Pollen Tube Guidance: The Role of Adhesion and Chemotropic Molecules

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Publisher Summary

In many reproductive systems, adhesion and guidance are essential components of fertilization. In animals, sperm cells are motile and when guided to the egg cell, the sperm penetrates through the extracellular matrix (ECM) and adheres to the egg plasma membrane. Sperm cells in marine animals and algae are released into the open sea and must be guided to the egg. Marine invertebrates provide excellent material for the study of fertilization and information about the basic biology of the interaction between cell surfaces, as well as discoveries of the few molecules known to be involved in sperm–egg interaction. Motile sperm cells are also present in the lower divisions of land plants and in some seed plants. In ferns, sperm cells are released from the male gametophyte (gamete producing haploid phase of the life cycle) and swim, usually through rainwater, to the nearby female gametophyte, which bears archegonia with eggs enclosed. In both animals and plants, guidance cues from the female tissues are critical to accomplish fertilization. One of the most extensively studied guidance mechanisms is chemotaxis, defined as the movement of a cell up a molecular gradient; chemotropism refers to the growth of a cell up a molecular gradient. Adhesion molecules have been implicated in guidance in both reproduction and in embryonic cell movements in animal development, including neuron guidance. In plants, adhesion molecules are involved in reproduction, both in guidance and in the fertilization event, of gamete fusion. It is not unusual to find the same molecules involved in both adhesion and chemotropism in animals. However, in plants only a few such molecules have been reported. Recently, molecules involved in both pollen tube adhesion and guidance have been isolated from the flowering plant stigma and style transmitting tract tissues. This chapter discusses adhesion and chemotropism and looks at a chemotropic peptide in the lily stigma.

Introduction

In many reproductive systems, adhesion and guidance are essential components of fertilization. In animals, sperm cells are motile and when guided to the egg cell, the sperm penetrates through the extracellular matrix (ECM) and adheres to the egg plasma membrane (Primakoff and Myles, 2002). Sperm cells in marine animals and algae are released into the open sea and must be guided to the egg. Marine invertebrates have provided excellent material for the study of fertilization and information about the basic biology of the interaction between cell surfaces as well as discoveries of the few molecules known to be involved in sperm–egg interaction (Kresge 2001, Maehashi 2003, Riffell 2002, Ward 1985). Motile sperm cells are also present in the lower divisions of land plants and in some seed plants. In ferns, sperm cells are released from the male gametophyte (gamete producing haploid phase of the life cycle) and swim, usually through rainwater, to the nearby female gametophyte, which bears archegonia with eggs enclosed. In fact, the first sperm chemotropic compound described was malic acid, which is produced by the receptive archegonium in ferns (Mascarenhas, 1978). Sperm attractants in ferns and algae are small organic compounds lacking nitrogen, but in animals they are typically peptides or small proteins 1–25 kDa in size (Cosson 1990, Eisenbach 1999).

The more advanced flowering plants, the angiosperms, have a complex architecture of reproductive tissues contained in the flower, a modified shoot system that encloses the gametophyte phases of the life cycle (Lord and Russell, 2002). The term angiosperm literally means “vessel seed,” in reference to the pistil (stigma, style, and ovary), which encloses the ovule in which the egg resides. Sperms in flowering plants have become immotile: they have lost their flagella, but still move with the assistance of an unusual plant cell type produced in the anthers, called pollen, a highly reduced male gametophyte. Pollen is like a spore into which two sperm cells are endocytosed during development. Pollen tubes grow by tip growth and function to convey the sperm cells to the egg. The stigma provides the female receptive surface at which pollen grains, carried in the air by various mediators (wind, insects, etc.), land, adhere, hydrate, and germinate to produce pollen tubes. The stigma is the entry into the pistil's specialized transmitting tract tissue, which produces an ECM that acts to guide the pollen tube into the style. The style connects the stigma to the ovary and the pollen tube must be guided through the transmitting tract ECMs to the ovule to reach the egg. At the entrance to the ovule, the pollen tube is guided into the embryo sac (the female gametophyte), where it ruptures and releases two sperm cells for double fertilization. One sperm cell is guided to the egg cell where it fuses and makes the zygote, and the other is guided to and fuses with the central cell, the result of which forms a polyploid, nutritional tissue for the developing embryo in the seed (Fig. 1A). For successful fertilization in plants, correct and timely delivery of the sperm cell to the egg is essential. Guidance of the pollen tube in the pistil plays a major role in plant reproduction, but we know relatively little about the molecules involved.

In both animals and plants, guidance cues from the female tissues are critical to accomplish fertilization (Lord, 2003). One of the most extensively studied guidance mechanisms is chemotaxis, defined as the movement of a cell up a molecular gradient; chemotropism refers to the growth of a cell up a molecular gradient. Many compounds are known to be responsible for sperm chemotaxis in invertebrates (Gagnon, 1990) and many molecules are capable of attracting the motile mammalian sperm cell, but those active in vivo have been difficult to find. The only known vertebrate sperm chemotactic molecule is a small protein called allurin, which is produced by the Xenopus egg (Olson et al., 2001). In plants, the idea that chemotropism occurs in pollination was considered dubious by some (Heslop-Harrison and Heslop-Harrison, 1986) and the idea of a universal chemoattractant in flowering plants was discarded years ago. But, the consensus at present is that a variety of mechanisms exist in the flowering plants for pollen tube guidance (Johnson and Preuss, 2002).

Adhesion molecules have been implicated in guidance in both reproduction and in embryonic cell movements in animal development, including neuron guidance. In plants, adhesion molecules are involved in reproduction both in guidance and in the fertilization event of gamete fusion (Lord and Russell, 2002). It is not unusual to find the same molecules involved in both adhesion and chemotropism in animals (Li 2001, Olson 2001). However, in plants only a few such molecules have been reported. Recently, molecules involved in both pollen tube adhesion and guidance have been isolated from the flowering plant stigma and style transmitting tract tissues (Kim et al., 2003).

Section snippets

Adhesion and Chemotropism

In animal systems, axon guidance shows some similarities to pollen tube guidance (Palanivelu 2000, Park 2000). In the case of commissural axons, which connect the two symmetrical halves of the central nervous system, growth is first toward the midline and then further across the midline toward the final target (Dickson 2001, Lyuksyutova 2003, Tessier-Lavigne 1996). This guidance is particularly interesting because the same axon should be attracted to the first target and then repulsed from it

Chemocyanin: A Chemotropic Peptide in the Lily Stigma

Chemocyanin is a small basic protein secreted into the lily stigma ECM where, together with the more abundant SCA, it acts to guide pollen tubes into the style (Kim et al., 2003). Chemocyanin is the first described chemotropic peptide in flowering plants. It was purified from the lily stigma by using several in vitro pollen tube chemotropism assays. A crude assay (Fig. 3A, B), based on one described many years ago for lily (Miki, 1954), confirmed the existence of chemotropic factors in the lily

Outlook

Plants spend much of their time and energy in responding to external signals, no doubt because they are rooted in the soil. With their open system of growth at the meristems, they have a limited opportunity to grow away from or toward external stimuli. With growth of new parts, plant cells accumulate like bricks in a wall cemented by their ECMs, which restrain cell movements. We are just beginning to appreciate the amount and variety of signaling that must go on in the ECMs of plants in

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      It is remarkable that, after landing on a stigma, the gametophyte seems to totally or partially lose control again. Pollen–stigma interactions are at least partly controlled by the sporophytic pollen receiver, including: the different incompatibility systems (Mulcahy and Bergamini Mulcahy, 1983; Lee et al., 1994; Swanson et al., 2004), pollen tube growth (Sanders and Lord, 1989; Herrero and Hormaza, 1996; Wilhelmi and Preuss, 1997; Lord, 2000; Kim et al., 2004; Swanson et al., 2004; Crawford et al., 2007; Crawford and Yanofsky, 2007) and interaction with ovules (Wilhelmi and Preuss, 1996; Shimizu and Okada, 2000; Swanson et al., 2004; Higashiyama and Hamamura, 2008). These interactions can also be seen as resulting from conflicts over the control of fertilization, with strong selection on the recipient sporophyte to take control: the gametophyte loses more in not germinating than the sporophyte in blocking or directing the growth of a particular pollen tube.

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