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. 2012 Feb 1;7(2):165–169. doi: 10.4161/psb.18743

Metabolism and roles of phosphatidylinositol 3-phosphate in pollen development and pollen tube growth in Arabidopsis

Xin-Qi Gao 1, Xian Sheng Zhang 1,*
PMCID: PMC3405687  PMID: 22307045

Abstract

Phosphoinositides play important roles in eukaryotic cells, although they constitute a minor fraction of total cellular lipids. Specific kinases and phosphatases function on the regulation of phosphoinositide levels. Phosphatidylinositol 3-phosphate (PtdIns3P), a molecule of phosphoinositides regulates multiple aspects of plant growth and development. In this article, we introduce and discuss the kinases and phosphatases involved in PtdIns3P metabolism and their roles in pollen development and pollen tube growth in Arabidopsis.

Keywords: kinase, phosphatase, phosphatidylinositol 3-phosphate, Pollen, pollen tube

Introduction

Phosphatidylinositols (PtdIns) are minor components in the eukaryotic cell membrane. The inositol ring of PtdIns can be phosphorylated at D3, D4, and D5 by specific phosphoinositide kinases, resulting in formation of phosphatidylinositol phosphate (PtdInsP), phosphatidylinositol bisphosphate (PtdInsP2) and phosphatidylinositol trisphosphate (PtdInsP3). These inositol phospholipids are called phosphoinositides (PIs). The lipid phosphatases remove the D3, D4, or D5 phosphates from these PIs to establish PI homeostatic levels in cell. Each PI isoform shows a specific pattern of intracellular distribution.

Fluorescence protein labeling has revealed that phosphatidylinositol 3-phosphate (PtdIns3P) mainly distributes in late endosomes, multivesicular bodies, and prevacuolar membranes.1,2 PIs themselves or serving as precursors for second messengers regulate plant growth and development, such as pollen development, pollen hydration and germination, pollen tube growth, root hair elongation, and stomatal movement modulation.3-12 Here, we focus on reviewing the functions of kinases and phosphatases in the PtdIns3P metabolism involved in pollen development, germination, and pollen tube growth in Arabidopsis.

The conversion between PtdIns and PtdIns3P

PtdIns can be phosphorylated to PtdIns3P by class III PtdIns 3-kinases (PtdIns3K) (Fig. 1). VPS34 is the first identified class III PtdIns3K in yeast with lipid kinase activity.13 Two kinds of PtdIns3K complexes were identified in yeast and mammals. Complex I is composed of vacuolar protein sorting-associated protein (VPS) 34, VPS15, VPS30/autophagy-related protein (ATG) 6/coiled-coil myosin-like BCL2-interacting protein (BECLIN) 1 and ATG14, and regulates vesicle nucleation in autophagy. Complex II consists of VPS34, VPS15, VPS30/ATG6/BECLIN 1 and VPS38/UV irradiation resistance-associated protein (UVRAG), and functions on hydrolase sorting through the vacuolar protein sorting (VPS) pathway.14,15 By interacting directly with VPS34, VPS15 regulates the membrane targeting and activity of VPS34.16-18 VPS30/ATG6 was identified by searching AuTophaGy-related mutants in yeast. Mammalian Beclin1 is a homolog of yeast ATG6.19 Although Vps30/Atg6/Beclin1 is found to be involved in autophagy and vesicular trafficking, its roles in PtdIns3K complexes are little known.20,21 ATG14 together with ATG6 mediates the localization of complex I and other ATG proteins on phagophore assembly site (PAS).22 VPS38 serves as a bridge between VPS34-VPS15 and VPS30, and localizes complex II to endosome.22,23

graphic file with name psb-7-165-g1.jpg

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Figure 1. Metabolism of Phosphatidylinositol 3-phosphate. PtdIns3K, PtdIns 3-kinase; PtdIns3P5K, PtdIns3P 5-kinase.

AtVPS34, AtVPS15 and AtVPS30 in Arabidopsis are the homologs of yeast VPS34, VPS15 and VPS30 (Table 1). The knockout of AtVPS34 in Arabidopsis plants leads to pollen failure in undergoing normal fission after the first mitotic division. Although the morphology of the atvps34 mutant is normal, its pollens display defects in vacuolar morphology and cannot germinate.8 Either atvps15 or atvps30 mutant also shows abnormal pollen germination. The defect of atvps15 pollen germination can be restored partially after applification of PtdIns3P in vitro.11,24-26 Therefore, AtVPS34, AtVPS15 and AtVPS30 might be the components of PtdIns3K complex in plant cells as in yeast, and function in PtdIns3P generation and pollen tube growth. PtdIns3P is mainly localized in endosomes and vacuolar membrane in plant cells.2,7 Although both atvps15 and atvps30 mutants displays abnormal germination of pollen, no vacuolar phenotype in atvps30 pollen was observed.24-26 It is likely that AtVPS30 in the PtdIns3K complex are not involved in PtdIns3P metabolism. Alternatively, AtVPS15 and AtVPS34, but not AtVPS30, may regulate vacuolar development in pollen development. It was reported that AtVPS30 is co-localized with ATATG8, a PAS marker protein in Arabidopsis.24 AtVPS30 may be involved in vesicular trafficking by recruiting the PtdIns3K complex to the putative PAS in Arabidopsis plant cells, which is required for pollen germination and pollen tube growth. Three putative homologs of ATG14/UVRAG were identified in Arabidopsis (gene ID: AT2G32760, AT4G08540, AT1G77890; Table 1) according to their putative protein containing the conserved ATG14 domain. These indicate that class III PtdIns3K complex is conserved in animals, yeast and plants. Two genes (ID: AT4G08540, AT1G77890) are predicated to encode the DNA-directed RNA polymerase. Another gene’s (ID: AT2G32760) function is unknown although its expression is detected during pollen development (bbc.botany.utoronto.ca/efp/cgi-bin/efpWeb.cgi). The components of class III PtdIns3K complex and their functions remain to be investigated.

Table 1. Enzymes and regulators for PI3P metabolism in Saccharomyces cerevisiae and Homo sapiens, and their homologs in Arabidopsis.

 
 S. cerevisiae
 H. sapiens
 Arabidopsis
      Protein Gene ID* Physiological functions References
PtdIns3K complex
 VPS34
 hVPS34
 AtVPS34
 AT1G60490
 Pollen development and germination
 5, 7, 8, 61
 
 VPS15
 hVPS15
 AtVPS15
 AT4G29380
 Pollen development and germination
 11
 
 VPS30/ATG6
 BECLIN 1
 AtBECLIN/AtATG6/AtVPS30
 AT3G61710
 Pollen germination
 24, 25, 26
 
 ATG14
 hATG14
 AtATG14
 AT2G32760
 ND
  
 
 VPS38
 UVRAG
  
  
  
  
FAB1/PIKfyve complex
 FAB1
 PIKfyve
 AtFAB1A
AtFAB1B
 AT4G33240
AT3G14270
 Pollen development
 43, 44
 
 VAC14
 hVAC14
 AtVAC14
 AT2G01690
 ND
 62
 
 ATG18
 hATG18/ WIPI
 AtATG18A
AtATG18B
AtATG18C
AtATG18D
AtATG18E
AtATG18F
AtATG18G
AtATG18H
 AT3G62770
AT4G30510
AT2G40810
AT3G56440
AT5G05150
AT5G54730
AT1G03380
AT1G54710
 Nutrient stress and senescence
 63
 
 FIG4
  
  
  
  
  
 
 VAC7
 ND
 ND
  
  
  
PtdIns3P 3-phosphatases
 YMR1
 MTMs
MTMRs
 ATMTM1
ATMTM2
 AT3G10550
AT5G04540
 Dehydration stress
 32, 64
 
 TEP1
CDC14
 hPTEN/MMAC1
 AtPTEN1
AtPTEN2A
AtPTEN2B
 AT5G39400
AT3G19420
AT3G50110
 Pollen development and pollen tube growth
 12, 36, 37
PtdIns(3,5)P2 5-phosphatases and regulator
 FIG4
SAC1
SJL1
SJL2
SJL3
 hSAC1
hSAC2
hSAC3
Synaptojanin1
Synaptojanin2
 AtSAC1
AtSAC2
AtSAC3
AtSAC4
AtSAC5
AtSAC6
AtSAC7
AtSAC8
AtSAC9
 At1G22620
At3G14205
At3G43220
At5G20840
At1G17340
At5G66020
At3G51460
At3G51830
At3G59770
 Pollen development; Cell wall thickening; Root hair development; Stress response
 49, 54, 55, 56, 57, 58
  VAC14 hVAC14 AtVAC14 AT2G01690 ND 62
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*

The bold gene ID indicating the gene has high expression in pollen according to bar.utoronto.ca/efp/cgi-bin/efpWeb.cgi. ND, not determined.

PtdIns3P 3-phosphatases can cleave the 3-phosphate from PtdIns3P and form PtdIns (Fig. 1).27 The level of PtdIns3P decreases in yeast that expresses myotubularin-related protein (MTMR) 3, a human PtdIns3P 3-phosphatases belonging to the myotubularin family.28 Myotubularins (MTMs) is a lipid phosphatase family with specificity for PtdIns3P and phosphatidylinositol 3,5-bisphosphate (PtdIns(3,5)P2) as substrates.29 Yeast myotubularin-related protein (YMR) 1, the only myotubularin 3-phosphatase in yeast, corporately functions with synaptojanin-like phosphatase synaptojanin-like protein (SJL) 3 in regulating the localization and level of PtdIns3P.30 In human, 14 members of myotubularin family PtdIns3P 3-phosphatases were identified, and their mutation led to human diseases.31 ATMTM1 and ATMTM2 in Arabidopsis are myotubularin family homologs (Table 1).32,33 ATMTM1 dephosphorylates for PtdIns3P, however its phosphatase activity is higher with PtdIns(3,5)P2 as substrate than with PtdIns3P in vitro. Gene expression analysis reveals that the transcription of AtMTM1 increases significantly after drought stress, indicating its function might be involved in a drought responsive pathway.32 ATMTM2 shows high expression level in pollen (www.bar.utoronto.ca/efp/cgi-bin/efpWeb.cgi), but its roles in pollen development and pollen dehydration remains to be established.

PTEN/MMAC (a phosphatase and tensin homolog / mutated in multiple advanced cancers), dephosphorylating the D3 phosphate group of phosphatidylinositol 3,4,5-trisphosphate (PtdIns(3,4,5)P3), functions in autophagy of mammalian.34,35 In Arabidopsis genome, there are three putative PTEN homologs, AtPTEN1, AtPTEN2A and AtPTEN2B, and they show high expressions in pollen.36,37 The silencing of AtPTEN1 by RNA interference led to aborted pollen grains.36 Additionally, the overexpression of either AtPTEN1 or AtPTEN2A induces male sterility.12,37 Although AtPTEN1 can dephosphorylate PtdIns(3,4,5)P3 in vitro, it still can bind PtdIns3P. The overexpression of AtPTEN1 caused the accumulation of autophagic bodies in tobacco pollen tube, which can be inhibited by exogenous PtdIns3P or by the expression of AtVPS34.12 Thus, AtPTEN1 regulating PtdIns3P metabolism is involved in the autophagy in pollen tube.

The Conversion between PtdIns3P and PtdIns(3,5)P2

Class III PtdIns3P 5-kinases (PtdIns3P5K) catalyze the phosphorylation of PtdIns3P to PtdIns(3,5)P2 (Fig. 1) that plays vital roles in endosomal trafficking.38 FYVE (FAB1, YGL023, VPS27 and EEA1) domain-containing proteins, yeast formation of haploid and binucleate cells 1 (FAB1) and mammal FYVE finger-containing phosphoinositide kinase (PIKfyve), exhibit PtdIns3P5K activity.39 Mutation of FAB1 reduces PtdIns(3,5)P2 level in yeast. The PtdIns3P5K activity of FAB1 is required for cargo-selective sorting into the vacuolar lumen in yeast. PIKfyve regulates the retrograde traffic from endosome to trans-Golgi-network.40,41 Arabidopsis genome contains two putative FAB1/PIKfyve homologs, AtFAB1A and AtFAB1B.42 The pollen of the double mutant atfab1a atfab1b is lethal and shows severe defects in vacuolar organization.43 The enhanced or reduced levels of AtFAB1A/B expression interfere the endomembrane homeostasis including endocytosis, vacuolar formation and acidification.44 In yeast, hyperosmotic stress increases the level of PtdIns(3,5)P2 that plays roles in membrane trafficking in the endosomal/lysosomal system.38 Endocytosis is also involved in pollen tube growth.45 Therefore, PtdIns(3,5)P2 might play roles through similar mechanism in pollen tube growth with yeast hyperosmotic tolerance.

FAB1/PIKfyve forms a protein complex with factor-induced protein (FIG) 4/suppressor of actin (SAC) 3, vacuolar segregation protein (VAC) 7, ATG18 and VAC14 in yeast.46,47 Homologs of the subunits of the FAB1/PIKfyve complex except VAC7 were identified in Arabidopsis (Table 1). Although VAC7 is a FAB1 activator in PtdIns(3,5)P2-synthesizing complex, hyperosmotic shock still induces the increase in PtdIns(3,5)P2 levels in the absence of VAC7 in yeast.48 Thus, VAC7 is not necessary in this complex for PtdIns(3,5)P2 synthesis and turnover. Whereas, FIG4 itself can function in both PtdIns(3,5)P2 synthesis and turnover in yeast. Function of the most Arabidopsis homologs of FAB1/PIKfyve complex components are not investigated, except that the FIG4 homolog (gene ID: At5G66020, Table 1) was found to be involved in pollen development.49

PtdIns(3,5)P2 5-phosphatase hydrolyzes the 5-phosphate of PtdIns(3,5)P2 to form PtdIns3P (Fig. 1). In yeast, the level of PtdIns(3,5)P2 significantly increases after hyperosmotic stress, and then, it decreases to the basal level after 30 min. It was found that yeast FIG4, a SAC phosphatase domain-containing protein, functions in this process.50 In the cells lacking FIG4, PtdIns(3,5)P2 level shows a little decrease after hyperosmotic shock. Other proteins, SAC1, SJL1, SJL2 and SJL3, also show similarity with FIG4 in yeast.51 Synaptojanin is the mammalian phosphoinositide 5-phosphatases, such as hSAC1, hSAC2, hSAC3, Synaptojanin 1 and Synaptojanin 2 in human. The loss of function of hSAC3, a homolog of FIG4 in human, reduces the level of PtdIns(3,5)P2 and leads to neuronal degeneration.52,53 Arabidopsis genome encodes nine putative SAC domain-containing proteins (AtSACs) that can be classified into three classes: AtSAC1–5 are similar to yeast FIG4, AtSAC6–8 are similar to yeast SAC1, and AtSAC9 contains unique domains (Table 1).54 AtSAC1 exhibits phosphatase activity with PtdIns(3,5)P2 as the substrate. Mutation of AtSAC1 causes a decrease in the wall thickness, and results in a weak stem phenotype.49 However, AtSAC7 (ROOT HAIR DEFECTIVE 4) and AtSAC9 all display a preference for phosphatidylinositol 4,5-bisphosphate (PtdIns(4,5)P2) as substrate in vitro.55,56 Mutation of both AtSAC7 and AtSAC9 lead to overaccumulation of PtdIns(4,5)P2, resulted in root hair-defect and constitutive expression of the stress-response genes. Five SAC-like genes (gene ID At1G22620, At3G51460, At3G59770, At3G14205, At5G20840 and At5G66020) show high expression level in Arabidopsis pollen (Table 1).57 Only the function of AtSAC6 was found to be involved in β-aminobutyric acid-induced pollen sterility.58

Conclusion and Perspective

Although some information has been accumulated on understanding for PtdIns3P metabolism in Arabidopsis, the functions of itself and its products remain to be investigated in the development and transmission of male gametophyte.59 Arabidopsis genome encodes the homologs of the binding proteins of PtdIns(3,5)P2 and PtdIns3P, such as Arabidopsis β-propellers that binds phosphoinositides, epsin-like protein EpsinR2, and sorting nexin 2b, however, their function is still unknown in plant.60 Further investigations on PtdIns3P metabolism will provide a deeper insight for the function of phosphoinositides in plant reproductive development.

Acknowledgments

This work is funded by the Major Research Plan from the Ministry of Science and Technology of China (No. 2007CB947600) and the National Natural Science Foundation of China (No. 31170293).

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.

Footnotes

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