent D. Chapman and Ivo Feussner.

Section snippets

Complex control of membrane function - regulatory lipids

Cellular membranes of eukaryotic organisms serve a multitude of biological functions and many cellular processes occur at and within membranes. Examples include the exchange of metabolites or information across membranes, the controlled expansion or reduction of membrane area, the interaction of membranes with the cytoskeleton or the polarized distribution of peripheral or membrane-integral proteins. All these processes take place all the time, as aspects of normal cellular function.

The plant PI-network and its associated enzymes

The formation of PIs in plants resembles the situation in other eukaryotes. All PIs are derived from the phospholipid, PtdIns, by phosphorylation of different positions of its inositol headgroup [1], [2], [3]. Five out of seven known PIs have been detected in plants, as has previously been reviewed [4]. The presence of phosphatidylinositol 3,4-bisphosphate (PtdIns(3,4)P₂) and phosphatidylinositol 3,4,5-trisphosphate (PtdIns(3,4,5)P₃), which are known from other eukaryotic organisms, is still

The complexity of analyzing plant PI-levels

The in vitro characterization of enzymes involved in PI-formation (see previous paragraph) has given valuable insights to the players manifesting the PI network in plants. The analyses on recombinant enzymes have been complemented by in vivo studies on Arabidopsis mutants carrying defects in various of these enzymes, providing links between the formation of certain PIs and ensuing phenotypes in the living plant. Based on these phenotypes the control of numerous cellular processes has been

Dynamic changes in PI-levels

Dynamic changes in the levels of PIs have first been observed upon treatment of cell cultures and intact plants with salt or osmotic challenge. Early studies of PI dynamics have utilized unicellular algae as model systems, as some of these organisms display higher proportions of PIs in their membrane lipids than is found in more complex plants, such as Arabidopsis or the moss, Physcomitrella patens, aiding biochemical analysis. For instance, the unicellular halophilic alga, Dunaliella salina,

Dynamic changes in PI-distribution

The report that PIs formed in Arabidopsis upon stress may contain more unsaturated fatty acids compared to PIs formed under constitutive conditions [35], [36] may have relevance for the lateral distribution of PIs within cellular membranes. Examples from other biological systems indicate that PI-populations with distinct fatty acid patterns coexist [46] and it has been demonstrated that the degree of unsaturation of fatty acids can result in divergent association of lipids with planar or curved

PI-microdomains and cell polarity

It has been reported for several plant cell types that PIs may not distribute evenly within the plasma membrane but display pronounced polarization. A prime example is the distribution of PtdIns(4,5)P₂ in cells exhibiting polar tip growth, including pollen tubes and root hairs. The growth of pollen tubes [15], [50], [55], [56] and root hairs [17], [57] requires the formation of PtdIns(4,5)P₂. In pollen tubes PtdIns(4,5)P₂ accumulates in a subapical membrane domain close to the growing tip that

Control of plant PI formation and distribution: Regulation of enzyme activities

To elucidate functional aspects of dynamic PI changes, it is important to interfere with the dynamic formation of PIs and study the consequences. The enzymes likely responsible for a substantial portion of PtdIns4P or PtdIns(4,5)P₂ in non-challenged plants have been identified [61], [67]. However, the origin of stress-induced PIs is currently still unclear. It is possible that enzymes of PI-metabolism with housekeeping function are modulated in their activity upon perception of the stresses, as

Transcriptional regulation of PI metabolism

PI-formation is partially regulated at the transcriptional level, which controls the abundance of enzymes of PI-metabolism. For instance, different enzymes display tissue-specific expression patterns that may be restricted to roots [17], [57] or to pollen tubes [15], [16], [55], whereas other enzymes appear to be expressed at a constitutive basis [61], [62], [63]. Dynamic changes of the abundance of enzymes of PI metabolism that are based on transcriptional control have also been reported. For

Posttranslational modifications

In order to explain the dynamic changes in PI levels and underlying enzyme activities that have been reported, a fast mode of regulation must be assumed. Some of the activation events reported for plant cells subjected to salt stress occur within seconds to few minutes, additionally making a major involvement of transcriptional control unlikely. Instead, the fast dynamics suggest posttranslational activation of pre-existing enzymes. This assumption is consistent with the notion that PIs undergo

Localized potentiation of PI-biosynthesis through accessory proteins

Besides the control of catalytic activities or membrane association of enzymes of PI-metabolism, another mechanism to enable enhanced interconversion of PIs is by controlling substrate accessibility. In this context it has been proposed that Sec14-like proteins from Arabidopsis act as potentiators that bind to substrate lipids, such as PtdIns4P, and alter their sterical geometry within the membrane to facilitate the interaction with, e.g., PI4P 5-kinases [87], [88], [89]. This concept is

Conclusions

Overall, a substantial amount of evidence supports the notion that the plant PI-system undergoes dynamic changes in response to environmental stresses or as part of endogenous developmental programs. These dynamics are likely a consequence of the action of counteracting enzymes continuously generating and degrading PIs at high rates, establishing a dynamic equilibrium. This equilibrium is easily perturbed, enabling rapid increases in the levels of PIs upon stimulation. Perturbation of the

Conflict of interest

The author does not indicate a conflic of interest.

Transparency document

Transparency document.

Acknowledgements

The author would like to thank Dr. Mareike Heilmann (Martin-Luther-University Halle-Wittenberg, Germany) for helpful discussion and support with the review of transcriptomics data. Financial support from the German Research Foundation (grants He3424/2 and He3424/3) and from the European Regional Development Fund (EFRE) of the European Commission is gratefully acknowledged.

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View all citing articles on Scopus

^☆: This article is part of a Special Issue entitled: Plant Lipid Biology edited by Kent D. Chapman and Ivo Feussner.

View full text

ReviewPlant phosphoinositide signaling - dynamics on demand☆

Highlights

Abstract

Section snippets

Complex control of membrane function - regulatory lipids

The plant PI-network and its associated enzymes

The complexity of analyzing plant PI-levels

Dynamic changes in PI-levels

Dynamic changes in PI-distribution

PI-microdomains and cell polarity

Control of plant PI formation and distribution: Regulation of enzyme activities

Transcriptional regulation of PI metabolism

Posttranslational modifications

Localized potentiation of PI-biosynthesis through accessory proteins

Conclusions

Conflict of interest

Transparency document

Acknowledgements

Phosphoinositide-derived messengers in endocrine signaling

J. Endocrinol.

Green light for polyphosphoinositide signals in plants

Curr. Opin. Plant Biol.

Synthesis and function of membrane phosphoinositides in budding yeast, Saccharomyces cerevisiae

Biochim. Biophys. Acta

Plant phosphoinositides-complex networks controlling growth and adaptation

Biochim. Biophys. Acta

Inositol phospholipid metabolism in Arabidopsis. Characterized and putative isoforms of inositol phospholipid kinase and phosphoinositide-specific phospholipase C

Plant Physiol.

Identification of a phosphatidylinositol 3-hydroxy kinase in plant cells: association with the cytoskeleton

Biochem. J.

AtVSP34, a phosphatidylinositol 3-kinase of Arabidopsis thaliana, is an essential protein with homology to a calcium-dependent lipid binding domain

Proc. Natl. Acad. Sci. U. S. A.

Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting

Science

A phosphatidylinositol 4-kinase pleckstrin homology domain that binds phosphatidylinositol 4-monophosphate

J. Biol. Chem.

A plant 126-kDa phosphatidylinositol 4-kinase with a novel repeat structure. Cloning and functional expression in baculovirus-infected insect cells

J. Biol. Chem.

Characterization of a new family of protein kinases from Arabidopsis containing phosphoinositide 3/4-kinase and ubiquitin-like domains

Biochem. J.

Identification of a new polyphosphoinositide in plants, phosphatidylinositol 5-monophosphate (PtdIns5P), and its accumulation upon osmotic stress

Biochem. J.

Rapid structural changes and acidification of guard cell vacuoles during stomatal closure require phosphatidylinositol 3,5-bisphosphate

Plant Cell

Phosphatidylinositol 3-phosphate 5-kinase, FAB1/PIKfyve kinase mediates endosome maturation to establish endosome-cortical microtubule interaction in Arabidopsis

Plant Physiol.

Type B phosphatidylinositol-4-phosphate 5-kinases mediate pollen tube growth in Nicotiana tabacum and Arabidopsis by regulating apical pectin secretion

Plant Cell

Phosphatidylinositol-4,5-bisphosphate influences Nt-Rac5-mediated cell expansion in pollen tubes of Nicotiana tabacum

Plant J.

The type B phosphatidylinositol-4-phosphate 5-kinase 3 is essential for root hair formation in Arabidopsis thaliana

Plant Cell

Phosphatidylinositol specific phospholipase C of plant stems: membrane associated activity concentrated in plasma membranes

Plant Physiol.

Characterization of a polyphosphoinositide phospholipase C from the plasma membrane of Avena sativa

Plant Physiol.

Up-regulation of phosphoinositide metabolism in tobacco cells constitutively expressing the human type I inositol polyphosphate 5-phosphatase

Plant Physiol.

Expression and evolution of the phosphoinositide-specific phospholipase C gene family in Arabidopsis thaliana

Plant Physiol. Biochem.

Plant phosphoinositide-dependent phospholipases C: variations around a canonical theme

Biochimie

FRAGILE FIBER3, an Arabidopsis gene encoding a type II inositol polyphosphate 5-phosphatase, is required for secondary wall synthesis and actin organization in fiber cells

Plant Cell

Mutation of SAC1, an Arabidopsis SAC domain phosphoinositide phosphatase, causes alterations in cell morphogenesis, cell wall synthesis, and actin organization

Plant Cell

SAC phosphoinositide phosphatases at the tonoplast mediate vacuolar function in Arabidopsis

Proc. Natl. Acad. Sci. U. S. A.

Mutations in the Arabidopsis phosphoinositide phosphatase gene SAC9 lead to overaccumulation of PtdIns(4,5)P2 and constitutive expression of the stress-response pathway

Plant Physiol.

ROOT HAIR DEFECTIVE4 encodes a phosphatidylinositol-4-phosphate phosphatase required for proper root hair development in Arabidopsis thaliana

Plant Cell

A novel class of PTEN protein in Arabidopsis displays unusual phosphoinositide phosphatase activity and efficiently binds phosphatidic acid

Biochem. J.

Arranged marriage in lipid signalling? the limited choices of PtdIns(4,5)P in finding the right partner

Plant Biol. (Stuttg.)

Hyperosmotic stress induces rapid synthesis of phosphatidyl-D-inositol 3,5-bisphosphate in plant cells

Planta

Phosphoinositides in plants: novel functions in membrane trafficking

Curr. Opin. Plant Biol.

Review
Plant phosphoinositide signaling - dynamics on demand☆

Mutations in the Arabidopsis phosphoinositide phosphatase gene SAC9 lead to overaccumulation of PtdIns(4,5)P₂ and constitutive expression of the stress-response pathway