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Ca2+ influx and phosphoinositide signalling are essential for the establishment and maintenance of cell polarity in monospores from the red alga Porphyra yezoensis.

Li L, Saga N, Mikami K - J. Exp. Bot. (2009)

Bottom Line: The results indicate that the inhibition of the establishment of cell polarity, as judged by the ability of F-actin to localize asymmetrically, cell wall synthesis, and development into germlings, occurred when monospores were treated with inhibitors of the Ca2+ permeable channel, phospholipase C (PLC), diacylglycerol kinase, and inositol-1,4,5-trisphosphate receptor.Moreover, it was also found that light triggered the establishment of cell polarity via photosynthetic activity but not its direction, indicating that the Ca2+ influx and PLC activation required for the establishment of cell polarity are light dependent.Taken together, these findings suggest that there is functional diversity between the PLC and PLD signalling systems in terms of the formation of cell polarity; the former being critical for the light-dependent establishment of cell polarity and the latter playing a role in the maintenance of established cell polarity.

View Article: PubMed Central - PubMed

Affiliation: Graduate School of Fisheries Sciences, Hokkaido University, Hakodate 041-8611, Japan.

ABSTRACT
The asymmetrical distribution of F-actin directed by cell polarity has been observed during the migration of monospores from the red alga Porphyra yezoensis. The significance of Ca2+ influx and phosphoinositide signalling during the formation of cell polarity in migrating monospores was analysed pharmacologically. The results indicate that the inhibition of the establishment of cell polarity, as judged by the ability of F-actin to localize asymmetrically, cell wall synthesis, and development into germlings, occurred when monospores were treated with inhibitors of the Ca2+ permeable channel, phospholipase C (PLC), diacylglycerol kinase, and inositol-1,4,5-trisphosphate receptor. Moreover, it was also found that light triggered the establishment of cell polarity via photosynthetic activity but not its direction, indicating that the Ca2+ influx and PLC activation required for the establishment of cell polarity are light dependent. By contrast, inhibition of phospholipase D (PLD) prevented the migration of monospores but not the asymmetrical localization of F-actin. Taken together, these findings suggest that there is functional diversity between the PLC and PLD signalling systems in terms of the formation of cell polarity; the former being critical for the light-dependent establishment of cell polarity and the latter playing a role in the maintenance of established cell polarity.

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Proposed model of the relationship between the PI signalling system and formation of cell polarity in monospores. PtdIns(4)P produced by PI4K from PtdIns is phosphorylated by PIPK to generate PtdIns(4,5)P2. PtdIns(4,5)P2 can be hydrolysed by PLC to generate the second messengers IP3 and DG. IP3 then binds IP3R, which results in the release of Ca2+ from the cytoplasm. The inhibition of PLC, DGK, and IP3R in addition to Ca2+ influx prevents the establishment of cell polarity. The catalysis of PLC and PI3K depends on Ca2+ influx, which is triggered by light irradiation. DG is converted to PA by DGK. PA is also produced from PC by PLD. PA activates PIPK to produce PtdIns(4,5)P2 as a precursor of the substrate of PLC and PtdIns(4,5)P2 activates PLD which hydrolyses PC to produce PA. According to the function of PLD, the positive regulatory circuit indicated by the box drawn with a dashed line is proposed for the maintenance of cell polarity. Pharmacological reagents and their actions are indicated by red characters and bars.
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fig6: Proposed model of the relationship between the PI signalling system and formation of cell polarity in monospores. PtdIns(4)P produced by PI4K from PtdIns is phosphorylated by PIPK to generate PtdIns(4,5)P2. PtdIns(4,5)P2 can be hydrolysed by PLC to generate the second messengers IP3 and DG. IP3 then binds IP3R, which results in the release of Ca2+ from the cytoplasm. The inhibition of PLC, DGK, and IP3R in addition to Ca2+ influx prevents the establishment of cell polarity. The catalysis of PLC and PI3K depends on Ca2+ influx, which is triggered by light irradiation. DG is converted to PA by DGK. PA is also produced from PC by PLD. PA activates PIPK to produce PtdIns(4,5)P2 as a precursor of the substrate of PLC and PtdIns(4,5)P2 activates PLD which hydrolyses PC to produce PA. According to the function of PLD, the positive regulatory circuit indicated by the box drawn with a dashed line is proposed for the maintenance of cell polarity. Pharmacological reagents and their actions are indicated by red characters and bars.

Mentions: The data presented above reveal that Ca2+ influx, the PI signalling system, and light are essential for the establishment and maintenance of cell polarity during the early development of monospores from the marine red alga P. yezoensis. The formation of cell polarity in directional cell migration or chemotaxis has been extensively studied in mammalian leukocytes and Dictyostelium cells (Affolter and Weijer, 2005; Bagorda et al., 2006), indicating the importance of signalling systems involving phosphatidylinositol kinases and phospholipases (Harris et al., 2008; Kölsch et al., 2008). In plants, however, knowledge about the importance of the PI signalling system in cell polarity is restricted to tip growth of pollen tubes, root hairs, and rhizoids (Gardiner et al., 2003; Helling et al., 2006; Peters et al., 2007). Our findings on migrating monospores using pharmacological inhibitors therefore provide new evidence of the critical roles of PI signalling in cell polarity formation in plants. Based on our findings, together with the involvement of light in the establishment of cell polarity (Fig. 5), it is hypothesized that light triggers the activation of Ca2+ permeable channels and/or PI3K, which follows PLC activation to establish the cell polarity required for the asymmetrical distribution of F-actin and PLD activation for the maintenance of cell polarity (Fig. 6). Similar functional diversity between PLC and PLD in polarity formation has recently been found in zygotes of a brown alga Silvetia compressa, in which inhibition of PLC signalling by R59022 disrupted polarization and the subsequent polar growth, including germination and cell division, with the formation of microtubule arrays, whereas inhibition of PLD with 1-butanol only affected cell division during polar growth (Peters et al., 2008).


Ca2+ influx and phosphoinositide signalling are essential for the establishment and maintenance of cell polarity in monospores from the red alga Porphyra yezoensis.

Li L, Saga N, Mikami K - J. Exp. Bot. (2009)

Proposed model of the relationship between the PI signalling system and formation of cell polarity in monospores. PtdIns(4)P produced by PI4K from PtdIns is phosphorylated by PIPK to generate PtdIns(4,5)P2. PtdIns(4,5)P2 can be hydrolysed by PLC to generate the second messengers IP3 and DG. IP3 then binds IP3R, which results in the release of Ca2+ from the cytoplasm. The inhibition of PLC, DGK, and IP3R in addition to Ca2+ influx prevents the establishment of cell polarity. The catalysis of PLC and PI3K depends on Ca2+ influx, which is triggered by light irradiation. DG is converted to PA by DGK. PA is also produced from PC by PLD. PA activates PIPK to produce PtdIns(4,5)P2 as a precursor of the substrate of PLC and PtdIns(4,5)P2 activates PLD which hydrolyses PC to produce PA. According to the function of PLD, the positive regulatory circuit indicated by the box drawn with a dashed line is proposed for the maintenance of cell polarity. Pharmacological reagents and their actions are indicated by red characters and bars.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC2724695&req=5

fig6: Proposed model of the relationship between the PI signalling system and formation of cell polarity in monospores. PtdIns(4)P produced by PI4K from PtdIns is phosphorylated by PIPK to generate PtdIns(4,5)P2. PtdIns(4,5)P2 can be hydrolysed by PLC to generate the second messengers IP3 and DG. IP3 then binds IP3R, which results in the release of Ca2+ from the cytoplasm. The inhibition of PLC, DGK, and IP3R in addition to Ca2+ influx prevents the establishment of cell polarity. The catalysis of PLC and PI3K depends on Ca2+ influx, which is triggered by light irradiation. DG is converted to PA by DGK. PA is also produced from PC by PLD. PA activates PIPK to produce PtdIns(4,5)P2 as a precursor of the substrate of PLC and PtdIns(4,5)P2 activates PLD which hydrolyses PC to produce PA. According to the function of PLD, the positive regulatory circuit indicated by the box drawn with a dashed line is proposed for the maintenance of cell polarity. Pharmacological reagents and their actions are indicated by red characters and bars.
Mentions: The data presented above reveal that Ca2+ influx, the PI signalling system, and light are essential for the establishment and maintenance of cell polarity during the early development of monospores from the marine red alga P. yezoensis. The formation of cell polarity in directional cell migration or chemotaxis has been extensively studied in mammalian leukocytes and Dictyostelium cells (Affolter and Weijer, 2005; Bagorda et al., 2006), indicating the importance of signalling systems involving phosphatidylinositol kinases and phospholipases (Harris et al., 2008; Kölsch et al., 2008). In plants, however, knowledge about the importance of the PI signalling system in cell polarity is restricted to tip growth of pollen tubes, root hairs, and rhizoids (Gardiner et al., 2003; Helling et al., 2006; Peters et al., 2007). Our findings on migrating monospores using pharmacological inhibitors therefore provide new evidence of the critical roles of PI signalling in cell polarity formation in plants. Based on our findings, together with the involvement of light in the establishment of cell polarity (Fig. 5), it is hypothesized that light triggers the activation of Ca2+ permeable channels and/or PI3K, which follows PLC activation to establish the cell polarity required for the asymmetrical distribution of F-actin and PLD activation for the maintenance of cell polarity (Fig. 6). Similar functional diversity between PLC and PLD in polarity formation has recently been found in zygotes of a brown alga Silvetia compressa, in which inhibition of PLC signalling by R59022 disrupted polarization and the subsequent polar growth, including germination and cell division, with the formation of microtubule arrays, whereas inhibition of PLD with 1-butanol only affected cell division during polar growth (Peters et al., 2008).

Bottom Line: The results indicate that the inhibition of the establishment of cell polarity, as judged by the ability of F-actin to localize asymmetrically, cell wall synthesis, and development into germlings, occurred when monospores were treated with inhibitors of the Ca2+ permeable channel, phospholipase C (PLC), diacylglycerol kinase, and inositol-1,4,5-trisphosphate receptor.Moreover, it was also found that light triggered the establishment of cell polarity via photosynthetic activity but not its direction, indicating that the Ca2+ influx and PLC activation required for the establishment of cell polarity are light dependent.Taken together, these findings suggest that there is functional diversity between the PLC and PLD signalling systems in terms of the formation of cell polarity; the former being critical for the light-dependent establishment of cell polarity and the latter playing a role in the maintenance of established cell polarity.

View Article: PubMed Central - PubMed

Affiliation: Graduate School of Fisheries Sciences, Hokkaido University, Hakodate 041-8611, Japan.

ABSTRACT
The asymmetrical distribution of F-actin directed by cell polarity has been observed during the migration of monospores from the red alga Porphyra yezoensis. The significance of Ca2+ influx and phosphoinositide signalling during the formation of cell polarity in migrating monospores was analysed pharmacologically. The results indicate that the inhibition of the establishment of cell polarity, as judged by the ability of F-actin to localize asymmetrically, cell wall synthesis, and development into germlings, occurred when monospores were treated with inhibitors of the Ca2+ permeable channel, phospholipase C (PLC), diacylglycerol kinase, and inositol-1,4,5-trisphosphate receptor. Moreover, it was also found that light triggered the establishment of cell polarity via photosynthetic activity but not its direction, indicating that the Ca2+ influx and PLC activation required for the establishment of cell polarity are light dependent. By contrast, inhibition of phospholipase D (PLD) prevented the migration of monospores but not the asymmetrical localization of F-actin. Taken together, these findings suggest that there is functional diversity between the PLC and PLD signalling systems in terms of the formation of cell polarity; the former being critical for the light-dependent establishment of cell polarity and the latter playing a role in the maintenance of established cell polarity.

Show MeSH