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(American Journal of Botany. 2008;95:664-671.) doi: 10.3732/ajb.2007388 © 2008 Botanical Society of America, Inc. |
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Cell Biology |
-Tubulin and microtubule organization during meiosis in the liverwort Ricciocarpus natans (Ricciaceae)1Department of Biology, University of Louisiana-Lafayette, Lafayette, Louisiana 70504 USA
Received for publication 28 November 2007. Accepted for publication 9 April 2008.
ABSTRACT
Extant liverworts are "living fossils" considered sister to all other plants and as such provide clues to the evolution of the microtubule organizing center (MTOC) in anastral cells. This report is the first on microtubule arrays and their 
-tubulin-nucleating sites during meiosis in a member of the Ricciales, a specialized, species-rich group of complex thalloid (marchantioid) liverworts. In meiotic prophase, -tubulin becomes concentrated at several sites adjacent to the nuclear envelope. Microtubules organized at these foci give rise to a multipolar prometaphase spindle. By metaphase I, the spindle has matured into a bipolar structure with truncated poles. In both first and second meiosis, -tubulin forms box-like caps at the spindle poles. -Tubulin moves from spindle poles to the proximal surfaces of telophase chromosomes where interzonal microtubules are nucleated. Although a phragmoplast is organized, no cell plate is deposited, and second division occurs simultaneously in the undivided sporocyte. -Tubulin surrounds each of the tetrad nuclei, and phragmoplasts initiated between both sister and nonsister nuclei direct simultaneous cytokinesis. The overall pattern of meiosis (unlobed polyplastidic sporocytes, nuclear envelope MTOC, multipolar spindle origin, spindles with box-like poles, and simultaneous cytokinesis) more closely resembles that of Conocephalum than other marchantiod liverworts.
Key Words: anastral spindle • bryophytes • cytokinesis • evolution • Ricciocarpus natans • Ricciaceae • sporogenesis
There is more variation in microtubule organizing centers (MTOCs) and cytoskeletal organization in liverworts than in any other group of plants (Brown and Lemmon, 2007
). As early-divergent plants sister to all other land plants (Qiu et al., 2006), the critical position of liverworts in our understanding of plant evolution is uncontested. Analysis of the basic cell biology of liverworts (e.g., Cook et al., 1997; Carafa et al., 2003; Shaw and Renzaglia, 2004; Shimamura et al., 2004; Brown and Lemmon, 2006; Mineyuki, 2007; Renzaglia et al., 2007) has revealed a wealth of information on early manifestations of structures and mechanisms involved in plant developmental processes such as the cell cycle, karyokinesis, cytokinesis, and cytodifferentiation.
The liverworts are an extraordinarily diverse group with numerous structures unique to the plant kingdom. There are three basic forms of gametophyte organization in liverworts commonly referred to as leafy, simple thalloid, and complex thalloid. Traditional systems of liverwort classification largely mirror these three body plans. According to the most recent syntheses (Crandall-Stotler and Stotler, 2000; Shaw and Renzaglia, 2004; Forrest et al., 2006), the division Marchantiophyta (liverworts) is divided into the classes Marchantiopsida (complex thalloids) and Jungermanniopsida. The Jungermanniopsida is further divided into the subclasses Jungermanniidae (leafy) and Metzgeriidae (simple thalloid).
This dichotomy is reflected in characters of sporogenesis. The leafy and simple thalloid hepatics (Jungermanniopsida) have quadrilobed sporocytes, whereas the sporocytes of the complex thalloids (Marchantiopsida) are unlobed (Schuster, 1984). Lobing of the cytoplasm in meiotic prophase of the Jungermanniidae can be so extreme that wall ingrowths reach to the nucleus in the small central portion of the sporocyte (Brown et al., 1986). This cytoplasmic shaping is a typically plant-like process involving localized wall deposition and is not the result of actin-driven constriction typical of cytokinesis in animal cells. Recently, girdling bands of microtubules associated with cytoplasmic lobing of the sporocytes were discovered in Aneura pinguis (Brown and Lemmon, 2006). The bands interact to form a cloverleaf pattern in close association with the nucleus and define the cytokinetic planes for the eventual partitioning of the sporocyte into a tetrad of spores following the second division of meiosis. As prophase progresses and the cytoplasm increases in volume, the cytoplasm protrudes through the bands and forms distinct lobes. Thus, the girdling bands appear to be the meiotic equivalent of preprophase bands, having a role in demarcation of the future division planes and the process of cytoplasmic shaping, which together determine the final arrangement of the spore tetrad.
The complex thalloids themselves are an early-divergent and highly evolved group of organisms. Putatively beginning with a simple thalloid body plan like that of the Blasiales, the Marchantiopsida radiated to give rise to more complex chambered forms with elaborate elevated gametangiophores as well as groups such as the Ricciales with cryptic receptacles completely submerged within the thallus. The Ricciales have thalli with simple pores, scattered gametangia, reduced sporophytes, and loss of elaters. This reduction trend accompanied the evolution of exceptional desiccation tolerance and the ability to colonize disturbed areas. This tendency to weediness drove strong selection to reproduce rapidly and provide maximum protection for gametangia (Schuster, 1992, p. 12). Accordingly, the Ricciaceae are highly reduced and one of the most derivative families of the Marchantiopsida. For a thorough discussion of the evolutionary position of ricciod liverworts from an ecological and morphological perspective, see Schuster (1992). In molecular studies coupled with morphological characters, Ricciales was found to be a monophyletic group (Forrest et al., 2006).
An essential component of microtubule nucleation in all eukaryotic cells is -tubulin. In animal and most algal cells, -tubulin is tightly associated with centrioles and comprises a centrosome, an inheritable organelle that is conspicuous throughout the cell cycle. In plants, this organelle is typically absent. The microtubule organizing centers (MTOCs) of plants are diffuse and mobile entities that change in form and location during the cell and life cycles (reviewed by Brown and Lemmon, 2001, 2007). The nature of the highly variable pleiomorphic plant MTOC has been the subject of several recent reviews (Brown and Lemmon, 2007; Mineyuki, 2007; Murata et al., 2007).
Spindle organization in higher plants occurs at the nuclear membrane (Stoppin et al., 1994; Vaughn and Harper, 1998), but a variety of MTOCs occur in the development of the spindle in bryophytes. Five types of MTOCs have been identified (Brown and Lemmon, 2007) based on the location of -tubulin-rich complexes from which microtubule arrays are organized: nuclear envelope (NE-MTOC), plastid envelope (plastid-MTOC), polar organizer (PO), diffuse spheriodal polar mass not associated with membranes (diffuse polar MTOC), and a typical centrosomal MTOC, which arises de novo only in spermatogenesis. Analysis of the patterns of microtubules and their nucleating sites provides additional characters for the study of land plant evolution.
Information on the cytoskeleton and mechanisms of meiosis is known for only three genera of marchantioids, Conocephalum,Dumortiera, and Marchantia, and they differ distinctly from each other (Brown et al., 2007). Dumortiera hirsuta undergoes monoplastidic meiosis with precocious establishment of quadripolarity similar to mosses and hornworts, but with only slight cytoplasmic lobing (Shimamura et al., 2000, 2001, 2004). In early meiotic prophase of D. hirsuta, as in other bryophytes with monoplastidic meiosis (Brown and Lemmon, 1997), the plastids are distributed to the four future tetrad poles where they serve as MTOCs. Microtubules nucleated at the four plastid MTOCs give rise to the meiotic spindle, which is initially quadripolar before becoming bipolar. In contrast, Conocephalum conicum (Brown and Lemmon, 1988) and C. japonicum (Shimamura et al., 1998) undergo polyplastidic meiosis in unpolarized sporocytes. Meiotic prophase spindles of C. japonicum are nucleated at -tubulin in the perinuclear area, and the spindle is gradually organized into a bipolar structure as in higher plants (Shimamura et al., 2004). While C. japonicum regularly produces linear tetrads, a relatively uncommon tetrad arrangement, C. conicum produces variable arrangements of tetrads with cytokinetic planes determined by the interaction of postmeiotic radial microtubule systems (RMSs) emanating from the tetrad nuclei. Recent analysis of Marchantia polymorpha (Brown et al., 2007) rounds out the picture. Meiosis in Marchantia can best be described as oligoplastidic and intermediate between monoplastidic meiosis in Dumortiera and the polyplastidic type of Conocephalum. The plastid in M. polymorpha undergoes regular division and positioning to establish quadripolarity, but then the -tubulin leaves the four plastids and remains as diffuse spheres at the tetrad poles, and the plastids in the four domains divide further. The spindle is initially quadripolar as in monoplastidic meiosis, but it originates from four spheres of diffuse -tubulin rather than from plastid MTOCs (Brown et al., 2007).
As part of our continuing investigation into the evolution of sporogenesis in land plants, we undertook this study of Ricciocarpus natans (L.) Corda with the goal of providing comparable data on MTOCs and the organization of microtubule arrays responsible for the processes of meiosis and cytokinesis in this highly derived liverwort. As in previous studies (Shimamura et al., 2004; Brown et al., 2007), we used the G9 monoclonal antibody against -tubulin from fission yeast. This antibody has been thoroughly characterized and shown to recognize -tubulin in both seed plants (Ovenchkina and Oakley, 2001) and bryophytes (Shimamura et al., 2004). Data from the current study of triple-stained sporocytes show the relationship of -tubulin to the organization of microtubules in all stages of meiosis and cytokinesis.
MATERIALS AND METHODS
Young sporophytes of Ricciocarpus natans (L.) Corda were collected from long-lived populations growing as weeds in greenhouses of the Forest Hills nursery district of central Louisiana, USA. The plants grow profusely and produce copious sporophytes during the cool winter months allowing repeated sampling of materials and replication of experiments. Fertile thalli were sliced transversely to reveal the embedded sporophytes. The sporophytes were teased free from the slices of surrounding thallus and fixed overnight at 4°C in 4% formaldehyde freshly prepared from paraformaldehyde in microtubule-stabilizing buffer (Brown and Lemmon, 1995) as modified for application to liverworts (Brown and Lemmon, 2006). Sporocytes were adhered to coverslips with Mayer’s egg albumin histological adhesive and covered by a thin agarose–gelatin film. Cells were permeabilized with an enzyme/detergent mixture, washed, and incubated with a 1:160000 dilution of mouse monoclonal antibody (G9) and a 1:100 dilution of rhodamine red anti-mouse IgG to label -tubulin and a 1:100 dilution of rat monoclonal anti-
-tubulin and a 1:100 dilution of fluorescein anti-rat IgG to label microtubules. The G9 antibody was raised in mouse against bacterially expressed S. pombe -tubulin (Horio et al., 1999), and its specificity in bryophytes has been thoroughly characterized (Shimamura et al., 2004). Following several washes in water, nucleic acids were stained with 1 µM To-Pro-3 iodide (Molecular Probes, Eugene, Oregon, USA) in deionized H20, before mounting in Prolong antifade reagent (Molecular Probes). Fluorescence was examined with a BioRad (Hercules, California, USA) MRC 1024 confocal laser scanning microscope (CLSM). Series of images were collected in the z-axis and NIH Image software (Research Services Branch, NIMH, National Institute of Health, Bethesda, Maryland, USA; http://rsb.info.nih.gov) used to generate projections for illustrations.
RESULTS
Triple localization of -tubulin, microtubules, and chromatin showed a general scheme of polyplastidic meiosis and simultaneous cytokinesis (Figs. 1–11) in which -tubulin is associated with the nuclear envelope (NE-MTOC), a pattern that is typical of euphyllophytes but rare in bryophytes where it has been reported only in the marchantioid genus Conocephalum. Like Conocephalum, R. natans has a small nucleus to cytoplasmic volume ratio. In early meiotic prophase (Figs. 1, 2), microtubules are arranged in a reticulate pattern over the nucleus and throughout the cytoplasm. This array is associated with -tubulin surrounding the nuclear envelope (Fig. 1B).
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-tubulin becomes concentrated at several foci (3–8) around the nucleus (Fig. 2B) and gives rise to bundles of microtubules that comprise the early multipolar spindle (Fig. 2A). The several poles gradually consolidate into a bipolar structure with truncated polar regions. The mature metaphase spindle has a distinctive cylindrical shape with squared off poles (Fig. 3). -Tubulin is concentrated at the truncated poles where it forms box-like caps. -Tubulin also extends along the distal kinetochore fibers especially those at the perimeter of the spindle (Fig. 3B). Many metaphase I spindles are bent (v-shaped) as is the one shown in Fig. 3A, a phenomenon that may be associated with precocious disjunction of a bivalent (Fig. 3C).
Figure 4 illustrates a fortuitious alignment of two sporocytes in metaphase of first (left) and second meiosis (right). The overall organization of the spindles appears identical. In late anaphase (Fig. 5), the -tubulin is concentrated at the polar regions distal to the sister groups of chromosomes. At a slightly later stage, the -tubulin has migrated to proximal surfaces of the sister nuclei where it is associated with the organization of interzonal/phragmoplast microtubules. Interaction of these opposing sets of microtubules gradually gives rise to a well-defined phragmoplast (Figs. 5–7). The phragmoplast consists of bipolar arrays of dense brush-like microtubules emanating from -tubulin on proximal faces of nuclear envelopes on either side of an unstained midzone (Figs. 6, 7). There is no evidence of cell plate deposition or wall ingrowths in the equatorial region of first meiosis. In inframeiotic interphase (Fig. 8), -tubulin is evenly distributed around surfaces of the nuclei where it is associated with the development of RMSs that clearly delimit dyad domains in the undivided sporocyte.
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-tubulin and microtubules during spindle development and chromosome separation in second division (Figs. 4, 9, 10) is similar to that of first division. Orientation of second division spindles results in tetrahedral positioning of the tetrad nuclei in the voluminous cytoplasm (Fig. 10).
After chromosomes have moved to the poles of second division, -tubulin once again surrounds the nuclear envelopes and microtubules radiating from the newly formed nuclei fill the interzones and radiate into the cytoplasm (Figs. 10, 11). Phragmoplasts very similar to those of first division are constructed between the sister groups of chromosomes (Fig. 11), and microtubules radiating from nonsister groups of chromosomes form secondary interactions leading to additional phragmoplasts (Fig. 11). Fusion of primary and secondary phragmoplasts results in a complex that directs cell plate deposition. Simultaneous cytokinesis results in a tetrahedral tetrad of spores. The positions of the first division equatorial region as well as the newly formed second division equatorial regions are marked by strong fluorescence particularly in the nuclear channel (Fig. 11C). It is not known if this represents especially dense cytoplasm or organellar DNA from a concentration of mitochondria and plastids in this region. Intersporal cell plates that develop in the phragmoplasts fuse to separate the four spores of the tetrad. Cell plates seem to be laid down first in the centers of phragmoplasts and then to expand to the periphery (Fig. 11C). There is no evidence of wall ingrowth or other structural marking of the position where the expanding intersporal walls will join the periphery.
DISCUSSION
The overall pattern of meiosis in Ricciocarpus natans is unusual among bryophytes in that meiosis occurs in unlobed polyplastidic sporocytes and the spindle is organized by NE-MTOCs. The spindles of both first and second meiosis are cylindrical in shape with box-like polar regions. In these respects, meiosis in R. natans closely resembles Conocephalum (Brown and Lemmon, 1988; Shimamura et al., 1998). In these two complex thalloid (marchantiod) liverworts, there is no indication of the premeiotic establishment of quadripolarity that is typical of bryophytes in which it is associated with cytoplasmic lobing in the leafy and simple thalloid liverworts and monoplastidy in mosses and hornworts. The relationships among these organisms are shown in Fig. 12.
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; Shaw and Renzaglia, 2004). Monoplastidic meiosis occurs sporadically in disparate members of marchantioid liverworts (Renzaglia et al., 1994; Shimamura et al., 2003). Significantly, it is characteristic of both monotypic genera, Blasia (Renzaglia et al., 1994) and Cavicularia (Shimamura et al., 2005) of the Blasiales, a group considered to be sister to all other marchantiods in recent cladistic studies (Forrest et al., 2006). Monoplastidic meiosis also occurs in the complex thalloid liverworts Dumortiera and Monoclea, an alliance that is supported by cladistic analysis (Forrest et al., 2006).
Recent investigation of Marchantia polymorpha (Brown et al., 2007) in the crown group Marchantiales, suggests an intermediate stage in the evolution from monoplastidic to polyplastidic meiosis. Plastid MTOCs occur only in early meiotic prophase. After the single plastid divides and migrates, microtubules emanating from MTOCs at the four plastid tips form a quadripolar microtubule system (QMS). Then the -tubulin leaves the plastids and forms diffuse poles in the future spore domains. The plastids, which are no longer MTOCs, continue to proliferate and cluster around the -tubulin poles. In typical monoplastidic meiosis, the four plastids serve as MTOCs throughout meiosis, and each spore inherits a single plastid.
Ricciocarpus natans is very similar to Conocephalum in having polyplastidic sporocytes with anastral spindles that are organized in the perinuclear region with no indication of predivision establishment of quadripolarity such as precocious cytoplasmic lobing or clustering of plastids at future tetrad poles. However, R. natans does routinely produce tetrads of spores in tetrahedral arrangement as a result of precisely oriented spindles. This arrangement is unlike that seen in Conocephalum, which has unusual patterns of tetrads (e.g., predominately linear in C. japonicum and variable in C. conicum). The variable pattern of tetrads in Conocephalum conicum provided strong evidence for a postmeiotic determination of division plane where spore domains are measured by radial microtubule systems emanating from tetrad nuclei (Brown and Lemmon, 1988).
Bryophytes hold clues to the evolution of microtubule organization in plants. The appearance of anastral spindle organization at NE-MTOCs in certain marchantioids is intriguing, both because such spindle organization is not known to occur in other bryophytes and because of its similarity to spindle origin in higher plants. Meiotic prophase in R. natans progresses without any vestige of the quadripolarity that characterizes sporogenesis in the majority of bryophytes. These data emphasize the need for additional comparative studies on meiosis in the marchantiod liverworts, which have multiple patterns of spindle development and may hold clues to the evolution of the anastral spindle.
FOOTNOTES
1 The authors thank Dr. T. Horio for the gift of the G9 antibody (prepared by M. Yamato of Univ. Tokushima), Dr. B. Crandall-Stotler for taxonomic identification, Dr. D. Krayesky for help with phylogeny, and Harold Poole Nursery, Forest Hills, Louisiana for allowing us to collect bryophytes from their greenhouses and growing fields. 
2 Author for correspondence (e-mail: rcb{at}louisiana.edu)
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