JXB Advance Access originally published online on September 15, 2006
Journal of Experimental Botany 2007 58(1):75-82; doi:10.1093/jxb/erl122
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RESEARCH PAPER |
Structural and functional compartmentalization in pollen tubes
1Department of Biochemistry and Molecular Biology, University of Massachusetts, Lederle Graduate Research Tower, Amherst, MA 01003, USA
2Molecular Cell Biology Program, University of Massachusetts, Lederle Graduate Research Tower, Amherst, MA 01003, USA
3Plant Biology Program, University of Massachusetts, Lederle Graduate Research Tower, Amherst, MA 01003, USA
* To whom correspondence should be addressed. E-mail: acheung{at}biochem.umass.edu
Received 14 January 2006; Accepted 17 July 2006
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Abstract |
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Eukaryotic cellular functions are achieved by concerted activities in the cytosol and functions compartmentalized in the nucleus and other membrane-bound organelles. Moreover, the cytosol and nucleoplasm are populated with mega molecular ensembles that are specialized for different metabolic and biochemical processes. Pollen tubes are unique plant cells with a dramatic growth polarity. Tube growth is restricted to the tip and is supported by a polarized cytoplasmic organization. The apical region of elongating pollen tubes is a domain occupied exclusively by transport vesicles to support the secretion and endocytic activity needed for the rapid cell expansion at the apex. Larger organelles are predominantly segregated to the cytoplasm distal to the subapical region. Underlying the organelle compartmentalization is an elaborate actin cytoskeleton with distinct structural and dynamics properties at the tip, in the subapical region, and in the cytoplasm subtending it. Cytoplasmic domains with differential ionic conditions and spatially restricted localization of molecules in pollen tubes may also be important for regulating the polar cell growth process. The polarized cellular organization in pollen tubes drives an extremely efficient cell growth process that is responsive to extracellular signals, including directional cues. It may be an amplified framework of the cytoplasmic architecture that supports growth in other plant cell types that involves considerably more subtle and transient differential cell expansion.
Key words: Molecular and ion compartments, organelle, pollen tubes, tip-growth, vesicle
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Introduction |
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Structural and functional compartmentalization in the nucleus, cytosol, and organelles such as the mitochondria, chloroplasts, Golgi bodies, and lysosomes differentiates eukaryotes from prokaryotes. When considering the growth, maintenance, and development of a plant, it is quite easy to conceive that many cells maintain or undergo transient organization of functional compartments to carry out spatially-restricted processes or in response to spatially oriented cues. For instance, the presence of a cell plate assembly matrix at the equatorial plane of dividing cells reflects a polarized organization of an elaborate network of cytoskeletal and secretory organelles to support cell plate formation during cytokinesis (Assaad, 2001; Segui-Simarro et al., 2004; Jurgens, 2005). Moreover, functional compartments may be distinct at the molecular level. For instance, the basal cell membrane where the auxin efflux proteins PINs are located (Paponov et al., 2005) may be regarded as a functional domain to achieve directional transport of auxin and to establish a hormone gradient essential for apical–basal patterning and other developmental characteristics of a plant (Weijers and Jurgens, 2005). Differential organization of cellular structures and activities undoubtedly underlie a polarized cell growth process. For instance, the formation of lobes in epidermal cell differentiation, a subtle polar outgrowth process involving differential expansion of contiguous membrane domains, is supported by localized concentrations of cytoskeletal and vesicular components (Bloch et al., 2005; Fu et al., 2005). In flowering plants, pollination relies on a dramatic polar cell growth process, pollen tube elongation. Upon landing on the stigmatic surface of the pistil, pollen grains hydrate and germinate by extruding the polarized outgrowth of a pollen tube. Pollen tubes elongate rapidly and directionally within the female tissues and extend over long distances from the stigma to the ovules to deliver the male gametes to the egg and central cell in the embryo sac for a double fertilization process (Cheung, 1996; Cheung and Wu, 2001; Lord and Russell, 2002). Pollen tubes elongate in a tip-growth process whereby cell expansion is restricted to the apex of the tubular structure. As the tip advances, a callosic partition is laid down periodically some distance from the tip and compartmentalizes the protoplast with a majority of its cytoplasm to the most proximal region of the tube. It is the chemical staining of these callosic plugs that gives rise to the dramatic images that have come to be associated with pollen tubes (Fig. 1). Early cytological and physiological studies on pollen tubes revealed a dramatic compartmentalization pattern of organelles and non-membrane-bound cytosolic domains in elongating pollen tubes (for reviews see Steer and Steer, 1989; Derksen et al., 1995a, b; Hepler et al., 2001; Feijo et al., 2004). Recent molecular and cell biological studies have affirmed the traditional view that the pollen tube tip region is concentrated with hydrolytic enzymes secreted to the extracellular matrix to facilitate growth and membrane-associated signalling molecules that perceive extracellular signals and regulate the tip-growth process. They have also provided refined information on the structural and functional segregation within the pollen tube cytoplasm. These recent observations are discussed here in the light of long-standing knowledge on the cytosolic organization and growth characteristics of these uniquely motile plant cells.
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Organization of organelles in the polarized pollen tube cell |
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 TopAbstractIntroduction Organization of organelles in... The apical cytoplasm as...The subapical region as...Cytoplasmic zoning of ions...Dynamic relationship between non...PerspectiveReferences |
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The polarized pollen tube morphology is accompanied by an asymmetric distribution of cellular organelles, many of which are highly motile and display what is referred to as a reverse-fountain streaming pattern i.e. they move tip-ward along the edge of the tube, reverse direction in the subapical region and flow grain-ward in the centre of the tube. Light microscopy revealed a relatively smooth cytoplasm restricted to an inverted cone region, called the clear zone, at the apex of elongating pollen tubes (Fig. 2). This is subtended by cytoplasm populated with highly motile structures that rarely invade the clear zone. Detailed ultrastructural analyses of pollen tubes showed that the clear zone is almost exclusively occupied by transport vesicles, whereas larger organelles are located in the cytoplasm distal to the clear zone (Lancelle and Hepler, 1992; Derksen et al., 1995a). Mitchondria and Golgi bodies were seen throughout the pollen tube, but there were few in the inverted cone region while the highest concentration was found in the subapical region (
5–25 µm distal to the apex in a tobacco pollen tube, which is around 10 µm in diameter). Tubular endoplasmic reticulum was seen most concentrated at 5–10 µm from the apex and outside the inverted cone of vesicles whereas rough endoplasmic reticulum was abundant, starting behind the inverted cone region and throughout the rest of the cytoplasm. In these studies, the region around 5–25 µm from the apex was said to correlate with where the cytoplasmic streams reversed direction. Recent live-cell images of pollen tubes expressing GFP-labelled organelle-associated proteins revealed a polarized cytoplasmic organization consistent with these ultrastructural analyses (Fig. 2). Moreover, they vividly showed the dynamics of organelle motility (Cheung, 2001; Chen et al., 2002; Cheung et al., 2002; De Graaf et al., 2005).
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The male germ unit, which is comprised of the tube cell nucleus and two sperm cells, may be viewed as a genetic compartment of the male gametophyte; it is usually located distal to the subapical region. Although the pollen tube cytoplasm is occupied by numerous vacuoles (Hicks et al., 2004), a large vacuole constitutes the majority of cellular volume in the most distal region of the pollen tube protoplast and is believed to provide turgor to the expanding cell and contribute to its ionic homeostasis. Interestingly, vacuoles in pollen tubes of a Nicotiana species that displays self-incompatibility seem to act as a sequestration compartment for S-RNases during compatible pollen tube growth (Goldraij et al., 2006). This compartmentalization apparently breaks down during incompatible pollination, releasing S-RNases to the cytoplasm and resulting in pollen tube growth arrest.
How the boundary of an apical cytoplasm packed with vesicles and a trailing organelle-rich cytoplasm in the pollen tube shank is maintained is not well understood. Pollen tube growth and cytoplasmic streaming are largely supported by activity from the actin cytoskeleton as both processes are sensitive to inhibition by pharmaceuticals that inhibit actin polymerization (Hepler et al., 2001). Phalloidin-staining of chemically fixed pollen tubes revealed long actin cables that extend along the length of the tube, except in the apical region. These, together with the reversal of cytoplasmic streaming directions in the subapical region, lend support to the view that actomyosin-based intracellular trafficking activity maintains the segregation of vesicles to the apical clear zone and localization of larger organelles thereafter distal to this apical cytosolic domain. That the tip-focused concentration of transport vesicles is rapidly dissipated by actin-inhibiting drugs also supports a critical role of actin-based motility for the short-distance trafficking of these vesicles to and from the tip membrane (De Graaf et al., 2005). The differential distribution of cellular structures suggests a logical functional compartmentalization whereby the transport vesicles deliver copious amounts of membrane and wall materials to support cell growth at the tube apex and the subtending cytoplasm recycles larger organelles to ensure a continuous supply of freshly loaded secretory vesicles and the recycling of endocytic vesicles from the tip.
Although they are rather abundant, align with actin cables along the long axis of pollen tubes, and form associations with the endoplasmic reticulum and the cell membrane, the role of microtubules in angiosperm pollen tubes remains uncertain since tip growth is little affected by microtubule inhibitors (Derksen et al., 1995b; Lancelle and Hepler, 1992; Hepler et al., 2001; Geitmann and Emons, 2000). On the other hand microtubules apparently play an important role in maintaining the germ cell unit as a co-migrating compartment within the tube cytosol (Astrom et al., 1995). Moreover, organelles isolated from tobacco pollen tubes have been shown to be capable of translocating along in vitro assembled microtubules, leading to the suggestion that microtubules could be used for short-range transport in pollen tubes (Romagnoli et al., 2003). Furthermore, in gymnosperm pollen tubes, microtubules apparently co-ordinate with the actin cytoskeleton and profoundly affect gymnosperm pollen tube growth and its cytoplasmic streaming pattern at the tube tip, which is characteristically distinct from that in angiosperm pollen tubes (Anderhag et al., 2000; Justus et al., 2004).
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The apical cytoplasm as a functional compartment that supports focused growth at the pollen tube tip |
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When GFP-labelled secretory proteins were expressed in elongating pollen tubes, they were observed to concentrate most predominantly at the inverted cone region (Cheung et al., 2002; De Graaf et al., 2005) (Fig. 2), consistent with this cytoplasmic domain being packed with secretory vesicles. Moreover, permeable lipophilic FM dyes (Bolte et al., 2004) were taken up into pollen tubes and concentrated in the inverted cone region in a temporal pattern consistent with occupancy by transport vesicles that have arisen from recycled endocytosed membrane (Camacho and Malho, 2003; Parton et al., 2003). Thus the clear zone cytoplasm is packed with both exocytic and recycled vesicles. When pollen tubes expressing a secretory form of GFP or other GFP-labelled secretory proteins were observed using time-lapse microscopy, punctate fluorescent structures were constantly observed to be feeding into the inverted conical region from the tipward cytoplasmic stream and out from the region into the grainward cytoplasmic stream at the base of the inverted cone, consistent with the notion that the collection of vesicles in the apical domain is constantly being recycled (AY Cheung and H-M Wu, unpublished observations; Parton et al., 2003).
Functionally, the ability of pollen tubes to maintain a tip-focused cytosolic domain packed with transport vesicles is essential for their rapid and directionally-guided growth characteristics (Camacho and Malho, 2003; De Graaf et al., 2005). Disrupting membrane trafficking along the secretory pathway abolished the apical concentration of vesicles, resulting in considerable retention of secreted proteins and retarded pollen tube growth (Cheung et al., 2002; De Graaf et al., 2005). These pollen tubes developed a broader girth, suggesting that membrane expansion and the deposition of cell wall material have occurred over a broader domain around the apical and subapical regions as vesicle fusion was more evenly distributed around the apical dome rather than focused at the apical membrane. In more severe cases, the ability of pollen tubes to follow a stable growth trajectory was highly compromised and these pollen tubes tended to twist and turn. Presumably, the foci for maximum secretory activity was not maintained at the extreme apex but shifted around the apical dome, resulting in migrating areas of membrane expansion and thus the meandering growth path. The dissipation of this apex-focused compartment of transport vesicles had severe consequences on reproductive success as male fertility became compromised. Under normal conditions, pollen tubes elongating in the pistil also maintain a prominent concentration of transport vesicles in an apical inverted cone region (De Graaf et al., 2005). It is conceivable that, when tip-focused secretion was compromised, zigzagging pollen tubes would not have been able to maintain a growth trajectory long enough to target and penetrate ovules. Nevertheless, the reduced ability of pollen tubes to penetrate ovules could have been exacerbated by the possibility that targeted secretion of receptors for female factors to the tube apex was also compromised.
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The subapical region as a distinct structural and functional domain in elongating pollen tubes |
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Phalloidin staining revealed subapical cytoplasm marked by a dense mesh of actin cables subtending the apical clear zone (Gibbon et al., 1999; Geitmann et al., 2000; Vidali et al., 2001; Lovey-Wheeler et al., 2005). Live-cell imaging of in vitro elongating pollen tubes expressing a GFP-actin depolymerizing factor (ADF) fusion protein showed a network of interdigitating actin cables at the subapical region and revealed dramatic dynamics associated with this actin mesh (Chen et al., 2002; Cheung and Wu, 2004). This subapical actin structure oscillates back and forth, but always appears to be coincident with where the tipward flow of long actin cables terminate and the reverse flow gets organized. Short actin cables appear to be channelled from the tube flank into the mesh and out from this structure into the reverse flow of long actin cables in the centre of the pollen tube, giving rise to a dynamic basket-shaped structure subtending the mesh with actin cables running towards the rear of the tube. Moroever, the pollen tube membrane in the vicinity of the subapical actin mesh may constitute a zone where nascent actin filaments arise as a result of stimulation by the membrane-associated actin-nucleating proteins, formins (Cheung and Wu, 2004). The intimate spatial relationship between formin-induced nascent actin cables and the actin mesh suggests that they may be recruited into this subapical actin compartment. The dynamic relationships between nascent actin cables synthesized along the apical and subapical membrane, the subapical actin mesh, and the long actin cables in the shank of the pollen tubes will need to be examined in order to gain an understanding on the production and maintenance of this elaborate actin structure.
Observations of numerous elongating pollen tubes expressing GFP-actin binding proteins to mark the actin cytoskeleton show that the subapical actin mesh is a highly sensitive reporter for the vitality of these cells and that the most vigorous tubes display this structure most prominently (AY Chung and H-M Wu, unpublished observations; Chen et al., 2002; Cheung and Wu, 2004). Moreover, this actin mesh is always oriented perpendicular to the growth trajectory, even in turning pollen tubes (Chen et al., 2002), suggesting an interaction with mechanisms that maintain the growth orientation. Studies based on chemical and biological inhibitors of actin polymerization showed that the subapical actin mesh is considerably more sensitive to disruption than the long actin cables in the shank (Gibbon et al., 1999; Vidali et al., 2001). Treatments with the actin polymerization inhibitor latrunculin B led to the rapid dissipation of the apical concentration of transport vesicles (Parton et al., 2003; De Graaf et al., 2005), consistent with an intimate linkage between the subapical actin structure, regulation of secretory activity, and pollen tube growth direction. The subapical region with the dense actin network apparently marks a critical domain for pollen tube growth. This is shown by the observation that its disruption by actin polymerization inhibitors at concentrations considerably lower than that needed to arrest cytoplasmic streaming was coupled to the arrest of tube growth (Vidali et al., 2001). Moreover, polarized growth is also intimately dependent on the proper level of actin-related activity in this subapical region, as perturbing the normal level of actin polymerization (Cheung and Wu, 2004) and the dynamics of actin filaments (Kost et al., 1999; Fu et al., 2001; Vidali et al., 2001; Chen et al., 2002, 2003) invariably resulted in dissipation of this subapical actin structure and substantial actin reorganization. Growth around the apical domain became anisotropic, resulting in pollen tube tip broadening or even ballooning. This prominent subapical actin structure was also observed in pollen tubes elongating within pistil tissues (Chen et al., 2002).
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Cytoplasmic zoning of ions and specific proteins and the polar pollen tube growth process |
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The elaborate structural and functional organization observed in elongating pollen tubes is actually overlying what can be viewed as cytoplasmic zoning at the level of ions and molecules. Elongating pollen tubes maintain a tip-focused cytosolic Ca2+ and H+ concentration gradients (Hepler et al., 2001; Robinson and Messerli, 2002; Holdaway-Clarke and Hepler, 2003; Feijo et al., 2004). In lily pollen tubes, peak apical Ca2+ has been reported to reach 10 µM, declining to around 200 nM a short distance (
20 µm) from the apex. Pollen tubes also maintain a slightly acidic tip. The cytosolic pH had been shown to be about 1 pH unit higher than the so-called alkaline band region located close to the base of the clear zone (Feijo et al., 1999), although a universal presence of a H+ gradient in pollen tube tips remains to be established (Robinson and Messerli, 2002). Nevertheless, a tip-focused Ca2+gradient and an acidic tip, in cases where a detectable H+ gradient is present, are apparently important for pollen tube growth as treatments that dissipate the tip concentration of these ions resulted in growth inhibition. The differential H+ and Ca2+ distribution in pollen tubes must be dependent on intracellular and cell surface regulatory mechanisms that regulate cytosolic ion homeostasis. Tip-focused influx of extracellular Ca2+ via stretch-activated calcium channels are necessary for growth and believed to play an important role in generating the cytosolic Ca2+ gradient (Dutta and Robinson, 2004). However, efflux by plasmalemma-Ca2+ pumps also appears to be critical for pollen tube growth since Arabidopsis knock-out mutants in a pollen-expressed Ca2+-ATPase are severely male-deficient (Schiott et al., 2004). Regulated release from internal Ca2+ stores may also contribute to pollen tube cytosolic Ca2+ dynamics (Franklin-Tong et al., 1996), especially when considering the high density of endoplasmic reticulum in the pollen tube subapical region (Fig. 2D). A current circuit of robust proton influx at the tube apex and efflux at the base of the clear zone has been detected in elongating pollen tubes and probably underlie the maintenance of the H+ gradient (Feijo et al., 1999). Localized ion fluxes would imply restricted localization or activity of ion transporters. In fact, preferential localization of a GFP-H+-ATPase fusion protein to the subapical membrane and a relatively low abundance of this protein at the apical membrane seems most fitting to support the pattern of apical influx and subapical efflux of protons (Feijo et al., 1999; C Certal, J Feijo, AY Cheung, and HM Wu, unpublished observations). Nevertheless, it is apparent that a clear picture on the production and maintenance of differential ionic conditions at the pollen tube apical region and how they are coupled to growth is still to emerge.
To support a growth process that is responsive to the extracellular environment created by the female tissue, the functions of molecules that mediate extracellular signals to the intracellular machinery for growth should also somehow be spatially defined. In fact, Rho-GTPases, known to play essential roles in pollen tube tip growth (Kost et al., 1999; Fu et al., 2001; Chen et al., 2003; Gu et al., 2005), and have been localized to the expanding membrane domains in elongating pollen tubes (Klahre et al., 2006; C Chen, AY Cheung, HM Wu, unpublished results). Moreover, it has been observed that tip membrane-localized Rho GTPases physically associate with a phosphatidylinositol monophosphate kinase, whose product, phosphatidylinositol 4,5-bisphosphate, also localizes to the same membrane domain as the Rho-GTPases, suggesting the clustering of components of a signalling pathway to a restricted pollen tube tip membrane region (Kost et al., 1999). Together, these would suggest that molecular compartmentalization maintained on the cell membrane level must play important roles in mediating extracellular signals and maintaining cytosolic conditions in supporting pollen tube growth.
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Dynamic relationship between non-membrane bound cytoplasmic domains |
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TopAbstractIntroductionOrganization of organelles in...The apical cytoplasm as...The subapical region as...Cytoplasmic zoning of ions...Dynamic relationship between non...PerspectiveReferences |
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Unlike membrane-bound organelles, the cytoplasmic zones described here, the apical zone of transport vesicles, the regions of actins in various configuration, and the cytoplasm with differential ionic constituency in elongating pollen tubes are functional domains whose boundaries are not physically defined. In fact, each of the domains described is a dynamic zone. For instance, it has been observed that in just a period of 2–3 min, the transport vesicles-packed region at the pollen tube tip might occupy a narrow span of cytosol against the apical membrane, then expand to fill a prominent inverse conical volume whose base reached the vicinity of the subapical actin mesh region (between 5–10 µm in tobacco pollen tubes) (De Graaf et al., 2005). The subapical actin mesh is also not defined in its location, but oscillates back and forth to be almost against the apical membrane then retracts to a subapical location. The oscillatory nature of the tip-focused Ca2+ gradient, peak apical Ca2+ concentrations, and oscillations related to H+ conditions and their relationship to growth have all been documented (Hepler et al., 2001; Robinson and Messerli, 2002; Feijo et al., 2004). The oscillatory nature of these cytoplasmic zones with functions in secretion, cytoskeletal activity, and regulating ion homeostasis must somehow be correlated to the oscillatory nature of pollen tube growth, although a clear correlation of how their phase relationship with each other translates into the observed pollen tube growth property is still to emerge. Interestingly, tip membrane Rho-GTPase activity oscillates and seems to do so in the same frequency as growth oscillation, ahead of growth and tip-localized Ca2+, but in phase with GFP-talin revealed apical F-actin (Hwang et al., 2005). This, together with the co-compartmentalization of components of the phosphatidylinositol signalling pathway with Rho-GTPases (Kost et al., 1999), suggest the apical membrane may indeed be a signalling compartment that sets the parameters for orchestrating the multiple cellular pathways that underlie the oscillatory pollen tube tip growth process.
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Perspective |
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The structural and functional compartmentalization in pollen tubes is necessarily dramatized to provide for the rapid polar cell growth characteristics reserved for these uniquely motile plant cells. While it may not be a blueprint, some aspects of the pollen tube cytoplasmic organization pattern must be a framework shared by other plant cell types to maintain their cellular architecture and support growth. Root hairs, for instance, the other tip growth plant cell types, maintain many of the features seen in pollen tubes although at reduced magnitude (Hepler et al., 2001), apparently to match their lower growth activity. Cells whose expansion depends on diffuse growth or differential growth in neighbouring membrane domains, may nevertheless, still rely on linkages between the actin cytoskeleton and vesicle trafficking similar to those observed in pollen tubes (Smith and Oppenheimer, 2005), and Rho-GTPases have been shown to orchestrate downstream pathways regulating actin and microtubules in a concerted manner to achieve differential growth (Fu et al., 2005). Subtle fluctuations in cytosol ionic conditions may modulate the activity of these structural and signalling systems to achieve the required membrane expansion and wall deposition. Additional players that regulate the production and maintenance of these cytoplasmic domains or contribute to the execution of their functions will undoubtedly be identified. The challenge will be to decipher the spatial and temporal relationship between these structural and functional domains during cell growth processes.
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Acknowledgements |
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Research described from our laboratory was supported by the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service, grant numbers 2001-01936, 2003-35304-13241, 2004-35304-14873, 2005-35304-16030.
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  C. B. Lee, S. Kim, and B. McClure A Pollen Protein, NaPCCP, That Binds Pistil Arabinogalactan Proteins Also Binds Phosphatidylinositol 3-Phosphate and Associates with the Pollen Tube Endomembrane System Plant Physiology, February 1, 2009; 149(2): 791 - 802. [Abstract] [Full Text] [PDF]
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 C. B. Lee, K. N. Swatek, and B. McClure Pollen Proteins Bind to the C-terminal Domain of Nicotiana alata Pistil Arabinogalactan Proteins J. Biol. Chem., October 3, 2008; 283(40): 26965 - 26973. [Abstract] [Full Text] [PDF]
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 A. Y. Cheung, Q.-h. Duan, S. S. Costa, B. H.J. de Graaf, V. S. Di Stilio, J. Feijo, and H.-M. Wu The Dynamic Pollen Tube Cytoskeleton: Live Cell Studies Using Actin-Binding and Microtubule-Binding Reporter Proteins Mol Plant, July 1, 2008; 1(4): 686 - 702. [Abstract] [Full Text] [PDF]
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