Journal of Experimental Botany, Vol. 54, No. 380, pp. 47-54,
January 1, 2003
© 2003 Oxford University Press
Adhesion and guidance in compatible pollination
Received 12 April 2002; Accepted 30 August 2002
Department of Botany and Plant Sciences, University of California Riverside, Riverside, CA 92521-0124, USA
1 To whom correspondence should be addressed. E-mail: LORD{at}ucracl.ucr.edu
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Abstract |
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 Top Abstract IntroductionAdhesion and hydration on...Germination and chemotropism on...Pollen tube guidance in...References |
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The mechanisms of compatible pollination are less studied than those of incompatible pollination and yet most of the angiosperms show self-compatibility. From the release of pollen from anthers to the penetration of the micropyle by the pollen tube tip, there are numerous steps where the interaction between pollen and the pistil can be regulated. Recent studies have documented some diverse ways in which pollen tubes carrying sperm cells are guided to the ovules through the pistil extracellular matrices of the transmitting tract. What is still missing is an understanding of pollen tube cell biology in vivo. A recent finding supports the role of the synergids in the crucial guidance cue for the pollen tube tip at the micropyle, but experimental evidence for other ‘guidepost’ cells in the pistil is still lacking. The fact that the pollen tube must first travel through the matrices of the stigma and style before it can respond to the cue from the ovule makes it likely that there is a hierarchy of signalling events in pollen–pistil interactions starting at the stigma and ending at the micropyle. On the pistil side, several model systems have been used in the discovery of molecules implicated in either physical or chemical guidance. In lily, which has a hollow style, adhesion molecules (pectin and SCA) are implicated in guidance. SCA alone is also capable of inducing pollen chemotropism in an in vitro assay, suggesting that this peptide plays a dual role in lily pollination: chemotactic in the stigma and haptotactic (adhesion mediated) in the style.
Key words: Adhesion, guidance mechanisms, pollen–pistil interactions, pollen tube cells, signalling.
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Introduction |
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TopAbstractIntroductionAdhesion and hydration on...Germination and chemotropism on...Pollen tube guidance in...References |
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In the third century BC Theophrastus, in his Enquiry into Plants, referred to the pollination of the dioecious date palm in a ceremony where a priest shakes a male date palm frond over a female tree to ensure a good date crop (Maheshwari, 1950). This practical, you might say applied, knowledge was not recognized by biologists until 1682 when Grew in his Anatomy of Plants mentioned the stamens of the flower as the male organ and the pollen as necessary for fruit production, but the mechanism remained a mystery. An Italian mathematician and astronomer, Amici (1824) first observed pollen tubes germinating on a stigma. He later proposed that the pollen tube carried the sperm cells to the ovule where the egg resided. Amici was opposed in this view by Schleiden (1837) who claimed that the pollen tube tip contained the young plant and that the ovule simply nourished its growth. This view, that the male component or sperm were ‘seeds’ and the female merely provided the nutrients in which they were planted, was also accepted by many zoologists at the time and harked back to Aristotle’s ideas 2000 years earlier (Horowitz, 1976). The maternal contribution to embryology in general was unsuspected until the 17th century. In the past ten years the field has gained a new appreciation for the role of the gynoecium (pistil) in pollination, but so far only a few molecules are known to be involved in compatible interactions between the pollen tube and the pistil. In this review the focus is mainly on the female side of the compatible pollination process. Those aspects of pollen tube cell biology that still need addressing are highlighted and discussed, so that events in vivo can be better understood. Several reviews have also come out recently on this topic (Franklin-Tong, 2002; de Graaf et al., 2001; Lord and Russell, 2002; Wheeler et al., 2001).
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Adhesion and hydration on the stigma |
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TopAbstractIntroductionAdhesion and hydration on...Germination and chemotropism on...Pollen tube guidance in...References |
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The stigma is the first tissue to receive the pollen grain and in self-compatible species (which predominate in the angiosperms) pollen from the same flower can adhere, hydrate, germinate, and penetrate into the style. The pollen coat contains many molecules involved in the initial interaction with the stigma (Dickinson et al., 2000). The most famous one now is the male determinant of SI in the Brassicaceae, a small cysteine-rich protein (SCR) (Kachroo et al., 2001; Schopfer et al., 1999; Shiba et al., 2001). In Brassica, stigmatic proteins involved in SI, including SLR (S-locus-related glycoprotein), have been implicated in the adhesion of the pollen grain to the stigma (Doughty et al., 2000; Luu et al., 1999). A pollen coat protein was found specifically to bind SLR from the Brassica campestris stigma (Takayama et al., 2000). Binding of the pollen grain to the stigma shows some specificity in Arabidopsis, since related genera were less apt to adhere (Zinkl et al., 1999). After adhesion, the pollen grain hydrates and this step is somehow aided by the presence of the coat that, in Arabidopsis, contains predominantly lipases and oleosins (Mayfield et al., 2001). The loss of one oleosin protein from the coat (GRP17–1) impairs pollen hydration (Mayfield and Preuss, 2000). In an Arabidopsis mutant, Cer6-2, which is depleted in long-chain lipids in the pollen coat, hydration is also disrupted (Fiebig et al., 2000). Hydration of pollen is regulated by controlling water flow into the grain from the stigma. In Brassica, aquaporin-like proteins in the stigma may act as water channels to accomplish this (Dixit et al., 2001).
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Germination and chemotropism on the stigma |
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TopAbstractIntroductionAdhesion and hydration on...Germination and chemotropism on...Pollen tube guidance in...References |
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For many years researchers have noticed that the number of pollen grains on the stigma affected the germination rate. This is known as the mentor effect, but its cause was only recently discovered to be a secreted peptide called phytosulphokine (Chen et al., 2000). This five amino acid, sulphated peptide was found to induce germination in pollen populations of low number. Putative receptors for this peptide are a 120 kDa and a 160 kDa, glycosylated membrane protein. Only two of the four known plant signalling peptides, Clavata 3 and S-locus cysteine-rich protein (SCR), have receptors identified and both are receptor kinases (Matsubayashi et al., 2001).
Once germination occurs, pollen tubes must enter the style. In dry stigma types the adhesion of the pollen grain to a stigmatic papilla determines the point of entry of the pollen tube into the transmitting tract of the style. In wet stigmas the situation is different. Here the extracellular matrices (ECMs) cover the stigma surface and pollen tubes can grow there to some length before penetrating into the style. In the case of tobacco, a lipidic ECM provides a gradient of water that is thought to provide a directional cue of a physical nature for pollen tube penetration into the stigma (Wolters-Arts et al., 1998). In other species, there is evidence of a chemical signal that provides directional guidance for pollen tubes on the stigma to facilitate entry into the stylar ECM. There are many references in the literature to these chemotropic molecules in the stigma, but other than calcium in Antirrhinum majus (Mascarenhas and Machlis, 1962), none have been identified in planta. The chemotropic assays are done by blotting a stigma on an agar growth medium and assaying the imprinted substances for their ability to attract pollen tubes. In this way species were categorized as having chemotropic chemicals in their stigmas or not (Zeijlemaker, 1956; Tsao, 1949). Early studies on lily showed that a small, heat-stable, stigma molecule could attract pollen tubes in vitro (Miki, 1954; Welk et al., 1965). Lily has a hollow style so no tissue penetration is necessary for the pollen tube to enter the style from the stigma surface. Rather, the pollen tubes are guided toward the central canal where they enter the style. A small, heat-stable molecule that shows chemotropic activity on pollen tubes grown in vitro was identified in the lily stigma (S Kim, EM Lord, unpublished data). The molecule is a cysteine-rich peptide called SCA (stigma/stylar cysteine-rich adhesin) (Park et al., 2000). This protein was discovered as a component of the lily style where pollen tubes adhere to the transmitting tract epidermis and are guided to the ovary (Fig. 1) (see below). SCA bound to a pectic polysaccharide from the style is capable of causing adhesion of pollen tubes in vitro (Mollet et al., 2000). This peptide is abundant in the stigma and exists in two forms, one bound to pectin and the other free from the pectin and so able to set up a gradient to guide pollen tubes into the canal (J-C Mollet, EM Lord, unpublished data). In the stigma it appears to behave as a chemotropic molecule and in the style as a haptotactic (adhesion-mediated guidance) molecule in association with the pectin. Whether SCA is also in the ovary and involved in guidance to the ovule is under investigation now.
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In solid stigmas and styles, enzymes are probably needed to facilitate entrance into the transmitting tract ECMs. Several have been described in pollen such as cutinase (Hiscock et al., 1994), polygalacturonase (Dearnaley and Daggard, 2001), pectin esterase (Mu et al., 1994), glucanase (Kotake et al., 2000; Doblin et al., 2001), and endoxylanase (Bih et al., 1999). All of these enzymes could serve to modify the ECM of the stigma and style as the pollen tube traverses the pistil, but it is possible that they act as well on the pollen wall itself. The manner in which the pollen enzymes modify the ECMs they encounter in the pistil and vice versa is still unclear and requires further study. From structural data it appears that the pollen tube ECM and that of the pistil, where they join, become as one entity (Lennon and Lord, 2000). The two matrices may be remodelled to form a third, reflecting components of both.
Group I allergens are the major allergens of grass pollen and so of medical interest. Ninety-five per cent of people allergic to grass pollen have IgE antibodies to group I allergens (Friedhoff et al., 1986). The role for these glycoproteins in pollination biology though is unknown. They reside in the pollen coat and are structurally related to expansins that induce wall loosening in other parts of the plant (Cosgrove et al., 1997). Recently, these same proteins from grass have been shown to have a cysteine proteinase function that may also be involved in matrix modification on the grass stigma that is of the dry, solid type (Grobe et al., 1999).
On the pistil side, much less is known about the stigma-specific genes relating to pollination other than those involved in the rejection of self pollen (Dixit and Nasrallah, 2001). The pis63 gene in Brassica napus is expressed in the stigma papillae where pollen adheres (Robert et al., 1999) and a reduction in the transcript level of this gene results in reduced seed set (Kang and Nasrallah, 2001). Adhesion still occurs in these transgenics, but subsequent events are disrupted in pollination in some unknown way to reduce seed set. A technique used in this last study to isolate stigma-specific genes without having to do tedious tissue isolations is genetic ablation of the stigmatic papillae (Kang and Nasrallah, 2001). This they accomplished using a cellular toxin under the control of a stigmatic papillar cell-specific promoter and then compared mRNA transcripts of wild-type stigmas to those of ablated ones using differential display. Several stigma genes were isolated this way including a homologue of the pis63 gene and pectin methylesterase (PME), a known cell wall modifying enzyme (Micheli, 2001) that could loosen the papillar cell wall in advance of pollen tube penetration.
Changes detected in the stigmatic papilla when pollen tubes penetrate must be numerous, but few have been documented. One striking change is an elevation in secreted calcium at the site of pollen adhesion on the papillar surface (Elleman and Dickinson, 1999). This increase in calcium in the ECM of the transmitting tract on pollination has also been reported in styles (Lenartowska et al., 1997; Russell, 1992; Yu et al., 1999; Zhang et al., 1995) and may be a source of the divalent cation that has been shown to be essential for pollen tube growth in vitro. Application of the pollen coat alone to the stigma can induce changes in papillar cell biology such as loosening of the outer wall layer in Brassica (Elleman and Dickinson, 1999).
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Pollen tube guidance in the style and ovary |
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A recent review (Hepler et al., 2001) covered most of the exciting new work on pollen tube cell biology including the cytoskeleton and ion channels. The biology of the in vivo pollen tube cell remains somewhat of a mystery though, due to the technical difficulties encountered in observing pollen tubes in the style. The pollen tube, carrying the sperm cells, which are endocytosed into the tube cell, grows by tip growth through the ECM of the transmitting tract of the pistil. How the tube cell is maintained at the tip of the pollen tube for such long distances is unclear.
There is an actomyosin driven, reverse fountain streaming of the cytoplasm in the tube cell that may play a role in the net forward movement of the tube cell protoplast. The mechanism that results in the tube cell movement along the wall is unknown. Microtubules (MT) may be involved since drug treatments that disrupt MTs allow for tube cell cytoplasm to be trapped behind the last callose plug (Joos et al., 1994). There is also evidence of MT motor proteins associated mainly with the cortical MT (Cai et al., 2001) that could be involved in net forward movement.
Though in vitro pollen tube growth rates may achieve the rates seen in vivo for the first phase of growth (i.e. 10–15 µm min–1 in lily) (Messerli et al., 2000), they never grow as fast or as long as in vivo-grown tubes, established on the transmitting tract of the style. Here the rates can be 45 µm min–1 (lily) (Jauh and Lord, 1995) or even 180 µm min–1 (maize) (Barnabas and Fridvasky, 1984). Clearly, speed is of the essence when hundreds of pollen tubes start on a stigma and only a fraction of them will fertilize ovules. No in vitro system has been developed to mimic these fast rates of tube cell movement.
Using GFP tagged actin-binding domain of mouse talin, Yang’s laboratory has found a dynamic form of F-actin at the pollen tube tip (Fu et al., 2001). These short F-actin bundles are regulated by Rop-GTPase, which belongs to the Rho family (Zheng and Yang, 2000). These short F-actin bundles are necessary for tube growth and oscillate in appearance at the tip. How they function in tip growth is unknown, but such dynamic actin is seen as well at the leading edge of moving animal cells and has been implicated in the force that moves the plasma membrane forward in these cells (Pantaloni et al., 2001). Many of the other players at the leading edge such as the ARP2/3 complex (Higgs and Pollard, 2001), are also in plants (Klahre and Chua, 1999) so there may well be parallels between pollen tube tip growth and moving cell systems.
It was once fashionable to invoke turgor pressure alone as the driving force for growth of the pollen tube, but efforts to correlate turgor with growth rates have failed and even measuring turgor in pollen tubes is difficult (Benkert et al., 1997). Pollen tube cells regulate their own turgor. New work on K+ (Fan et al., 2001; Mouline et al., 2002) and Cl– channels (Zonia et al., 2001) is revealing how this occurs but a purely physical mechanism for pollen tube growth is unlikely given the new information on the role of F-actin and Rop GTPase signalling at the tip (Fu and Yang, 2001).
When you read the voluminous and contested literature on pollen tube guidance in the pistil you realize quickly how much variation there is in the mechanisms of pollination in the flowering plants. Attempts to describe universal models for pollination, whether self-incompatible or compatible, have failed. Instead, plants have a variety of ways to reject self pollen and probably also a variety of ways to accept compatible pollen and guide the sperm cells to the ovule. To date, there is no one compatible system that is thoroughly understood, but there are aspects of several systems for which there are data showing that pollen tube guidance probably does occur in the pistil and some of the mechanisms involve proteins and glycoproteins. One major obstacle to this research is the technical difficulties that arise in demonstrating chemotropism in vivo. The data are usually from in vitro studies and sometimes accompanied by genetic studies that implicate proteins in guidance.
The tobacco style contains a glycoprotein called TTS (transmitting tract specific glycoprotein) which occurs in a glycosylation gradient in the style and which is chemotropically active towards pollen tubes in vitro (Cheung et al., 1995; Wu et al., 2001). TTS is an AGP and this class of molecules is abundant in styles (Clarke et al., 2000). TTS is deglycosylated by pollen tubes in vivo and in vitro and the sugars are incorporated into the pollen tube wall. TTS is one of the few examples of a chemotropic stylar molecule where genetic data using transgenics has provided support for its role in pollen tube growth in the style.
The fact that pollen tubes incorporate stylar molecules into their tube cell during passage down the style has led to the proposal that the stylar ECM is a source of nutrients for these fast-growing cells that must produce an extensive wall to transport the sperm cells to the ovule. There are other studies showing the incorporation of stylar matrix molecules into pollen tubes (Bosch et al., 2001), a striking example being the pistil S-gene product in gametophytic SI (Luu et al., 2000). How these molecules, many of them quite large, are incorporated into pollen tubes is not understood though there is some evidence for endocytosis at the pollen tube tip (O’Driscoll et al., 1993). The fact that pollen tubes secrete enzymes to modify the ECMs they grow in also implies they are utilizing these molecules for growth.
Calcium has long been proposed as a chemotropic factor in pollination, but no gradients have been detected in styles other than in Antirrhinum (Mascarenhas, 1966, 1978). There is some evidence that pollination itself can induce the secretion of calcium into the transmitting tract that then becomes taken up by pollen tubes (Yang, 2001; Yu et al., 1999). Another case where pollen tubes act on stylar matrix molecules that may result in guidance is that of pectins in the Petunia style (Lenartowska et al., 2001). Here the matrix is full of low esterified pectins that bind Ca2+ prior to pollination and these pectins become degraded, presumably releasing calcium to the ECM as pollen tubes grow through the style. Pollen tubes and stylar matrices contain polygalacturonases that can accomplish the breakdown of low esterified pectins and the released calcium may be incorporated into the growing pollen tube. It is well known that in vitro growth of most pollen tubes requires calcium in the medium, but a source of calcium for pollen tube growth in the style is unknown.
Once the pollen tubes reach the ovary they are guided by the placental tissues to the ovules where a last guidance event occurs which is very dramatic, entrance into the micropyle and the embryo sac. The exciting findings in this stage of guidance are due to several genetic studies that implicated the female gametophyte (Hulskamp et al., 1995; Ray et al., 1997; Shimizu and Okada, 2000). Using a novel in vitro fertilization system, Higashiyama and his colleagues were able to show that the synergids themselves were the source of the chemotropic substance (Higashiyama et al., 2001, 1998) as predicted by earlier studies (Russell, 1992). Pollen tubes had to travel through the stigma and style before they were capable of perceiving this signal at the ovule, which supports the hypothesis that there is a hierarchy of guideposts in the pistil that signal the pollen tube as it progresses to the ovary. How the pollen tube perceives these signals is of interest to several laboratories that are exploring the receptor kinases in the pollen tube plasma membrane and looking for their ligands in the stylar ECMs of the pistil. Plant receptor serine/threonine kinases comprise a large class of receptors in plants (McCarty and Chory, 2000). These include several structural families including the LRR-type (leucine rich repeat) and the S-domain type (S-glycoprotein). There is a receptor kinase in tomato pollen tubes that is specifically de-phosphorylated by contact with stylar extracts (Muschietti et al., 1998). Using a yeast two hybrid system McCormick’s group has isolated many possible ligands for this transmembrane kinase, many of which are secreted molecules likely to reside in the stylar matrix. One candidate, LAT52, occurs in the pollen tube wall itself (Tang et al., 2002). PEX glycoproteins are found in the pollen walls of maize and tomato and they also have conserved LRRs (Stratford et al., 2001).
There is too little information about the cell biology of pollen tubes growing in vivo. A few structural studies have revealed significant differences in these cells compared to those growing in vitro (Lennon and Lord, 2000; Roy et al., 1997). One common aspect of in vivo pollen tubes is their adhesion to the transmitting tract cells which act to guide them to the ovules (Lord, 2000). In lily, molecules from the style that cause this adhesion event between pollen tubes and transmitting tract epidermis (TTE) (Fig. 1) have been isolated (Mollet et al., 2000; Park et al., 2000). They are a pectic polysaccharide and a peptide, SCA (stigma/stylar cysteine rich adhesin). Together these two molecules are bound to the surface of the TTE cells and cause adhesion of the pollen tubes to this surface and to one another. The receptor in the pollen tube is not known, but it probably resides in the tip because the adhesion event occurs there and only with tube growth. An in vitro adhesion assay was developed to isolate the stylar ECM molecules involved (Jauh et al., 1997). Since the two molecules are present on the TTE surface that forms the tract from the stigma to the ovule, they may be laying a trail of adhesion molecules that act to guide the pollen tubes to the ovule much as occurs in neuron guidance. Neurons are guided by netrin, a small matrix protein, and by laminin, a large matrix adhesion molecule. Netrin receptors occur in the axon and the guidance occurs mainly due to a path of laminin and netrin laid out that the axon follows (Song and Poo, 2001). Such a mechanism could explain the role of adhesion and guidance in the style that does not have to invoke long-range chemical gradients.
Small cysteine-rich secreted proteins are frequently mentioned in the literature as ligands for cell surface receptors in a variety of recognition phenomena. The female SI factor in poppy is a small cysteine-rich protein (Franklin-Tong, 2002) as is the pollen coat SI factor in Brassica, SCR. SCA and SCR show no sequence similarity, but both are basic cysteine-rich peptides involved in reproductive processes, one from the pistil ECM (SCA), the other from the pollen ECM (SCR). Both are related to defence proteins (SCA is LTP-like and SCR is defensin-like, both known antimicrobial peptides). In animal systems cysteine-rich peptides are showing up in screens for chemotropic molecules and some are involved as well in adhesion and antimicrobial behaviour (Li et al., 2001; Olson et al., 2001). Allurin is a sperm chemotropic peptide involved as well in sperm/egg adhesion in Xenopus. This cysteine-rich peptide belongs to the CRISP family of proteins that contains one plant member, PR-1. The link between signalling in reproduction and pathogenesis-related proteins appears to cross phyla.
In lily, the first pollen tubes to enter the style adhere to the TTE cells where both the SCA and pectin reside. With continued pollination, layers of pollen tubes form so the next waves of tubes adhere to those that came before. Pollen tubes do not adhere in vitro in liquid medium so the style induces this adhesion even if the tubes do not directly contact the TTE cells. The first pollen tubes on the tract are probably the ones to cause fertilization and they may be acting as the ‘pioneer axons’ do (Bentley and Caudy, 1983), laying a path for those to follow in what could be called a stylar ‘mentor effect’ as occurs on the stigma. It would be interesting to know the fate of these pioneer pollen tubes versus those that follow. An abundance of pollen usually germinates on the stigma, much more than is needed for fertilization and a ‘weeding out’ occurs in the style (Malti and Shivanna, 1985). The mechanism for this is not known, but several guideposts have been described in fruit tree pistils that appear to be involved in selection (Herrero, 2001).
Adhesion and guidance are themes in animal cell movement (Burridge and Tsukita, 2001), but much less is known about the effects of adhesion in plant cells since cell movement occurs only in pollination. Adhesion is ubiquitous in plant cells, between cell walls and plasma membranes and walls, but the component molecules are not known. WAKs are certainly good candidates for PM/wall adhesion molecules (Kohorn, 2001) and pectins are known to reside in the middle lamellas, the extracellular sites of adhesion in plant cells laid down during cell division (Willats et al., 2001). Adhesion of the PM-cell wall is necessary for plants to respond to invading pathogens (Mellersh and Heath, 2001). Pollen tubes secrete an ECM at their tips to which the protoplast adheres, if only briefly, as evidenced by Hechtian strands (fine cytoplasmic strands adhered to the PM) when pollen tubes are plasmolysed (Parton et al., 2001). Further back in the pollen tube the PM is not attached to the wall; in fact the movement of the tube cell along its secreted wall or ECM precludes adhesion. The effects of adhesion on the pollen tube cell biology need to be studied. Previous work comparing in vivo- to in vitro-grown lily pollen tubes showed F-actin configurations in the in vivo tubes that looked like focal adhesions (Jauh and Lord, 1995; Pierson et al., 1986), but use of the lily adhesion assay did not induce these striking F-actin configurations (EM Lord, unpublished data). The effect on the cytoskeleton of pollen tube adhesion to the stylar ECM needs to be studied in vivo, preferably with live pollen tubes.
To summarize, recent attempts to study pollination in vivo, though technically difficult, are revealing a potentially fascinating system of signalling events. The work on self-incompatibility pioneered this approach and helped to show the complexity of signalling in this unusual case of cell–cell interaction in plants. One of the key areas still needing exploration is the cell biology of the pollen tube as it progresses through the transmitting tract of the pistil. So far, there is good evidence that the tube cell develops as it progresses from the stigma to the ovary acquiring the ability to respond to a last guidance event at the micropyle. There is virtually no information about the manner in which the tube cell progresses along the wall of the pollen tube as it travels often long distances to the ovary. Is there a mentor effect in the style and if so how does it affect the outcome of pollination? Adhesion to the transmitting tract matrices occurs in all instances studied in at least the placental area of the ovary and, in many cases, throughout the pistil. What is being communicated to the tube cell through these matrix interactions? Are sperm cells affected or are they passive cargo until entrance into the ovule? A continued focus on the interaction between the male gametophyte and the gynoecium will provide a wealth of new information about the unique way in which flowering plants get the sperm to the egg.
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