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© 2005 American Society of Plant Biologists
VANGUARD1—At the Forefront of Pollen Tube Growthneckardt{at}aspb.org
Pollen tube growth is one of the most fascinating—and essential—phenomena in the life cycle of flowering plants. After a compatible interaction between pollen grains and the stigma surface, the pollen germinates and forms the pollen tube, which grows through the stigma, style, and transmitting tract to deliver the sperm cells to the ovule. Pollen tube growth occurs only at the extreme apex of the tube through the mechanism of polarized tip growth (reviewed in Hepler et al., 2001
After germinating on the stigmatic surface, the pollen grain forms a tube that elongates exclusively at the apex (reviewed in Franklin-Tong, 1999  ; Lennon and Lord, 2000; Holdaway-Clarke and Hepler, 2003). Callose plugs are laid down at regular intervals behind the growing tip, and the region adjacent to the plug becomes vacuolated, which serves to maintain a region of concentrated cytoplasm, containing organelles and the sperm nuclei, near the growing tip. The extreme end of the growing tip consists of a highly dynamic clear zone that contains vesicles and cell wall precursors. Activity in this zone involves continual biosynthesis of cell wall and plasma membrane and turnover of cytoskeletal components as the tube elongates and interactions with the surrounding tissues that guide growth toward the ovule (reviewed in Feijó et al., 2004).
One of the key features of growing pollen tubes is a steep tip-focused Ca2+ gradient. The gradient is thought to be maintained by influx of extracellular Ca2+ through Ca2+ channels active only at the extreme end of the growing tip and dissipation of Ca2+ away from the tip where Ca2+ channels are not active (Franklin-Tong, 1999
There is also evidence that oscillatory behavior of protons is important for pollen tube growth, as high concentrations of protons in the tip region (i.e., low pH) are correlated with the most rapid growth rates (Feijó et al., 1999
Growing pollen tubes must maintain a delicate balance between loosening of the cell wall to allow for rapid cell elongation and maintaining sufficient rigidity to withstand the considerable turgor pressure within the growing tip. Ca2+ and protons are both intimately linked to dynamic properties of the cell wall, principally through their influence on pectin, a heterogeneous polymer of polygalacturonic acids that is a major component of cell walls. Ca2+ ions bind to anionic acid moieties of nonesterified homogalacturonan molecules in pectin, creating cross links between molecules that provide increased rigidity to the pectin polymer and cell wall (reviewed in Vorwerk et al., 2004
Pectin is thought to be secreted in the methylesterified state into the tip region of growing pollen tubes (Goldberg et al., 1996 ). Pectin methylesterases (PMEs) are considered to be key regulators of cell wall rigidity, as they catalyze the demethylesterification of homogalacturonans, thereby exposing the anionic sites where Ca2+ can bind. The cell wall at the growing tip of pollen tubes is highly pectinaceous, so the degree of Ca2+ cross-linking—and thus the activity and localization of PMEs—may be of particular importance in controlling pollen tube growth.
In this issue of The Plant Cell, Jiang et al. (pages 584–596) report a significant advance in our understanding of the mechanics of pollen tube growth. Previous reports have provided evidence that PMEs function in pollen tubes and that the pectin methylation state, both in pollen tubes and surrounding female tissues, is an important parameter in controlling pollen tube growth. For example, PMEs have been isolated from willow (Futamura et al., 2000 The authors isolated the vgd1 mutant in a screen for reduced fertility from Dissociation (Ds) transposon insertion lines of Arabidopsis. Homozygous vgd1 mutants produced smaller siliques with fewer seeds than the wild type, which was associated with a single Ds insertion affecting only the male gametophytic function. Further analysis showed that pollen was able to germinate, but growth of vdg1 pollen tubes through the transmitting tract of the style was retarded. Pollen tubes were morphologically normal when grown on stigmatic tissue, and guidance toward the ovule was unaffected, but pollen tubes grown in vitro (on an agar-sucrose medium) were misshapen, grew more slowly than wild-type pollen tubes, and more than 90% of them burst open, indicating structural instability (see figure).
VGD1 was cloned and found to encode a PME-homologous protein containing a secretion-related transmembrane domain, a PME inhibitor-homologous domain, and a PME-homologous domain. The authors next assayed PME activity in crude pollen extracts and found the activity associated with vgd1 pollen reduced to 82% of that measured in wild-type pollen. This suggests that VGD1 has PME activity in vivo, but it is likely not the only PME enzyme active in pollen. Comparison with the Arabidopsis genome revealed two other genes encoding PME-homologous proteins with >50% similarity to VDG1, one of which is located at the same locus as VGD1 along with a third gene encoding a smaller protein with lower homology to VGD1.
Depending on enzyme characteristics and conditions in the medium, PMEs may catalyze demethylesterification in a linear fashion or at random points along a pectin chain. These two types of reactions produce different products that may have distinct functions (Micheli, 2001 ). The linear reaction produces the anionic moieties that can interact with Ca2+ to create the pectate gel that provides increased rigidity to the cell wall, whereas random demethylesterification releases protons that contribute to the loosening of cell walls by promoting the activity of endopolygalacturonases. Historically, it was believed that acidic PMEs generally catalyze random demethylesterification and basic PMEs catalyze the linear reaction, but there is evidence that at least some PME isoforms can act randomly or linearly depending on environmental conditions (Micheli, 2001).
VGD1 has a predicted isoelectric point of a basic PME (corresponding to pH 8.9), and vgd1 mutant pollen tubes with decreased PME activity burst when grown in vitro, both of which suggest that the enzyme functions within the pollen tube cell wall to strengthen the growing pollen tube (i.e., through linear demethylesterification). However, it is also possible that the enzyme catalyzes random demethylesterification, for example, under conditions of low pH. Oscillations in pH at the growing tip might even cause oscillations in the activity of VGD1 between random and linear demethylesterification to promote wall loosening during periods of peak growth rate rapidly followed by brief periods of wall strengthening, respectively. Although there are no data to support this idea, it is consistent with the observation that pH oscillates in the tip region in phase with growth (lowest pH coinciding with peak growth rate; Feijó et al., 1999 Jiang et al. show that VGD1, and likely other pollen-specific PMEs, are essential for controlling the rapid growth rate of elongating pollen tubes. It may be that the family of pollen-specific PME genes in Arabidopsis (as well as other plants) encodes enzymes with distinct activities (e.g., wall loosening versus wall strengthening) in the growing pollen tube or that VGD1 and other PMEs have more than one type of activity, depending on pH and/or other conditions. Future research will need to pinpoint the precise location of action and in vivo catalytic function of each of these enzymes (e.g., random versus linear demethylesterification) as well as the parameters that control their localization and activity, including intracellular and intercellular signaling events, such as ROP GTPase and calcium signaling, and signaling related to navigation of the growing tube toward the ovule.
Feijó, J.A., Costa, S.S., Prado, A.M., Becker, J.D., and Certal, A.C. (2004). Signalling by tips. Curr. Opin. Plant Biol. 7, 589–598.[CrossRef][ISI][Medline]
Feijó, J.A., Sainhas, J., Hackett, G., Kukel, J.G., and Hepler, P.K. (1999). Growing pollen tubes have a constitutive alkaline band on the clear cap and a growth-dependent acidic tip. J. Cell Biol. 144, 483–496.
Franklin-Tong, V.E. (1999). Signaling and the modulation of pollen tube growth. Plant Cell 11, 727–738. Futamura, N., Mori, H., Kouchi, H., and Shinohara, K. (2000). Male flower-specific expression of genes for polygalacturnoase, pectin methylesterase and ß-1,3-glucanase in a dioecious willow (Salix gilgiana Seemen). Plant Cell Physiol. 41, 16–26. Goldberg, R., Morvan, C., Jauneau, A., and Jarvis, M.C. (1996). Methyl-esterification, de-esterification and gelation of pectins in the primary cell wall. In Pectins and Pectinases: Progress in Biotechnology, Vol. 14, J. Visser and A.G.J. Voagen, eds (Amsterdam: Elsevier Science), pp. 151–172.
Gu, Y., Vernoud, V., Fu, Y., and Yang, Z. (2003). ROP GTPase regulation of pollen tube growth through the dynamics of tip-localized F-actin. J. Exp. Bot. 54, 93–101. Hepler, P.K., Vidali, L., and Cheung, A.Y. (2001). Polarized cell growth in higher plants. Annu. Rev. Cell Dev. Biol. 17, 159–187.[CrossRef][ISI][Medline] Holdaway-Clarke, T.L., Feijó, J.A., Hackett, G.R., Kunkel, J.G., and Hepler, P.K. (1997). Pollen tube growth and the intracellular cytosolic calcium gradient oscillate in phase while extracellular calcium influx is delayed. Plant Cell 9, 1999–2010.[Abstract] Holdaway-Clarke, T.L., and Hepler, P.K. (2003). Control of pollen tube growth: Role of ion gradients and fluxes. New Phytol. 159, 539–563.[CrossRef]
Jiang, L., Yang, S.-L., Xie, L.-F., Puah, C.S., Zhang, X.-Q., Yang, W.-C., Sundaresan, V., and Ye, D. (2005). VANGUARD1 encodes a pectin methylesterase that enhances pollen tube growth in the Arabidopsis style and transmitting tract. Plant Cell 17, 584–596. Lennon, K.A., and Lord, E.M. (2000). In vivo pollen tube cell of Arabidopsis thaliana I. Tube cell cytoplasm and wall. Protoplasma 214, 45–56.[CrossRef]
Li, H., Lin, Y., Heath, R., Zhu, M.X., and Yang, Z. (1999). Control of pollen tube tip growth by a Rop GTPase-dependent pathway that leads to the tip-localized calcium influx. Plant Cell 11, 1731–1742. Messerli, M.A., Creton, R., Jaffe, L.F., and Robinson, K.R. (2000). Periodic increases in elongation rate precede increases in cytosolic Ca2+ during pollen tube growth. Dev. Biol. 222, 84–98.[CrossRef][ISI][Medline] Micheli, F. (2001). Pectin methylesterases: Cell wall enzymes with important roles in plant physiology. Trends Plant Sci. 6, 414–419.[CrossRef][ISI][Medline] Palanivelu, R., Brass, L., Edlund, A.F., and Preuss, D. (2003). Pollen tube growth and guidance is regulated by POP2, an Arabidopsis gene that controls GABA levels. Cell 114, 47–59.[CrossRef][ISI][Medline] Vorwerk, S., Somerville, S., and Somerville, C. (2004). The role of plant cell wall polysaccharide composition in plant disease resistance. Trends Plant Sci. 9, 203–209.[CrossRef][ISI][Medline] Wakeley, P.R., Rogers, H.J., Rozycka, M., Greenland, A.J., and Hussey, P.J. (1998). A maize pollen methylesterase-like gene, ZmC5, specifically expressed in pollen. Plant Mol. Biol. 37, 187–192.[CrossRef][ISI][Medline] Related articles in Plant Cell:
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KEY FEATURES OF POLLEN...
ROLE OF PECTIN METHYLESTERASES...
11 s later. Nonetheless, maintenance of the dynamic Ca2+ gradient is essential for pollen tube growth and seems to involve complex interactions among ROP GTPases, the actin cytoskeleton, and Ca2+ at the level of intracellular signaling (Li et al., 1999
-amino butyric acid in pollen tubes that is important in regulating growth and guidance toward the ovule (Palanivelu et al., 2003