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Sporogenesis in bryophytes: patterns and diversity in meiosis.

Polar Organizers in Meiosis of Sphaerocarpos texanus

Whereas POs are the only MTOCs known in liverwort mitosis, their occurrence in meiosis is sporadic. POs are usually associated with meiotic quadripolarity in the Jungermanniopsida where sporocytes are deeply quadrilobed (Fariner, 1895; Brown et al., 1986). In these liverworts and the early divergent marchantiod liverwort Blasia, quadripolarity is initiated by pre-meiotic bands of cortical microtubules that mark the sites of cytoplasmic infurrowing and the eventual cytokinetic planes (Brown & Lemmon, 2006). In prophase, distinct POs develop adjacent to the nuclear envelope in the deeply lobed sporocytes and the nucleus is drawn into a tetrahedron.

Interestingly, one of the most extreme examples of nuclear shaping in marchantioids occurs in association with POs in S. texanus, a species with large, unlobed polyplastidic sporocytes. Sphaerocarpos along with Riella and Geothallus comprise the small order Sphaerocarpales, a distinct and early divergent order. The sporocytes of the Sphaerocarpales are difficult to study by immunofluorescence as they contain abundant lipids and have a resistant wall. Neidhardt (1978) encountered similar difficulties in attempting TEM studies of sporogenesis in the aquatic R. affinis.

In S. texanus, the archesporium differentiates into sporocytes and accompanying nurse cells (Fig. 20a, b). There are no elaters. The small nurse cells are peculiar; they are thought to be nutritive but there is little evidence for this role (Kelley & Doyle, 1975). The nurse cells undergo several rounds of mitosis without cytokinesis (Fig. 20c, d). The sporocytes differentiate into large spherical cells (Fig. 21a-c) with no cytoplasmic evidence of quadripolarity. An extensive RMS (Fig. 21a) emanates from the relatively small nucleus (Fig. 21c). In early prophase I, microtubules (Fig. 21d) emanate from four POs with distinct concentrations of [gamma]-tubulin (Fig. 21e) and the nucleus is drawn into a tetrahedron (Fig. 21f). In spite of this QMS in early prophase, the prometaphase spindle is multipolar in origin (Fig. 21g-i). The [gamma]-tubulin becomes associated with the microtubules that enmesh the nucleus. In this manner transition to the bipolar metaphase I spindle is accomplished. By metaphase I (Fig. 21j-l) the spindle is rod-shaped (Fig. 21j) with [gamma]-tubulin concentrated at the polar regions (Fig. 21k).

As in other marchantioids, microtubules radiate from the telophase nuclei and an interzonal phragmoplast develops (not shown) but no wall is deposited. Meiosis II occurs in the undivided cytoplasm. Microtubules (Fig. 22a) emanating from distinct POs (Fig. 22b) that reform at opposite tips of the fusiform nuclei (Fig. 22c) form extensive astral arrays and outline nuclear envelopes to initiate the prophase II spindles. The second division spindles (Fig. 22d-f) are rod shaped with poles that are more focused than those of first division, [gamma]-Tubulin is distributed along the spindle fibers (Fig. 22e). Following telophase II a phragmoplast complex expands centrifugally and intersporal septae are deposited (Fig. 22g-i). In S. texanus, the spores remain united in permanent tetrads. Extensive RMSs emanate from the spore nuclei and a system of opposing microtubules develops at the spore boundaries (Fig. 22j). It is possible that this system of microtubules is somehow involved in wall deposition resulting in cohesion of the tetrad members.

Polyplastidic Meiosis in Asterella tenella

The crown marchantioid A. tenella also utilizes POs in meiotic spindle construction. Sporocytes are unlobed and polyplastidic. In early prophase, aster-like arrays of microtubules (Fig. 23a) emanate from several [gamma]-tubulin rich sites at the nuclear envelope (Fig. 23b). As prophase progresses the number of poles is typically reduced to four (Fig. 23c) although occasionally additional poles persist (not shown). Microtubules closely invest the nucleus, now tetrahedral in shape, and radiate into the cytoplasm (Fig. 23c). Concentrations of [gamma]-tubulin mark the POs and extend along the nuclear envelope (Fig. 23d). The interaction of opposing microtubules originating from these sites results in four cones of microtubules (Fig. 23e) and the nucleus is drawn out at the POs (Fig. 23f). In development of the metaphase I spindle, the four cones of microtubules migrate in pairs to establish bipolarity with opposite poles at ends of a single division axis (Fig. 24a-f). When the prometaphase spindle (Fig. 24d) is viewed in median optical section (Fig. 24e), the merging pairs of poles are seen to be mutually perpendicular; two poles are side by side and the other two are one behind the other. This accounts for the twisted rectangle spindle shape characteristic of the marchantioids. The prometaphase spindle with the shape of a twisted bowtie develops by fusion of pairs of poles (Fig. 24g-i).

The metaphase I spindle has a narrow equator and flared poles (Fig. 25a, b) and quite often is slightly bent (Fig. 25c, d), perhaps due to early separation of a bivalent on the periphery of the spindle. The anaphase I spindle (Fig. 26a, b) has narrowed poles. Microtubules emanating from the nuclei give rise to a well-developed phragmoplast in the interzone (Fig. 26c). The phragmoplast expands (Fig. 26e) and what appears to be a free-floating disc is deposited in the equatorial region (Fig. 26d, f). TEM would be necessary to determine if the structure shown is a concentration of organelles or actually a partial cell plate resulting from some degree of vesicle fusion. Such free-floating cell plate discs have been documented in meiosis of certain monocots, e.g. daylily (Juel, 1897). The second division prophase spindles (Fig. 26g, h) appear to be multipolar in origin. As the prophase spindles assemble, additional fan-like arrays (Fig. 26g), which may be remnants of the phragmoplast, remain in the equatorial region adjacent to the "cell plate disc" (Fig. 26h).

Second division (Fig. 27a, d) occurs in the undivided cytoplasm. The metaphase II spindles are similar to those of first division and may be similarly bent (Fig. 27a). In telophase II numerous microtubules radiate from the reforming nuclei (Fig. 27c) and form conspicuous primary phragmoplasts (Fig. 27e) between pairs of sister nuclei (Fig. 27f). The primary phragmoplasts expand and secondary phragmoplasts form between non-sister nuclei resulting a phragmoplast complex (Fig. 27g) that accomplishes simultaneous cytokinesis of the spore tetrad (Fig. 27h).

Broad Polar Organizers in Meiosis of Reboulia hemisphaerica

Spindle ontogeny in the crown marchantioid R. hemisphaerica is similar to that described above for S. texanus and A. tenella except that the nuclear quadrilobing is much less pronounced and the POs less discrete. In early prophase (Fig. 28a-c), microtubules radiate from numerous sites around the nuclear envelope where [gamma]-tubulin is concentrated (Fig. 28b). The multiple sites merge into four broad POs (Fig. 28d) tetrahedrally positioned at the surface of the nuclear envelope which itself becomes distended into a tetrahedron (Fig. 28f). Asters disappear as a tetrapolar spindle is assembled; microtubules emanating from the four poles are organized into spindle fibers at the surface of the tetrahedral nucleus (Fig. 28g-i). The metaphase spindle is rectangular (Fig. 28j-1). [gamma]-Tubulin, which was concentrated in the four polar regions during prophase (Fig. 28e), becomes concentrated in the two broad polar regions by metaphase I (Fig. 28k).

Following meiosis I radial microtubules emanate from the two nuclei (Fig. 29a-c) and give rise to a phragmoplast in which forms a free-floating disc. The apparent localization of [gamma]-tubulin in this disc is unaccountable. No such signal was associated with the similar disc in Asterella tenella. Microtubules (Fig. 29d) are organized at [gamma]-tubulin (Fig. 29e) associated with the nuclei (Fig. 29f). The box-like metaphase II spindles are located on either side of the free-floating disc (Fig. 29g-i). Following meiosis II, radial microtubules emanating from the nuclei form primary phragmoplasts between sister nuclei (Fig. 29j, k) and secondary phragmoplasts between nonsister nuclei (Fig. 29I).

Polyplastidic Meiosis and Multipolar Spindle Origin in Ricciocarpos natans

R. natans shows a scheme of polyplastidic meiosis and simultaneous cytokinesis in which there is no evidence of prophasic preparation of spore domains. The assembly of the spindle appears to be associated with the nuclear envelope, a pattern typical of euphyllophytes but rare in bryophytes where it is restricted to other crown marchantioids such as Conocephalum (Brown & Lemmon, 1988c; Shimamura et al., 1998) and apparently Sauteria and Athalamia (Shimamura et al., 2011).

In early meiotic prophase (Fig. 30a-c), microtubules are arranged in a reticulate pattern over the nucleus and throughout the cytoplasm. This array is associated with [gamma]-tubulin adjacent to the nuclear envelope (Fig. 30b).

In prometaphase (Fig. 30d-f), [gamma]-tubulin is concentrated at several foci around the nucleus (Fig. 30e, f) and gives rise to bundles of microtubules that comprise the early multipolar spindle (Fig. 30d). The several poles gradually consolidate into two blunt polar regions. The mature metaphase I spindle (Fig. 30g-i,) has a distinctive cylindrical shape with squared off poles and a broad equatorial region (Fig. 30g). [gamma]-Tubulin is more concentrated in the poles where it forms a distinct cap and extends along the distal kinetochore fibers especially those at the perimeter of the spindle (Fig. 30h).

Figure 31 illustrates a fortuitous alignment of two sporocytes, one in metaphase I and the other in metaphase II. The overall organization of the spindles appears identical. The slightly bent spindle of metaphase I is apparently typical (Fig. 30g-i). [gamma]-Tubulin is concentrated at polar regions in both first and second metaphase spindles (Fig. 31b), an unusual occurrence in plants where [gamma]-tubulin more often is distributed throughout the spindles.

In late anaphase I (Fig. 32a-c) microtubules emanate from [gamma]-tubulin at the poles (Fig. 32b). In telophase I (Fig. 32-f) the [gamma]-tubulin (Fig. 32e) moves to the proximal faces of reforming nuclei (Fig. 32f). Interaction of opposing sets of microtubules in the interzone gradually gives rise to a well-defined phragmoplast (Fig. 32d-i). [gamma]-Tubulin is now present both in the phragmoplast and surrounding the nuclear envelopes (Fig. 32h). There is no evidence of cell plate deposition or wall ingrowths in the equatorial region of first meiosis. In inframeiotic interphase (Fig. 32j-1) [gamma]-tubulin is evenly distributed around the surface of the dyad nuclei where it is associated with the development of RMSs (Fig. 32j) that clearly delimit the dyad domains in the otherwise undivided sporocyte.

Second division spindles develop simultaneously in the undivided cytoplasm (Fig. 33a-c). After chromosomes have moved to the poles of second division (Fig. 33d-f), [gamma]-tubulin once again surrounds the nuclear envelopes and microtubules radiate from the newly formed nuclei (Fig. 33g-i). Phragmoplasts very similar to those of first division are constructed between the sister groups of chromosomes (Fig. 33g) and microtubules radiating from non-sister groups of chromosomes form secondary interactions (Fig. 33g). This results in a phragmoplast complex that directs cell plate deposition to simultaneously cleave the 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 background fluorescence especially in the nuclear channel (Fig. 33i). It is not known if this represents particularly dense cytoplasm or organellar DNA in concentrations of mitochondria and plastids in this region.

Polyplastidic Meiosis and Variable Tetrad Arrangements in Concephalum conicum

Unlike nearly all other bryophytes, there is no evidence of prophasic establishment of division quadripolarity in C. conicum. Instead, the interactions among post meiotic nuclear-based radial microtubule systems establish NCDs determining apportionment of the cytoplasm into spores. Tetrad patterns, determined according to position of post-meiotic nuclei, vary from tetrahedral, rhomboidal, t-shaped and rarely even linear tetrads. In C. japonicum, the only other species in the genus, linear tetrads are typical (Shimamura et al., 1998).

The sporocytes emerge as spherical to elliptical cells (Fig. 34) with a reticulate cytoskeleton and no evidence of quadripolarity (Fig. 35a, b). The spindle appears to develop from bundles of microtubules outside the nuclear envelope and seems to be organized with several poles (Fig. 35c) before gradually converging on a spindle axis. The mature metaphase spindle (Figs. 35e, f and 36a) is generally rectangular.

Following chromosome separation in first meiosis, a well-developed phragmoplast begins as a bipolar array in the interzone (Fig. 36b) and expands (Fig. 36c) to the cell periphery without deposition of a wall. There is no evidence for the existence of an organelle band although this has not been looked for with TEM. At the onset of prophase II, microtubules are organized around the nuclear envelopes and radiate into the undivided cytoplasm (Fig. 36d). The metaphase II spindles are similar to that of metaphase I but smaller (Fig. 36e) and variously oriented in the cytoplasm. The irregular placement of tetrad nuclei results in variation in the arrangement of phragmoplasts. Microtubules radiating from nuclei initiate the development of phragmoplasts (Fig. 36f). Phragmoplasts expand centrifugally and deposit intersporal walls leading to the equal apportionment of cytoplasm to the four spores in variable patterns (Fig. 37a-c). This process of post-meiotic determination of tetrad patterns appears to be a feature found only in C. conicum and, based on presence of variable tetrad arrangements, to be expected in the related Athalamia and Sauteria (Shimamura et al., 2011).

Simple Thalloid and Leafy Liverworts

The simple thalloid and leafy liverwort clade (Jungermanniopsida) is a morphologically diverse and speciose group of organisms. This is the "lobed sporocyte" group of Schuster (1984) minus Monoclea, Blasia, and the Haplomitriopsida. Understanding relationships has been hampered by species diversity, poor fossil record, and lack of information on morphology and development. Molecular phylogeny has done much to refine understanding of relationships in this group (Frey & Stech, 2005; Forrest et al., 2006; Renzaglia et al., 2007; Crandall-Stotler et al., 2009a; b). Phylogenetic studies point to two paraphyletic assemblages. The Metzeriidae I includes most of the genera and is exemplified by taxa that are mostly thalloid but occasionally exhibit nodal anatomies as in the Fossombroniales. While the sister clade is sister includes the "true" leafy liverworts and small group of simple thalloids belonging to the Metzgeriales. In this scheme Pleurozia with decidedly nodal anatomy and classically thought of as a leafy liverwort is shown to be allied to the Metzgeriales. For a formal classification reflecting these relationships see Crandall-Stotler et al. (2009b).

Given the diversity of this group little is known of sporogenesis. We are fortunate to have a sampling of the major lineages. The preliminary findings on sporogenesis suggest that there are variations that may be of taxonomic importance in resolving relationships in this diverse group. Additional studies of key taxa such as Pleurozia are much needed. The studies reviewed here reveal taxa with POs while others show NE-MTOC function in the development of the quadipolar spindle.

In general terms it is in this group that predetermination of division polarity is manifested in the extreme. The establishment of quadripolarity for the two meiotic divisions is so extreme that in some taxa the spore domains are hOt only defined by quadrilobing but also are provisioned with templates for spore wall deposition in prophase I. In all jungermanniopsid liverworts investigated, the expression of quadripolarity is initiated in sporocytes just entering the meiotic pathway by premeiotic bands of microtubules that define the future cytokinetic planes and result in deeply quadrilobed cytoplasm. The cleavage furrows lie at right angles to each other; those at either end of the first division axis are designated the polar cleavage furrows and those at right angles, the equatorial. Surprising differences in the construction of the QMS are seen. In Fossombronia, Aneura, and the closely related Riccardia (Brown & Lemmon, 2011a) the poles have asters emanating from distinct POs. However, in Pallavacinia (Metzeriidae I) the spindle originates from nuclear envelope associated prophase microtubule systems and is more like that of leafy liverworts. Spindles are decidedly quadripolar and may remain so in metaphase I when each pole consists of a pair of poles straddling a polar cleavage furrow. The resultant spindle often has distinctly arched poles.

Meiosis in Fossombronia foveolata

Phylogenetic studies show the Fossombroniales to be an early divergent group. The Fossombroniales are a specialized group of simple thalloids in which the thalli are marginally dissected into leafy appendages that appear ruffled to the naked eye. They are desiccation tolerant and are often pioneers in disturbed areas. Meiosis occurs in large moderately lobed sporocytes containing copious accumulations of oil (Fig. 38). The large size of the sporocytes and numerous oil globules make preparations difficult but the microtubule systems of meiosis can nevertheless be studied adequately, especially in partially lysed cells.

The development of sporocyte quadripolarity is initiated with the appearance of girdling bands of cortical microtubules (Fig. 39a-f). These premeiotic bands mark the future cytokinetic planes along which cleavage of the spore tetrad will occur after meiosis. As the cytoplasm grows it expands into four distinct lobes, each of which is a future spore domain. The exceptionally large size of sporocytes makes it possible to see that the system of premeiotic bands is restricted to the cortical cytoplasm and is well removed from the relatively small spherical nucleus (Fig. 39a-f). [gamma]-Tubulin is distributed throughout the bands (Fig. 39b) and is not associated with the nuclear envelope. The three-dimensional relationship of bands to lobing can be seen in Fig. 40. As the cell enters prophase, microtubules flare from the bands, the [gamma]-tubulin in the bands is dispersed, and the small nucleus, which was acentrically located in earlier stages, is centered in the sporocyte (Fig. 39d-f). The premeiotic bands completely disappear before initiation of the prophase spindle (Fig. 39g-l). Four elongated POs (Fig. 39h) that appear at equidistant points along the nuclear envelope nucleate microtubules of the QMS (Fig. 39g). The nucleus is drawn into four points (Fig. 39i) at the POs. A nucleus and associated cytoskeleton (Fig. 39j-l) that was expressed from the cytoplasm is somewhat distorted but clearly shows the associated POs and four cones of microtubules of the QMS enclosing the nucleus. The POs are more rounded and the nucleus has rounded up suggesting that in the intact sporocyte the entire nuclear-cytoskeletal complex is under tension perhaps connected to other elements of the cytoskeletal or endomembrane systems. The extreme quadripolarity of the prophase spindle can be seen in stereo (Fig. 41). The metaphase spindle (Fig. 42a, b) is surprisingly conventional in appearance with no remaining hints as to its origin from four POs. This may be due to the fact that the sporocyte is only slightly lobed and the polar cleavage furrows do not influence the poles of the fusiform spindle.

Second division occurs simultaneously in the undivided cytoplasm (Fig. 42c, d). Following chromosome separation a phragmoplast system develops (Fig. 42e, f) and simultaneous cleavage results in a tetrad of spores (Fig. 42g, h). Each member of the newly cleaved tetrad of spores develops a nuclear associated RMS (Fig. 42g).

Meiosis in Pallavacinia lyellii

The widespread and conspicuous simple thalloid liverwort Pallavacinia was a favorite subject of the early cytologists who described quadrilobing of the sporocyte and the quadripolar origin of the spindle (e.g. Farmer, 1895, 1904; Davis, 1899; Moore, 1905). We were surprised to find that the spindle is not nucleated at distinct POs as it is in other simple thalloids, e.g. Fossombronia or Aneura, but instead shares similarities with the leafy liverworts to which it is not particularly closely related.

The extremely lobed sporocytes (Figs. 43 and 44a) are exemplary of the Metzgeriinae. The wall infurrows are so deep that they impinge upon the nucleus in the central isthmus and clearly define the future spore domains. Bands of microtubules are associated with the establishment of quadrilobing in sporocytes entering meiosis (Fig. 45a, b). As the premeiotic bands disappear, the nucleus is surrounded by a system of microtubules (Fig. 45c-f). Additional microtubules appear to emanate from the perinuclear region and extend into the cytoplasmic lobes (Fig. 45c) but POs do not appear, nor does the nucleus distend into the lobes. Instead, and most peculiarly, it seems to be drawn to the furrows (Fig. 45f). This is verified in TEM (Figs. 43 and 44a). A QMS develops (Fig. 45e) with poles on either side of cleavage furrows, which can now be identified as the polar furrows, and the nucleus (Fig. 45f) is drawn to the equatorial furrows at right angles to the polar furrows. The metaphase I spindle is a complex quadripolar structure with a pole extending into each of the four future spore domains (Fig. 45g, h). In face view, the poles at one of the polar cleavage furrows are side-by-side and those at the opposite polar furrow are one behind the other (Fig. 45g). Non-kinetochore microtubules in the equatorial region form a basket around the metaphase I chromosomes (Fig. 45h).

The events of inframeiotic interphase and second division (Fig. 45i-1) are typical of bryophyte meiosis. A distinct phragmoplast develops in the interzonal region in telophase I but no cell plate develops and cytokinesis is simultaneous. These features were clearly described in the early study using differential staining and light microscopy by Moore (1905). Numerous microtubules emanate from the four poles in the cytoplasmic lobes. Those impinging on the nuclei (Fig. 45i, j) form the half spindles of prophase II and numerous others radiate into the cytoplasm (Fig. 45i). The exact nature of the polar region is unknown, and is an interesting subject for further study. It is possible that the poles of first meiosis simply migrate, or are pushed by the opposing spindle microtubules, further into the spore domains. The second division spindles are mutually perpendicular (Figs. 44b and 45k) and deliver a nucleus into each tetrahedrally arranged spore domain. Phragmoplasts formed among telophase II nuclei (Fig. 44c, d) direct wall deposition to join precisely with preprophasic infurrows to complete cleavage of the tetrad of spores. As is typical of bryophytes, each young spore develops an RMS (Fig. 46a, b).

Meiosis in Aneura pinguis

Sporogenesis in Aneura was first studied about the time that meiosis in plants was first described in the late 1800s. Farmer (1895) clearly illustrated four asters of microtubules radiating from "centrospheres" in the quadrilobed sporocytes and described an unusual quadripolar spindle in Aneura multifida. The lobes, which are future spore domains, are in tetrahedral arrangement, although they may appear tetragonal due to flattening during processing. A more recent study of sporogenesis in A. pinguis (=Riccardia pinguis) (Horner et al., 1966) provided ultrastructural information on the lobed prophase sporocyte, cytokinesis, and spore wall development but no information on the cytoskeleton or spindle development. A single transmission electron micrograph showing the deeply lobed, polyplastidic, oil filled sporocyte was published by Shimamura et al. (2003).

Cells preparing to enter meiosis initially display bipolarity with opposite POs generating asters of microtubules that sheath the nucleus and radiate into the cytoplasm (Fig. 47a-c). [gamma]-Tubulin is concentrated in the POs (Fig. 47b). This cytoskeletal configuration is depicted in three dimensions in Fig. 48a, b. Very soon, however, bipolarity is lost as the microtubules, rather than forming a spindle, are organized into two intersecting bands around the nucleus (Figs. 47d-1 and 48c, d). POs lose their identity as discrete entities during formation of the girdling bands of microtubules and the [gamma]-tubulin becomes dispersed along the bands (Figs. 47d-i and 48d). The premeiotic bands define the division planes and influence the process of cytoplasmic shaping, both of which function to determine the final arrangement of the spore tetrad. A progression of stages in lobing is portrayed in Fig. 47d-1. The bands of microtubules are approximately perpendicular in the isthmus of the tetrahedrally lobed sporocyte, and in the fully lobed sporocyte, appear to constrict the proximal portions of the lobes. As prophase progresses and the cytoplasm increases in volume, the cytoplasm protrudes through the banals and forms distinct lobes (Fig. 47g-1). This complex cytoskeletal arrangement is depicted in three-dimensional view in Fig. 48c, d. Thus, the irregularly shaped archesporial cell displaying bipolarity is gradually transformed into a distinctive quadripolar sporocyte with four tetrahedral spore domains at the onset of meiotic prophase.

Following definition of the quadripolar sporocyte the girdling bands disappear. Two large broad POs appear adjacent to opposite cleavage furrows (Fig. 49a-f) and are accompanied by astral microtubules (Fig. 49a, d). [gamma]-Tubulin is concentrated in the POs (Fig. 49b, e). This configuration is shown in stereo in Fig. 50a, b. Each PO appears to separate into a pair of POs that migrate into adjacent spore domains to establish the four poles in tetrahedral arrangement. Once the four POs are each centered in a spore domain, astral arrays of microtubules emanating from each interact to form a QMS (Fig. 49g-i) surrounding the nucleus, which by this time is distinctly tetrahedral (Fig. 49i). This configuration is shown in stereo in Fig. 50c, d. The QMS is transformed into the metaphase spindle by convergence of pairs of poles.

The QMS becomes slightly elongate and begins to show signs of the development of the spindle axis (Fig. 49j-1). The POs are not perfectly spherical (Figs. 49k and 50d) and are perhaps distorted by forces acting on the nuclei envelope. The nucleus itself becomes drawn into four lobes that extend into the cytoplasmic lobes (Fig. 491).

Stages in the development of the bipolar metaphase spindle are shown in Fig. 51a-c. The asters in each lobe disappear and the four interacting arrays of the QMS gradually become reorganized to form parallel arrays closely investing the quadrilobed nucleus. The developing meiosis I spindle is oriented with the metaphase plate in the plane of the equatorial cleavage furrows and the poles straddling the mutually perpendicular polar cleavage furrows (Fig. 51d-f). Distinct kinetochore fibers terminate on either side of the polar cleavage furrows (Fig. 51f).

Concavity of the meiosis I spindle poles persists as the kinetochore fibers shorten in anaphase (Fig. 52a, b). The two groups of chromosomes are delivered directly to the polar cleavage furrows and the interphase nuclei are initially reniform (Fig. 52c, d). A phragmoplast develops in the interzonal region and expands to the equatorial cleavage furrows (Fig. 52c). It is unclear as to whether or not a dyad wall is produced. The occasional appearance of dyads (e.g. Fig. 52g, h, k, l) suggests wall deposition, but may be attributable to breakage during processing for microscopy. The only TEM study, that of Horner et al. (1966), is equivocal as to cell plate deposition after first division.

Following a brief inframeiotic interphase, nuclei enter prophase II simultaneously (Fig. 52e-h). Microtubules emanating from distinct POs (Fig. 52h) at opposite tips of the fusiform nuclei form extensive astral arrays in each of the spore domains (Fig. 52e) and outline nuclear envelopes to initiate the prophase II spindles (Fig. 52e-h). The spindles of meiosis II remain sharply focused (Fig. 52i-1) and [gamma]-tubulin extends along the polar portions of the spindle (Fig. 52l).

Following separation of chromosomes, phragmoplasts develop between the telophase II nuclei (Fig. 52m, n). Notice the absence of secondary phragmoplasts in the equatorial region of meiosis I suggesting again that cytokinesis is likely successive. The phragmoplasts mediate deposition of cell plates that join with the existing dyad wall to accomplish separation of the tetrad members (Fig. 52n). As the phragmoplasts complete expansion, radial systems of microtubules are generated from nuclear surfaces (Fig. 52o). Each spore of the tetrad contains an extensive RMS (Fig. 52p).

Leafy Liverworts

Of the approximately 5,000 species of extant liverworts, 80-90 % belong to the Jungermannidae or leafy liverworts. The phylogenetic relationships within this large group remain uncertain. The two species described here both fall within the Leafy Clade II of Forrest et al. (2006). Additional confirmatory evidence can be extracted from the early studies of Farmer (1895). Farmer studied several leafy taxa and reported the deeply lobed sporocytes, distension of the prophase nucleus into four lobes, and the quadripolar nature of the spindle. Although Farmer did not report premeiotic bands, perhaps due to limits of resolution, he did however comment on the lack of observable asters that are so prevalent in the members of the Metzgeriales. Modern studies of two species of leafy liverworts have shown that cytoplasmic quadrilobing of pre-meiotic sporocytes into future spore domains is initiated by girdling bands of microtubules and confirmed the curious lack of asters/POs.

Cephalozia macrostachya and Telaranea longicolis

Details of meiosis in the two species are essentially the same and descriptions are combined. Entry into meiosis is marked by remodeling of the cortical microtubule system and shaping of the cytoplasm. As sporocytes form, the cortical microtubules are reorganized into a branched system of bands (Fig. 53a). [gamma]-Tubulin is present in the developing bands but the signal is faint and is best seen when a band is viewed end-on and the signal reinforced (Fig. 53b). The nucleus is acentric and appears drawn to the cortex at the site of a band (Fig. 53c). The bands become organized and consolidated into a complex tetrahedral system (Fig. 53d, g). A strong [gamma]-tubulin signal is uniform along the mature bands (Fig. 53e,h). Four cytoplasmic lobes protrude through the circular bands (Fig. 53d-i) that mark the future cytokinetic planes along which the sporocyte will be cleaved into a tetrad of spores after meiosis.

Following the establishment of quadripolarity, numerous microtubules diverge from the bands and extend into the enlarging lobes (Fig. 53g). The bands disappear and are replaced by microtubules that arise from [gamma]-tubulin associated with the nuclear envelope (Fig. 54a-f). A microtubule system arising from the NE-MTOC extends into the 4 lobes (Fig. 54g) and is gradually reorganized into a quadripolar spindle.

The meiotic spindle is quadripolar (Fig. 55a-f) with a pole in each of the four cytoplasmic lobes. The metaphase plate of chromosomes occupies the equatorial cleavage furrows at right angles to the polar cleavage furrows, [gamma]-Tubulin is concentrated in the polar regions, although some signal is distributed throughout the spindle (Fig. 55b, e). The three dimensional shape of the metaphase I sporocyte is shown in Fig. 56. Chromosomes move on the quadripolar spindle to the polar cleavage furrows (Fig. 57a, b). The reniform daughter nuclei arch around the cleavage furrows at right angles to each other (Fig. 57c, d). A phragmoplast develops in the interzonal region and is itself concave (Fig. 57c). During a brief inframeiotic interphase, microtubules radiating from the dumbbell-shaped nuclei form extensive arrays in each of the spore domains (Fig. 57e, f). Dyad nuclei enter prophase II simultaneously. The events of second division (Fig. 57g-l) are typical of bryophytes occurring in response to the precocious establishment of quadripolarity. The second division spindles are quite pointed with poles centered in the spore domains (Fig. 57g). Phragmoplasts develop in the interzones between sister nuclei (Fig. 57i, j). The tetrad members have characteristic RMSs centered on the nuclei (Fig. 57k, l).


The mosses (Bryophytina) are the largest group of bryophytes consisting of some 10,000 species in three or four classes. The morphology is distinctive and remarkably uniform throughout this group of highly specialized and successful bryophytes. There is little difficulty in recognizing a moss with the possible exception of Takakia, a recently discovered and characterized taxon with only two known species. Takakiopsida, along with the Sphagnopsida appear sister to all other mosses (Renzaglia et al., 2007).

As in other bryophytes, the dominant stage in the life cycle is the gametophyte. Spores germinate into a filamentous algal like stage, the protonema, with a unique spreading growth pattern. This form of asexual propagation makes it possible for one spore to produce many gametophytes as multiple buds are organized along the protonema and the three-dimensional gametophytes develop. This transition is important in molecular and physiological investigations into plant growth regulation. The protonemal stages exhibit tip growth and an axially oriented system of microtubules, whereas the three dimensional gametophores exhibit growth from an apical cell/meristem and have cells with hooplike cortical arrays and PPBs prior to mitotic cell division (Doonan et al., 1987; Doonan & Duckett, 1988). At maturity the gametophytes typically consist of stem-like structures bearing leaf-like lateral organs.

Gametophytes, which may be either monicous or dioicous, produce gametangia in modified apices. The sporophyte consists of a foot embedded in the gametophyte, seta, and a terminal capsule where spores are produced. It is retained, and remains at least partially dependent, upon the gametophyte. Unlike hornworts and liverworts, the sporophyte grows to maximum height before sporogenesis occurs. The major lines of mosses are distinguished in large part by the morphology of the structures involved with release of spores. Longitudinal slits occur in capsules of Andreaeopsida and Takakiopsida. Sphagnopsida have a diaphragm that ruptures to explosively release the spores. The remainder of the mosses, with the exception of Oedipodium, has peristomes, elaborate structures of the capsule involved in controlled release of the spores.

All mosses so far investigated undergo monoplastidic meiosis. The number of chloroplasts is reduced from several in the differentiating archesporial cells to only a single plastid in each premeiotic sporocyte. A thick wall consisting of a mucopolysaccharide of uncertain composition is laid down by the sporocyte and the cellulosic vegetative cell wall lyses releasing the sporocytes into a common spore chamber. Once isolated, sporocytes depart on a precisely coordinated pathway in which quadripolarity for the eventual quadripartitioning into the tetrad of spores is established very early. In all mosses studied to date including Andreaeas, Sphagnums, Polytrichums, and bryopsids, the division polarity is marked by morphogenetic plastid division and migration so that the resultant four plastids are positioned at future tetrad poles. The plastids serve as MTOCs that nucleate four opposing systems of microtubules early in meiotic prophase. These four cones of microtubules interact to forma QMS. The plus-end interaction of microtubules establishes the future cytokinetic planes, much as do phragmoplasts after nuclear division. Preferential deposition of additional sporocyte wall material in the future cleavage planes contributes to lobing of the cytoplasm and further defines the quadripolarity. These two concurrent processes define the spore domains that will eventually be cleaved into a tetrad of spores. In bryopsid mosses, this results in a definite quadrilobing of the cytoplasm. In Sphagnum, however, the future cleavage furrows are marked by very shallow but precise infurrows and the sporocytes remain spherical. While it is thought that sporocyte wall deposition by sporocytes is a secretory process involving the deposition of wall materials at the interface of opposing microtubules of the QMS, this view must be modified in the case of Sphagnum where the process is brief and occurs only at the periphery.
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Title Annotation:p. 210-248
Author:Brown, Roy C.; Lemmon, Betty E.
Publication:The Botanical Review
Article Type:Report
Geographic Code:1USA
Date:Jun 1, 2013
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