Assembly and Motility of Eukaryotic Cilia and Flagella. Lessons from Chlamydomonas reinhardtii

Abstract

and flagella are among the most ancient cellular organelles, providing motility for primitive eu-karyotic cells living in an aqueous environment. During adaptation to life on land, some groups of organisms, including advanced fungi, red algae, cellular slime molds, conifers, and angiosperms, lost the ability to assemble flagella (Raven et al., 1999). The centriole or basal body, which organizes the assembly of flagella, also is absent in these groups. In other lineages, flagella were retained only on gametic cells. Land plants are believed to have arisen from one group of green algae, the charophytes (for review, see Bhattacharya and Medlin, 1998; Qiu and Palmer, 1999), in which the only flagellated cells are motile sperm. The first land plants, bryophytes, which are thought to be the ancestors of higher plants, also produce flagellated sperm cells that require water to swim to the egg. Ultrastructural features of the basal body apparatus in the flagellated cells have provided important morphological data for phylogenetic studies of algae and bryophytes. The absence of centrioles and flagella in all but sperm cells also characterizes seedless vascular plants (pteridophytes) including ferns and the genus Equisetum (Raven et al., 1999). Water is required for these sperm to swim to the archegonium containing the egg. A further adaptation for colonization on land developed in gymnosperm phyla represented by cycads and gingko. These plants produce pollen grains that are transferred to the vicinity of the female gametophyte. A pollen tube extends toward the archegonium and bursts to release flagellated sperm that swim through the released fluid to fertilize the egg. Sperm in seedless vascular plants, cycads, and gingko are large (up to 300 m in diameter), spectacularly complex cells that swim with hundreds to thousands of flagella. The de novo synthesis of the centrioles during the formation and differentiation of these sperm cells was documented a century ago, but fascinating questions remain about the developmental mechanisms for these events (see, for example, Hart and Wolniak, 1998). How do flagella of plants and animals differ? The main evolutionary difference is that in animals, fla-gella acquired new functions as multicellular forms evolved. For example, in mammals, epithelial cells in the respiratory system, the female reproductive system , and in the ventricles of the brain differentiate to produce multiple cilia that beat coordinately to propel fluids over the tissues. Most types of mammalian cells express a primary cilium whose growth is nu-cleated by the older of the two centrioles in a cell. These organelles have been shown to play crucial roles in embryo development (for review, see Schnei-der and Brueckner, 2000). Modified primary cilia play important roles in the function of sensory cells such as photoreceptor cells (for review, see Rosen-baum et al., 1999). Chlamydomonas reinhardtii, a unicellular, biflagel-late green alga in the order Volvocales, offers unique advantages for studying eukaryotic flagella and basal bodies (Fig. 1). These cells use flagella for motility and for cell-cell recognition during mating. Located on the surface of the cell, flagella may be isolated easily for biochemical analysis. More than 200 different proteins have been identified in the axoneme; at least an equal number of proteins comprise the basal body apparatus that regulates the assembly and positioning of the flagella. Although C. reinhardtii and mammals are separated by more than 10 9 years of evolution, C. reinhardtii flagella are amazingly similar in structure and function to mammalian cilia and flagella. For example, some of the flagellar proteins in C. reinhardtii show more than 75% identity and similarity to proteins with similar function in human sperm. FLAGELLAR FUNCTION IN C. REINHARDTII All plants need to optimize their exposure to light by growing toward it, as land plants do, or by swimming toward it, as flagellated organisms do. C. rein-hardtii cells swim to optimal light levels by regulating flagellar beating in the process of phototaxis. The two anterior flagella, 12 m in length, propel the cell forward by beating in opposite directions with an 1