Phosphoinositides and phosphatidic acid regulate pollen tube growth and reorientation through modulation of [Ca2+]c and membrane secretion

Abstract

The maintenance of a calcium gradient and vesicle secretion in the apex of pollen tubes is essential for growth. It is shown here that phosphatidylinositol-4,5-bisphosphate (PIP2) and D-myo-inositol-1,4,5-trisphosphate (IP3), together with phosphatidic acid (PA), play a vital role in the regulation of these processes. Changes in the intracellular concentration of both PIP2 and IP3 (induced by photolysis of caged-probes), modified growth and caused reorientation of the growth axis. However, measurements of cytosolic free calcium ([Ca2+]c) and apical secretion revealed significant differences between the photo-release of PIP2 or IP3. When released in the first 50 mum of the pollen tube, PIP2 led to transient growth perturbation, [Ca2+]c increases, and inhibition of apical secretion. By contrast, a concentration of IP3 which caused a [Ca2+]c transient of similar magnitude, stimulated apical secretion and caused severe growth perturbation. Furthermore, the [Ca2+]c transient induced by IP3 was spatially different causing a pronounced elevation in the sub-apical region. These observations suggest different targets for the two phosphoinositides. One of the targets is suggested to be PA, a product of PIP2 hydrolysis via phospholipase C (PLC) or phospholipase D (PLD) activity. It was found that antagonists of PA accumulation (e.g. butan-1-ol) and inhibitors of PLC and PLD reversibly halted polarity. Reduction of PA levels caused the dissipation of the [Ca2+]c gradient and inhibited apical plasma membrane recycling. It was also found to cause abolition of the apical zonation. These data suggest that phosphoinositides and phospholipids regulate tip growth through a multiple pathway system involving regulation of [Ca2+]c levels, endo/exocytosis, and vesicular trafficking.

Genome-wide analysis of the phospholipase D family in Oryza sativa and functional characterization of PLDβ1 in seed germination

“…Most PLD genes are induced by hormones (IAA, GA, ABA) or stress stimuli (salt and drought), indicating the possible involvement of PLDs in hormone effects and stress responses. In Arabidopsis, PLDs have been shown to be involved in multiple processes; for example, PLDα1 is involved in the signal transduction of ABA, GA, and ethylene, and in senescence, water loss and freezing tolerance; PLDδ1 is a positive regulator of stress response, and also acts as a bridge between the plasma membrane and microtubule [13,16]; PLDζ2 is involved in phosphorusdeficiency-induced root elongation and digalactosyldiacylglycerol accumulation [41,42], and is required for auxin response [26]. In rice, the distinct expression patterns of different PLD members in the presence of plant hormones and in stress responses reveal the multiple and specific roles Phospholipase D family in rice 892 npg of PLDs.…”

“…Treatment with the PLD-specific inhibitor 1-butanol results in inhibited seed germination, altered emergence of the radicle and cotyledons, and abnormal root elongation and pattern formation of root hairs [14,15]. It was also shown that PLD and PA are critical for pollen germination and pollen tube elongation; reduced production of PA by PLD resulted in inhibited pollen tube germination and tip growth, and altered apical polarity of the pollen tube [16]. In addition, the actin and microtubule structures were severely altered under 1-butanol treatment [14,[17][18][19].…”

Phosphatidic Acid Binds to Cytosolic Glyceraldehyde-3-phosphate Dehydrogenase and Promotes Its Cleavage in Arabidopsis

“…The cellular level of PA is increased under various stress conditions, such as treatments of abscisic acid (ABA) (4), osmotic stress (5-7), oxidative stress (8), pathogen infection (9,10), and cold and freezing conditions (11)(12)(13). In addition, PA is involved in regulating normal plant growth and development, particularly in roots (14,15) and pollen tubes (16,17).…”

Pollen Tube Growth Oscillations and Intracellular Calcium Levels Are Reversibly Modulated by Actin Polymerization

“…PIP 2 binds different actin binding proteins, including villin/gelsolin, and profilin (Yin and Janmey, 2003). IP 3 stimulates the release of Ca 21 from internal stores, and consequently may modulate the apical gradient of the ion (Franklin-Tong et al, 1996;Malhó , 1998;Monteiro et al, 2005). It seems pertinent to consider these growth-associated factors with the Rops, with which they may closely interact (Kost et al, 1999).…”