Trends in Plant Science
Volume 18, Issue 9, September 2013, Pages 496-504
Journal home page for Trends in Plant Science

Review
Regulation of cytoskeletal dynamics by phospholipase D and phosphatidic acid

https://doi.org/10.1016/j.tplants.2013.04.005Get rights and content

Highlights

  • Phosphatidic acid and phospholipase D are key regulators of cytoskeletal organization.

  • Two cytoskeletal-associated proteins have been identified as PA-binding proteins.

  • Genetic evidence indicates that CP and MAP65-1 are PA sensors in live plant cells.

  • Emerging models for PLD–PA–cytoskeleton crosstalk are highlighted.

Plants respond to diverse biotic and abiotic stimuli as well as to endogenous developmental cues. Many of these stimuli result in altered activity of phospholipase D (PLD), an enzyme that hydrolyzes structural phospholipids producing phosphatidic acid (PA). PA is a key signaling intermediate in animals, but its targets in plants are relatively uncharacterized. Recent studies have demonstrated that the cytoskeleton is a major target of PLD–PA signaling and identified a positive feedback loop between actin turnover and PLD activity. Moreover, two cytoskeletal proteins, capping protein and MAP65-1, have been identified as PA-binding proteins regulating actin and microtubule organization and dynamics. In this review, we highlight the role of the PLD–PA module as an important hub for housekeeping and stress-induced regulation of membrane-associated cytoskeletal dynamics.

Section snippets

Linking lipid signaling with the cytoskeleton

The cytoskeleton serves as a molecular scaffold to position various cellular constituents, such as membrane-bound organelles and multiprotein complexes. It also serves as a highway for the transport of various cargoes by molecular motor proteins, and underpins cellular architecture and cell shape control. In plants, the cytoskeleton comprises two main components: actin filaments or F-actin, formed from actin monomers (G-actin); and microtubules polymerized from α/β tubulin heterodimers. Actin

PA production and its biophysical properties

PA represents the simplest phospholipid, comprising a diacylglycerol (DAG) hydrophobic body and a single phosphate group as the polar hydrophilic headgroup. There are numerous PA species with different lengths and degrees of fatty acyl chain saturation, which confers specific functional consequences [24]. A characteristic feature of all signaling phospholipids is their rapid and tightly regulated turnover. Apart from de novo PA synthesis and acylation of lyso-PA, there are two major, distinct

PA and the actin cytoskeleton

Several studies published over the past decade have shown that alteration of cellular PA levels can have a marked effect on actin cytoskeleton organization 17, 33, 34, 35, 36, 37, 38. The inhibition of PA production via PLD activity by n-butanol treatment causes disruption of actin filaments, whereas elevation of the PA level (by either exogenously added PA or the inhibition of PA phosphatase activity) increases the density of actin filaments consistent with actin assembly or stabilization 38,

PA and the microtubule cytoskeleton

Both PA and PLD have been identified as important regulators of microtubule array rearrangements and plasma membrane–microtubule cytoskeleton interactions 11, 20, 60, 61, 62. Similar to the actin cytoskeleton, microtubule arrays are also sensitive to the alteration of cellular PA levels. Applying n-butanol to tobacco Bright Yellow 2 (BY-2) suspension cells and Arabidopsis seedlings results in substantial cortical microtubule reorganization and/or depolymerization 34, 60, 61, 63, 64. Further, N

Concluding remarks

During the past decade, multifaceted interactions between PA-based signaling pathways and actin and microtubule dynamics have been revealed. Several studies have described the mechanism of PLD–PA interaction with actin and microtubule cytoskeletons, at varying levels of resolution. We propose a simplified model for the positive feedback loop that governs local actin polymerization status via PLD, PA, and CP (Figure 2). This model is corroborated by results showing for the first time that CP is

Acknowledgments

Research on CP in the Staiger laboratory is funded through a grant (DE-FG02-09ER15526) from the Physical Biosciences Program of the Office of Basic Energy Sciences, US Department of Energy. Phospholipid signaling research in the Žárský laboratory is supported by a grant (GACR 13-19073S to M.P.) from the Czech Grant Agency.

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