Modulation of endocytosis in pollen tube growth by phosphoinositides and phospholipids

Monteiro, D.; Coelho, J.P.; Rodrigues, Cecília M.P.; Camacho, Luísa; Quader, H.; Malhó, Rui

doi:10.1007/s00709-005-0102-x

Cited by 47 publications

(43 citation statements)

References 65 publications

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“…We also show that Arabidopsis Atg6/Vps30 partially complemented VPS function in atg6/vps30 mutant yeast. Several other Arabidopsis VPS homologs are required in pollen tubes (Hicks et al, 2004;Lobstein et al, 2004) because the polarized growth of pollen tubes requires membrane trafficking (Hepler et al, 2001;Monteiro et al, 2005). We found that disruption of AtATG6/VPS30 resulted in male sterility because the mutant pollen did not germinate.…”

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confidence: 79%

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An Arabidopsis Homolog of YeastATG6/VPS30Is Essential for Pollen Germination

2007

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Yeast (Saccharomyces cerevisiae) Atg6/Vps30 is required for autophagy and the sorting of vacuolar hydrolases, such as carboxypeptidase Y. In higher eukaryotes, however, roles for ATG6/VPS30 homologs in vesicle sorting have remained obscure. Here, we show that AtATG6, an Arabidopsis (Arabidopsis thaliana) homolog of yeast ATG6/VPS30, restored both autophagy and vacuolar sorting of carboxypeptidase Y in a yeast atg6/vps30 mutant. In Arabidopsis cells, green fluorescent protein-AtAtg6 protein localized to punctate structures and colocalized with AtAtg8, a marker protein of the preautophagosomal structure. Disruption of AtATG6 by T-DNA insertion resulted in male sterility that was confirmed by reciprocal crossing experiments. Microscopic analyses of AtATG6 heterozygous plants (AtATG6/atatg6) crossed with the quartet mutant revealed that AtATG6-deficient pollen developed normally, but did not germinate. Because other atatg mutants are fertile, AtAtg6 likely mediates pollen germination in a manner independent of autophagy. We propose that Arabidopsis Atg6/Vps30 functions not only in autophagy, but also plays a pivotal role in pollen germination.

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confidence: 79%

“…Extensive studies have identified several key components for pollen tube growth; one of these is vesicular trafficking (Hepler et al, 2001;Monteiro et al, 2005). The tip of the pollen tube contains numerous vesicles that could provide precursor materials for the rapidly expanding cell wall of the growing cells.…”

Section: Discussionmentioning

confidence: 99%

An Arabidopsis Homolog of YeastATG6/VPS30Is Essential for Pollen Germination

2007

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“…Several recent reports support a role for both PI4P and PI(4,5)P 2 in the regulation of tip growth in root hairs and pollen tubes (Monteiro et al, 2005a(Monteiro et al, , 2005bDowd et al, 2006;Helling et al, 2006;Preuss et al, 2006;Ischebeck et al, 2008;Kusano et al, 2008;Sousa et al, 2008;Stenzel et al, 2008;Thole et al, 2008;Szumlanski and Nielsen, 2009), but the mechanism by which these membrane-localized signaling molecules affect polarized cell growth remained unclear. Our results support the hypothesis that both PI4P and PI(4,5)P 2 play a critical role in the regulation of clathrin-dependent endocytosis at the tip of pollen tubes and that a proper balance between PI4P and PI(4,5)P 2 accumulation in the apical PM is important for clathrindependent endocytosis.…”

Section: Discussionmentioning

confidence: 99%

“…It was proposed that these PIP5Ks affect either pectin exocytosis or recycling of endocytic vesicles Sousa et al, 2008). Although several studies have implicated phosphoinositides in the regulation of endocytosis in pollen tubes (Monteiro et al, 2005a(Monteiro et al, , 2005bHelling et al, 2006;Sousa et al, 2008), the role and the mode of action for phosphoinositides in endocytosis remain unclear.…”

Section: Introductionmentioning

confidence: 99%

Phosphoinositides Regulate Clathrin-Dependent Endocytosis at the Tip of Pollen Tubes inArabidopsisand Tobacco

et al. 2010

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Using the tip-growing pollen tube of Arabidopsis thaliana and Nicotiana tabacum as a model to investigate endocytosis mechanisms, we show that phosphatidylinositol-4-phosphate 5-kinase 6 (PIP5K6) regulates clathrin-dependent endocytosis in pollen tubes. Green fluorescent protein-tagged PIP5K6 was preferentially localized to the subapical plasma membrane (PM) in pollen tubes where it apparently converts phosphatidylinositol 4-phosphate (PI4P) to phosphatidylinositol 4,5-bisphosphate [PI(4,5)P 2 ]. RNA interference-induced suppression of PIP5K6 expression impaired tip growth and inhibited clathrin-dependent endocytosis in pollen tubes. By contrast, PIP5K6 overexpression induced massive aggregation of the PM in pollen tube tips. This PM abnormality was apparently due to excessive clathrin-dependent membrane invagination because this defect was suppressed by the expression of a dominant-negative mutant of clathrin heavy chain. These results support a role for PI(4,5)P 2 in promoting early stages of clathrin-dependent endocytosis (i.e., membrane invagination). Interestingly, the PIP5K6 overexpression-induced PM abnormality was partially suppressed not only by the overexpression of PLC2, which breaks down PI(4,5)P 2 , but also by that of PI4Kb1, which increases the pool of PI4P. Based on these observations, we propose that a proper balance between PI4P and PI(4,5)P 2 is required for clathrin-dependent endocytosis in the tip of pollen tubes.

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“…Obviously, regulatory functions described for PtdIns(4,5)P 2 include some of those required for a regulator of growth processes in tip-growing cells. PtdIns(4,5)P 2 has previously been demonstrated to be involved in tip growth processes in pollen tubes (Kost et al, 1999;Monteiro et al, 2005;Dowd et al, 2006), a tip-growing system sharing some components of the growth machinery with root hairs (Song et al, 2006). In pollen tubes, Rac-type Rho proteins in the tip plasma membrane physically associate with an enzyme activity producing PtdIns(4,5)P 2 (Kost et al, 1999), and PtdIns(4,5)P 2 has been visualized in a plasma membrane microdomain of the pollen tube tip (Kost et al, 1999).…”

Section: Introductionmentioning

confidence: 99%

The Type B Phosphatidylinositol-4-Phosphate 5-Kinase 3 Is Essential for Root Hair Formation inArabidopsis thaliana

et al. 2008

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Root hairs are extensions of root epidermal cells and a model system for directional tip growth of plant cells. A previously uncharacterized Arabidopsis thaliana phosphatidylinositol-4-phosphate 5-kinase gene (PIP5K3) was identified and found to be expressed in the root cortex, epidermal cells, and root hairs. Recombinant PIP5K3 protein was catalytically active and converted phosphatidylinositol-4-phosphate to phosphatidylinositol-4,5-bisphosphate [PtdIns(4,5)P 2 ]. Arabidopsis mutant plants homozygous for T-DNA-disrupted PIP5K3 alleles were compromised in root hair formation, a phenotype complemented by expression of wild-type PIP5K3 cDNA under the control of a 1500-bp PIP5K3 promoter fragment. Root hair-specific PIP5K3 overexpression resulted in root hair deformation and loss of cell polarity with increasing accumulation of PIP5K3 transcript. Using reestablishment of root hair formation in T-DNA mutants as a bioassay for physiological functionality of engineered PIP5K3 variants, catalytic activity was found to be essential for physiological function, indicating that PtdIns(4,5)P 2 formation is required for root hair development. An N-terminal domain containing membrane occupation and recognition nexus repeats, which is not required for catalytic activity, was found to be essential for the establishment of root hair growth. Fluorescencetagged PIP5K3 localized to the periphery of the apical region of root hair cells, possibly associating with the plasma membrane and/or exocytotic vesicles. Transient heterologous expression of full-length PIP5K3 in tobacco (Nicotiana tabacum) pollen tubes increased plasma membrane association of a PtdIns(4,5)P 2 -specific reporter in these tip-growing cells. The data demonstrate that root hair development requires PIP5K3-dependent PtdIns(4,5)P 2 production in the apical region of root hair cells.

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Modulation of endocytosis in pollen tube growth by phosphoinositides and phospholipids

Cited by 47 publications

References 65 publications

An Arabidopsis Homolog of YeastATG6/VPS30Is Essential for Pollen Germination

An Arabidopsis Homolog of YeastATG6/VPS30Is Essential for Pollen Germination

Phosphoinositides Regulate Clathrin-Dependent Endocytosis at the Tip of Pollen Tubes inArabidopsisand Tobacco

The Type B Phosphatidylinositol-4-Phosphate 5-Kinase 3 Is Essential for Root Hair Formation inArabidopsis thaliana

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