Sperm Delivery in Flowering Plants: The Control of Pollen Tube Growth

摘要

Although most people think of pollen merely as an allergen, its true biological function is to facilitate sexual reproduction in flowering plants. The angiosperm pollen grain, upon arriving at a receptive stigma, germinates, producing a tube that extends through the style to deliver its cargo to the ovule, thereby fertilizing the egg, and completing the life cycle of the plant. The pollen tube grows rapidly, exclusively at its tip, and produces a cell that is highly polarized both in its outward shape and its internal cytoplasmic organization. Recent studies reveal that the growth oscillates in rate. Many underlying physiological processes, including ionic fluxes and energy levels, also oscillate with the same periodicity as the growth rate, but usually not with the same phase. Current research focuses on these phase relationships in an attempt to decipher their hierarchical sequence and to provide a physiological explanation for the factors that govern pollen tube growth.nnIn animals, meiosis produces gametes that fuse to form a zygote during sexual reproduction. The life cycle of flowering plants, referred to as an alternation of generations, is more complex. Here, a multicellular diploid generation, known as the sporophyte generation, alternates with a multicellular haploid generation, known as the gametophyte generation. Meiosis does not directly produce gametes. Rather, cells of the sporophyte generation undergo meiosis to produce haploid spores, which in turn divide mitotically to give rise to the gamete-producing gametophyte generation. The embryo sac, which bears the ovule and is embedded in the flower, constitutes the female gametophyte generation. The pollen grain is the male gametophyte generation produced from microspores in the anthers of flowering plants, and consists of a vegetative cell and a generative cell. Either in the grain or during pollen tube growth, depending on the species, the generative cell undergoes mitosis to give rise to two sperm cells (Raven et al. 1999).nnDouble fertilization is a hallmark of flowering plants (Dresselhaus 2006). In addition to the fusing of one sperm cell with an egg cell to give rise to an embryo, the second sperm cell fuses with the two polar nuclei in the central cell of the female gametophyte to produce the nutritive triploid tissue of the endosperm. The embryo and endosperm are packaged as a seed, which becomes encased in a fruit formed from the ovary and, in some instances, from additional floral parts. It will be apparent, therefore, that double fertilization is not only necessary for sexual reproduction in flowering plants but also essential for the production of much of the food that we eat, including nuts, seeds, grains, and fruits.nnBecause the sperm of flowering plants have no flagella, they do not depend on water to transport them to the ovule, as do the sperm of protists, bryophytes, ferns, and some gymnosperms. Instead, the pollen grain may travel a great distance, transported by wind or an animal carrier (e.g., bird, bat, insect), before alighting on a receptive stigma and germinating. The sperm cells then travel in the cytoplasm of the large vegetative cell of the pollen tube to their target. A pollen tube is thus the tricellular male gametophyte generation that emerges from a pollen grain to bring about double fertilization.nnPollen tube growth is fast and highly polarized, with new material being added at the tip, which is called the apex. Secretory vesicles inside the pollen tube transport the cellular building blocks required for growth to the apex, where they are incorporated into the extending pollen tube by exocytosis (Hepler et al. 2006). This process is so efficient that a pollen tube from Zea mays (corn) can attain growth rates of up to 1 centimeter (cm) per hour, or approximately 3 micrometers (μm) per second, making it one of the fastest-growing cells known. With the added realization that cell elongation can be visualized under carefully controlled in vitro conditions, the pollen tube becomes an excellent model system for studies of plant cell growth. Clearly, it is ideal for enhancing our understanding of other cells undergoing tip growth, such as root hairs, fungal hyphae, and fern and moss protonemata, but the pollen tube may also serve as an effective model for the many plant cells that exhibit diffuse growth. In defense of this assertion, we note the similarity in cell wall structure and composition and membrane trafficking machinery between pollen tubes and other plant cells.nnIn this article we describe the structure and physiology of a growing pollen tube, focusing on several processes believed to be key in the regulation of growth. We exploit the fact that pollen tube growth oscillates, as do many underlying physiological processes and structural elements. Through an analysis of the temporal and spatial ordering of these many factors, we provide insight into the basic regulatory events that control pollen tube growth. Although we include data from pollen tubes of different species (e.g., Arabidopsis and Nicotiana), we focus in particular on those from the lily family (e.g., the Easter lily, Lilium longiflorum), which, because of their relatively large size and their readiness to germinate in vitro and grow at in vivo rates, have been the subject of many insightful studies.