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Pre-meiotic bands and novel meiotic spindle ontogeny in quadrilobed sporocytes of leafy liverworts (Jungermannidae, Bryophyta)

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Abstract

Indirect immunofluorescence and confocal microscopy were used to study the nucleation and organization of microtubules during meiosis in two species of leafy liverworts, Cephalozia macrostachya and Telaranea longifolia. This is the first such study of sporogenesis in the largest group of liverworts important as living representatives of some of the first land plant lineages. These studies show that cytoplasmic quadrilobing of pre-meiotic sporocytes into future spore domains is initiated by girdling bands of γ-tubulin and microtubules similar to those recently described in lobed sporocytes of simple thalloid liverworts. However, spindle ontogeny is not like other liverworts studied and is, in fact, probably unique among bryophytes. Following the establishment of quadrilobing, numerous microtubules diverge from the bands and extend into the enlarging lobes. The bands disappear and are replaced by microtubules that arise from γ-tubulin associated with the nuclear envelope. This microtubule system extends into the four lobes and is gradually reorganized into a quadripolar spindle, each half spindle consisting of a pair of poles straddling opposite cleavage furrows. Chromosomes move on this spindle to the polar cleavage furrows. The reniform daughter nuclei, each curved over a cleavage furrow, immediately enter second meiotic division with spindles now terminating in the lobes. Phragmoplasts that develop in the interzones among the haploid tetrad nuclei guide deposition of cell plates that join with the pre-meiotic furrows resulting in cleavage of the tetrad of spores. These observations document a significant variation in the innovative process of sporogenesis evolved in early land plants.

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Acknowledgements

We thank Dr. Tetsuya Horio (Univ. Tokushima) for the gift of the G9 antibody and Paul Davison (Univ. of North Alabama) for taxonomic identifications.

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The authors declare that they have no conflict of interest.

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Correspondence to Roy C. Brown.

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ESM 1

Comparison of microtubule arrays (green) associated with nuclear changes and chromosome movements (blue) during meiosis in two leafy liverworts. Cephalozia macrostachya Kaal. subsp. australis Schuster is shown in a, c, e, g, i, k and Telaranea longifolia (Howe) Engel and Merr. is shown in b, d, f, h, j, l. The concordance is striking, especially when the unique organization of a quadripolar meiotic spindle at the nuclear envelope is compared to other liverwort groups in which the spindle microtubules are organized at four polar organizers (POs) or plastid MTOCs. Bar = 4 µm. In pre-prophase (a, b) microtubules in close association with the nucleus are organized into four interconnecting bands. These bands predict the planes between which the cytoplasm will protrude during meiosis and the cytokinetic planes along which the undivided sporocyte will be cleaved into four spores after the completion of meiosis. In meiotic prophase (c, d) microtubules disperse from the earlier bands and are associated more uniformly with the nuclear envelope (NE). These NE-based microtubules form a reticulum in the cytoplasm, which becomes lobed along the established cytokinetic planes. The meiotic spindle is quadripolar, with bifurcated poles in adjacent lobes. The sporocyte shown in f is in metaphase I and the sporocyte shown in e appears to have entered anaphase I. The two groups of telophase I chromosomes straddle opposite cleavage furrows (g, h), which are oriented at right angles to each other. Numerous interzonal microtubules are generated between sister nuclei and non-functional phragmoplasts are organized. No cell plates are deposited until after second nuclear division. Metaphase II spindles (i, j) are oblique with poles in lobes of the undivided cytoplasm. Interzonal phragmoplasts are organized between both pairs of telophase nuclei (k, l)and expand (l) to guide deposition of cell plates to complete cytokinesis in the small central portion of undivided cytoplasm (JPG 923 Kb).

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Brown, R.C., Lemmon, B.E. Pre-meiotic bands and novel meiotic spindle ontogeny in quadrilobed sporocytes of leafy liverworts (Jungermannidae, Bryophyta). Protoplasma 237, 41 (2009). https://doi.org/10.1007/s00709-009-0073-4

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