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First published online January 19, 2005; 10.1105/tpc.104.027631 © 2005 American Society of Plant Biologists VANGUARD1 Encodes a Pectin Methylesterase That Enhances Pollen Tube Growth in the Arabidopsis Style and Transmitting Tract
a Institute of Molecular and Cell Biology, Singapore 138673 3 To whom correspondence should be addressed. E-mail yede{at}cau.edu.cn; fax 86-10-62733798.
In flowering plants, penetration of the pollen tube through stigma, style, and transmitting tract is essential for delivery of sperm nuclei to the egg cells embedded deeply within female tissues. Despite its importance in plant reproduction, little is known about the underlying molecular mechanisms that regulate the navigation of the pollen tube through the stigma, style, and transmitting tract. Here, we report the identification and characterization of an Arabidopsis thaliana gene, VANGUARD1 (VGD1) that encodes a pectin methylesterase (PME)-homologous protein of 595 amino acids and is required for enhancing the growth of pollen tubes in the style and transmitting tract tissues. VGD1 was expressed specifically in pollen grain and the pollen tube. The VGD1 protein was distributed throughout the pollen grain and pollen tube, including the plasma membrane and cell wall. Functional interruption of VGD1 reduced PME activity in the pollen to 82% of the wild type and greatly retarded the growth of the pollen tube in the style and transmitting tract, resulting in a significant reduction of male fertility. In addition, the vgd1 pollen tubes were unstable and burst more frequently when germinated and grown on in vitro culture medium, compared with wild-type pollen tubes. Our study suggests that the VGD1 product is required for growth of the pollen tube, possibly via modifying the cell wall and enhancing the interaction of the pollen tube with the female style and transmitting tract tissues.
The fertilization of flowering plants requires delivery of the sperm to the egg. The process begins with deposition of pollen grains on the stigmatic tissue. The compatible interaction between pollen and stigmatic cells triggers the hydration and germination of the pollen. The resulting pollen tube invades the stigmatic tissue, penetrates the style, navigates through the transmitting tract, and then is directed to the egg embedded in the ovule (Hülskamp et al., 1995b  ; Wilhelmi and Preuss, 1996; Ray et al., 1997; Lennon and Lord, 2000; Palanivelu and Preuss, 2000; Johnson and Preuss, 2002; Lord and Russell, 2002; Preuss, 2002; Kim et al., 2003; Palanivelu et al., 2003). Several studies have revealed that components such as lipids on pollen and stigma are important for transportation of water from stigmatic cells to pollen (Elleman et al., 1992; Preuss et al., 1993; Hülskamp et al., 1995a; Wolters-Arts et al., 1998; Zinkl et al., 1999; Fiebig et al., 2000). The morphological studies also show that a compatible interaction between pollen tubes and stigmatic cells is required for triggering degradation of the stigmatic and stylar cell walls (Atkinson et al., 1993; Hiscock et al., 1994; Johnson and Preuss, 2002; Lord and Russell, 2002). However, the genetic and molecular mechanisms that control the penetration of pollen tubes through stigmatic and stylar tissues are poorly understood.
In plant species such as lily (Lilium longiflorum) with a hollow stigma and style, adhesion between the pollen tube and transmitting tract epidermis is required for growth of the pollen tube toward ovule. The stylar matrix secreted by the transmitting tract epidermis also has been suggested to play an important role in such adhesion (Jauh et al., 1997
Pectin methylesterases (PMEs) have been implicated to play roles in different physiological processes of plant development via modification of the cell wall (Bordenave and Goldberg, 1993
Isolation of the vgd1 Mutant The vgd1 mutant was identified by its reduced fertility in a phenotypic screen of the enhancer-trap dissociation (Ds) insertion lines in Arabidopsis ecotype Landsberg erecta (Sundaresan et al., 1995 ). The homozygous vgd1 plant produced smaller and shorter siliques with fewer seeds (Figures 1A and 1B) compared wild-type plants (Figures 1C and 1D). No morphological abnormality in other floral and vegetative parts was observed (Figures 1E and 1F).
vgd1 Was a Male Gametophytic Mutation That Cosegregated with a Single Ds Insertion To investigate if the vgd1 mutation affected male or female function, the vgd1 mutant plant was used as male or female to cross with wild-type plants. When a homozygous vgd1 plant was used as a female in a cross with a wild-type plant, nearly all ovules (449 out of 455) were able to produce viable seeds as those in the wild type, indicating that the vgd1 mutation did not affect female fertility. In a reciprocal cross, however, only a few ovules in the upper part of the silique were fertilized and developed into seeds. When a heterozygous vgd1 plant was used as a male in a cross with wild-type plants, the F1 seedlings segregated 1:40.8 (80:3261) kanamycin resistant to kanamycin sensitive instead of the expected 1:1 segregation. This result indicated that the vgd1 mutation led to a male gametophytic defect. In summary, the vgd1 mutation resulted in defects of male gametophytic function but did not affect female gametophytic function. When a heterozygous vgd1 plant was used as a female in a cross with a wild-type plant, the F1 seedlings showed an average segregation ratio of approximate 1:1 (321:316) kanamycin resistant (Kanr) to kanamycin sensitive (Kans). All Kanr F1 seedlings gave rise to fully fertile plants. All F2 families resulting from the selfing of Kanr F1 plants showed segregation of the vgd1 mutant phenotype. When a homozygous vgd1 plant was used as a female in a cross with a wild-type plant, all F1 seedlings were resistant to kanamycin (Kanr) upon germination and fully fertile when matured. All resulting F2 families also showed segregation of the vgd1 mutant phenotype. These results showed tight linkage of a single recessive vgd1 mutation to the kanamycin selection marker carried by a single Ds element in the vgd1 genome. We further confirmed a single Ds insertion with DNA gel blotting hybridization using a 755-bp Ds 5'-end fragment as a probe (data not shown).
The vgd1 Mutation Retarded Growth of the Pollen Tube in the Style and Transmitting Tract
The vgd1 Pollen Tube Was Unstable in Vitro In vitro germination showed that the vgd1 pollen tubes were unstable when cultured in vitro. Eighty-four percent of wild-type pollen could germinate in a wide range of in vitro conditions. Wild-type pollen tubes grew straight on the medium surface and were able to elongate up to an average length of 350 µm after an overnight incubation (Figure 4D). By contrast, although  83% of vgd1 pollens could germinate in an optimized in vitro condition (see Methods), they were shorter, grew more slowly, and had an unusual shape (Figure 4C) compared with the wild-type pollen tubes germinated in the same conditions (Figure 4D). In all, 93.8% (334 out of 356) of germinating vgd1 pollen tubes burst (Figure 4E), indicating that the vgd1 pollen tubes were structurally unstable. By contrast, bursting of wild-type pollen tubes was only occasionally observed, at a very low rate of 3.7% (12 out of 328). These results suggested that VGD1 might be involved in stiffening the pollen tube wall and enhancing its interaction with the medium surface.
The vgd1 Pollen Tube Is Morphologically Normal When Germinated on Stigma and Is Not Defective in Guidance The scanning electronic microscopic observations showed that the vgd1 pollen appeared morphologically normal (Figures 4A and 4B) and had the same germination rate (>95%) on stigmatic cells as wild-type pollen. There were no morphological differences between the vgd1 and wild-type pollen tubes when germinated on stigmatic cells of both vgd1 and wild-type stigmas (Figures 2A and 2B). In addition, the scanning electron microscopy observations showed that the vgd1 pollen tubes were directed to ovules normally as wild-type pollen tubes (data not shown), indicating that the vgd1 mutation did not affect pollen tube guidance.
Molecular Cloning of the VGD1 Gene
To confirm the identification of VGD1, a 5.131-kb genomic DNA fragment, including the predicted promoter, transcripted region, and 3'-end nontranscribed region, was amplified by high-fidelity PCR and introduced into the vgd1 homozygous plants through Agrobacterium tumefaciens–mediated infiltration. Thirty-six independent transformants were obtained in a screen. Eighteen of the thirty-six T1 seedlings gave rise to fully fertile plants. The other transformants exhibited variable restorations of male fertility. In the T2 generation, all hygromycin-selected seedlings from the 18 fully fertile families gave rise to normal fully fertile plants, whereas nonselected T2 plants showed the segregation of the vgd1 phenotype with concordance of hygromycin-sensitive segregation. The results show that the 5.131-kb genomic fragment from chromosome II contained all the genetic information required for normal functioning of VGD1. A BLASTN search of the databases showed that an 1823-bp cDNA sequence (AJ250430) in the GenBank database matched the predicted 1952-bp mRNA sequence (AY091768) from gene At2g47040. We used RT-PCR to clone the full-length cDNA. The cloned cDNA (AY830948) was 1952 nucleotides in length, which was consistent in size to a band shown by RNA gel blot hybridization (Figure 7A). To confirm the genetic function of cloned VGD1 cDNA, the 1952-bp cDNA fragment was fused to the predicted VGD1 promoter (a 1513-bp fragment flanking the 5'-end of the VGD1 coding region) and VGD1 terminator (a 1786-bp fragment flanking the 3'-end of the VGD1 coding region). The resulting construct [PVGD1-VGD1(cDNA)-TVGD1] was subcloned into pCAMBIA1300 Ti-plasmid vector and introduced into the homozygous vgd1 mutant plants. Twenty-four independent transformants were obtained in a screen. Eight of the twenty-four T1 seedlings gave rise to fully fertile plants. Others exhibited a variable restoration of male fertility. In the T2 generation, all hygromycin-selected seedlings from the eight families gave rise to fully fertile plants, whereas nonselected T2 plants showed segregation of the vgd1 phenotype. These results showed that the 1952-bp mRNA sequence was sufficient to encode the functional VGD1 protein.
VGD1 Encodes a PME-Homologous Protein The VGD1 mRNA encodes a PME-homologous protein of 595 amino acids, which consists of a secretion-related transmembrane domain, a PME inhibitor (PMEI)-homologous domain, and a pectinesterase-homologous domain (Figure 5B). A BLASTP search was performed using the entire amino acid sequence of the predicted VGD1 protein and showed that there was a group of PME proteins in the Arabidopsis genome with >50% amino acid sequence identity to VGD1. Specifically, VGD1 had 85% (514/598) identity and 91% (550/598) similarity to the predicted At2g47030 gene product (T02184; T52330) and 69% (426/611) identity and 81% (503/611) similarity to the predicted At3g62170 gene product (Figure 6). In addition, VGD1 is located in a genomic locus consisting of three homologous genes, At2g47030, VGD1 (At2g47040), and At2g47050 (Figure 5C). The predicted At2g47050 protein (T02182) has only 216 amino acids and contains only one PMEI domain, which is likely to be a unique PMEI gene sharing a lower homology (27% identity) with the PMEI domain of VGD1.
The vgd1 Mutation Reduced the Total Pectin Demethylesterification Activity of PMEs in Pollen Grain Molecular cloning shows that the VGD1 gene encoded a PME-homologous protein. PMEs belong to a family of cell wall enzyme proteins that act in the modification of cell walls via demethylesterification of cell wall pectin. To investigate whether the vgd1 mutation affected the PME activity in pollen and the pollen tube, we compared the total pectin demethylesterification activity of PMEs in the vgd1 pollen grain to that in wild-type pollen grain. The result showed that the total pectin demethylesterification activity of PMEs in the vgd1 pollen grain decreased 18% compared with that of wild-type pollen grain. This result indicated that VGD1 encoded a PME enzyme and that the retardation of pollen tube growth was caused by the loss of VGD1 PME activity in the pollen tubes.
VGD1 and Its Homologs, At2g47030 and At3g62170, All Were Expressed Specifically in the Pollen Grain and Pollen Tube
Comparing the densities of GUS stains revealed that the expressional levels of three genes were very different. The expressional signal of VGD1 was the strongest, and that of At2g47030 was the weakest. We further used quantitative real-time PCR to compare the expression levels of VGD1 and its homologs, At2g47030 and At3g62170, in wild-type plants. The results showed that the level of VGD1 mRNA transcription was
The At2g47030 Product Has the Same Biological Function as VGD1 Protein
The VGD1–Green Fluorescent Protein Fusion Was Distributed in the Whole Pollen Tube, Including the Plasma Membrane and Pollen Tube Wall
VGD1 Is Important for Growth of the Pollen Tube in Female Floral Tissue The vgd1 mutation we report here is a novel mutation that affects growth of pollen tubes in the Arabidopsis style and transmitting tract. Genetic studies indicated that the vgd1 mutation was a male gametophytic mutation and affected only the growth of pollen tubes. The vgd1 pollen tubes grew much more slowly than wild-type pollen in the style and transmitting tract, although they were able to germinate on the surface of the stigmatic cell and invaded into the stigmatic cell. Our observations also indicated that the vgd1 mutation did not obviously affect the growth rate of the pollen tube on the surface of stigmatic cells, and the retardation of pollen tube extension occurred mainly in the style and transmitting tract. Therefore, we conclude that the VGD1 product is required for enhancing the growth of the pollen tube in the style and transmitting tract.
The VGD1 protein was highly homologous to PMEs, a group of cell wall proteins. Consistently, shutting down of VGD1 function reduced PME activity in the pollen grain and indicated that VGD1 protein might function as a PME enzyme. In higher plants, different PME isoforms are encoded by multiple gene families (Richard et al., 1996 The null vgd1 mutation did not block the growth of pollen tubes in the style and transmitting tract completely. A possible reason for this finding is that the VGD1 protein may act redundantly with At2g47030. The At2g47030 protein had a high amino acid sequence identity to VGD1 and exhibited the same expression pattern as VGD1. The complementation experiment also showed that the At2g47030 gene product had the same biological function as the VGD1 protein. Disruption of VGD1 function significantly reduced the growth rate of pollen tubes in the style and transmitting tract. If these two genes act redundantly, VGD1 must be the major contributor to the process. As discussed above, the expression level of At2g47030 was 21 times lower than that of VGD1. Expression of At2g47030 at the same level as VGD1 using VGD1 promoter could complement the vgd1 mutant phenotype. This result indicates that different PMEs might have the same biological function when they are expressed at the same level and location. The At3g62170 gene product also was highly homologous to VGD1 protein and had the same expression profile as VGD1. However, we failed to complement the vgd1 mutant by overexpression of At3g62170 protein using the VGD1 promoter. It is possible that At3g62170 might not have the same function as VGD1. This result showed that homologous genes with high sequence similarity and even the same location of expression might not unconditionally have the same biological function. We still do not know the actual biological function of the At3g62170 gene product. The At3g62170 protein also might have lost its function in pollen tube growth during evolution, although it still is expressed actively in the pollen tube.
The VGD1 Product May Be Involved in Building up the Strength of the Pollen Tube Wall
Studies have shown that mature PMEs could have different modes of action. They may act either randomly or linearly along the pectin chain (Markovic and Kohn, 1984 Interestingly, we did not observe any burst pollen tubes on stigmatic cells. Possibly, the hydration expansion of pollen in vivo is milder or more controlled compared with our in vitro conditions. This finding implies that germination and development of pollen tubes are different in vivo and in vitro, and it is known that growth of pollen tubes in vivo is subject to intricate regulation. The interaction between pollen tubes and stigmatic cells may be important for the stabilization of the pollen tubes. The pollen tube grew within cell walls of stigmatic papillar cells; presumably the surrounding layer of the papillar cell wall also could provide additional physical support to the pollen tube wall.
The VGD1 Product May Involve the Interaction between the Pollen Tube and Female Floral Tissues via the Modification of Cell Walls
On one hand, the retardation of pollen tubes in the vgd1 mutant may result from the inefficient degradation of stigmatic and stylar cell walls. Studies have shown that many factors affect the mode of action of PMEs, such as pH, the initial degree of demethylesterification of pectins, and the presence of cations (Catoire et al., 1998 On the other hand, the retardation of the pollen tube also could result from the inefficient interaction of pollen tubes with the ECM in the style and transmitting tract. As mentioned previously, the VGD1 protein exhibited a predicted basic isoelectric point of 8.9, which is advantageous to linear demetylesterification. The conditions in the transmitting tract also may be suitable for linear demeylesterification by VGD1. The linear demethylesterification of pectin can make a contribution to the formation of the Ca2+ pectate gel lawn that benefits the interaction between pollen tubes and ECM in the style and transmitting tract, promoting the elongation of the pollen tube in the style and transmitting tract. Loss of VGD1 function may reduce the efficiency of interaction of the pollen tube with the ECM in the style and transmitting tract, resulting in the retardation of the pollen tube in the transmitting tract. In conclusion, we have described a novel vgd1 mutation that significantly retarded the navigation of the pollen tube through the style and transmitting tract, resulting in a significant reduction of male fertility. The VGD1 gene encoded a PME-homologous protein and was expressed specifically in pollen grain and the pollen tube. This study suggests that VGD1 plays an important role in growth of pollen tubes in female floral tissues, possibly via enhancing the interaction between the pollen tube and female floral tissues by modification of the cell walls.
Plant Materials and Mutant Isolation All Arabidopsis thaliana plants used in this study were in the Landsberg erecta background. The seeds were pregerminated on MS-salt agar plates with or without 50 µg/mL of kanamycin at 22°C under a light cycle of 16 h light/8 h dark. The plants were grown in soil at 22°C under the same light cycle as for germination. The generation of Ds insertion lines and screen of mutants were performed as described by Sundaresan et al. (1995) . The selected mutant plants were backcrossed with wild-type plants to purify the vgd1 mutation. The F3 plants with a single Ds insertion linked to the vgd1 phenotype were selected for further phenotypic characterization.
Characterization of vgd1 Mutant Phenotype
Aniline blue staining of pollen tubes in pistils was performed as described by Sumie et al. (2001)
The morphological observations of pollen grains and pollen tubes by scanning electronic microscopy and TEM were performed as described by Hülskamp et al. (1995b)
Genetic Analyses of vgd1
Molecular Cloning of the VGD1 Gene and DNA Sequencing
Complementation Experiments A 5.131-kb VGD1 genomic fragment was amplified by the ACCuTaq LA DNA polymerase PCR kit (Sigma-Aldrich, St. Louis, MO) with gene-specific primers 5'-GGATCCTGATGCTCCACATTCTGACGT-3' and 5'-GAATTCTGGGTCAACGAATGGCTGAGA-3' and cloned into the pGEM-T vector. After sequence verifications, the fragment was subcloned into pCAMBIA1300 Ti-derived binary vector (CAMBIA, Canberra, Australia; www.cambia.org.au). For cDNA complementation experiments, the VGD1 promoter (PVGD1) and VGD1 terminator (TVGD1) fragments were amplified from wild-type genomic DNA using the primers listed in Table 1. VGD1, At2g47030, and At3g62170 cDNAs were amplified from the flower-specific cDNA pool using the gene-specific primers homologous to both end sequences of cDNAs (Table 1). The resulting fragments were cloned into pGEM-T vector and verified by DNA sequencing. Restriction enzyme pairs PstI and SpeI, SpeI and NheI, or NheI and EcoRI were used to excise the promoter or cDNAs or terminator from the pGEM-T vector, respectively. They were then subcloned into pCAMBIA1300 vector, resulting in the transcriptional fusion construct PVGD1-cDNA-TVGD1. All constructs in pCAMBIA vector for complementation experiments were introduced into the vgd1 homozygous plants using the Agrobacterium tumefaciens–mediated infiltration method. The transformants were selected using 20 mg/L of hygromycin and 50 mg/L of kanamycin.
Measurement of the Relative PME Activity in vgd1 Pollen Grain
Subcellular Localization of VGD1-GFP Fusion Protein in the Pollen Tube
RNA and DNA Gel Blot Hybridization
Analysis of Promoter Activity
Quantification of the mRNAs Transcribed from the VGD1, At2g47030, and At3g62170 Genes in Wild-Type Flower Tissue Real-time PCR technology was used to quantify the mRNAs of VGD1, At2g47030, and At3g62170 in wild-type floral tissue. The poly(A)+ RNAs were purified using the Oligotex mRNA Midi kit (Qiagen, Valencia, CA) as described by the supplier and converted into single cDNAs with Stratagene cDNA synthesis kit (Stratagene, La Jolla, CA) following the instructions of the supplier. The single-strand cDNA pool was diluted to 50 ng/µL of single strand cDNA. Two microliters of diluted cDNA solution was used for each real-time PCR reaction. To prepare the standard template series, the cDNA fragments of the three genes were amplified by PCR using the gene-specific primer pairs listed in Table 3 and cloned into pGEM-T Easy vector, respectively. The plasmids containing the cDNA fragments were reproduced in Escherichia coli and recovered using the Qiagen plasmid mini preparation kit and then linearized with the restrictive enzyme NocI or SalI (Roche). The linearized plasmid DNAs were purified with Qiagen DNA spin columns and quantified with a UV spectrum photometer (UV-1601; Shimadzu, Columbia, MD). The template standards for each gene were prepared in a concentration series of 1010, 109, 108, 107, 106, 105, and 104 copies of the target cDNA molecules per microliter. The preparation of standard curves and quantification of each mRNA were performed using the Roche Lightcycler and FastStart DNA Master SYBR Green l kit following the instructions from the supplier (Roche).
Sequence data from this article have been deposited with the EMBL/GenBank data libraries under accession numbers AY830948 (VGD1 full-length cDNA), AY830949 (At2g47030 full-length cDNA), and AY830950 (At3g62170 full-length cDNA).
This work was supported by research grants from the Agency for Science, Technology, and Research of Singapore. We thank Megan E. Griffith and Jinrong Peng for their critical comments on manuscript preparation.
1 These authors contributed equally to this work. 
2 Current address: Temasek Life Science Laboratory, 1 Research Link, National University of Singapore, Singapore 117604. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantcell.org) is: De Ye (yede{at}cau.edu.cn). Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.104.027631. Received September 14, 2004; accepted November 16, 2004.
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