Abstract
Organization and rearrangements of microtubular cytoskeleton (MTs) during microsporogenesis are determined in ‘historical’ potato genotypes producing 2n pollen following different meiotic nuclear restitution mechanisms (‘parallel spindles’, ‘fused spindles’, ‘premature cytokinesis’). The scope of the investigation is to assess the abnormalities in MT cytoskeleton and their relationships to 2n pollen formation. The genotypes of Solanum used for MT immunofluorescence in this study are diploid interspecific hybrids (2n=2x=24) coming from Wisconsin (USA)and Wageningen (NL) Universities. Based on MT analysis, a reinterpretation of the restitution mechanisms following spindle abnormalities was performed in this study. The fusion of the nuclei at prophase II occurs through the perinuclear MTs in the genotype with ‘fused spindles’. In genotypes with misoriented spindles, the ‘non-spindle’ cytoskeletal arrays,occurring at telophase II, are clue in determining the meiotic products such as dyads and triads. A particular MT array could be crucially involved in meiotic nuclear restitutions both at telophase I and II: the interzonal MTs. It is discussed which is the relationship between this array and the spindle orientation at meta-anaphase II. It is hypothesized that the fusion of non-sister nuclei at each pole depends on the lack of secondary interzonal MTs and on the short distance between nuclei. In the genotype with premature cytokinesis, effectively, a premature phragmoplast occurs at the end of meiosis I. Furthermore, two genotypes are desynaptic with a high degree of male fertility restored by the nuclear restitutions. However, no clear relationship was found between univalents and restitution mechanisms.
Similar content being viewed by others
References
Amon, A., 1999. The spindle checkpoint. Curr Opin Genet Dev 9: 69–75.
Bhatt, A.M., C. Canales & H.G. Dickinson, 2001. Plant meiosis: the means to 1N. Trends Plant Sci 6: 114–121.
Bogre, L., O. Calderini, I. Merskiene & P. Binarova, 2000. Regulation of cell division and the cytoskeleton by mitogen-activated protein kinases in higher plants. In: H. Hirt (Ed.), MAP Kinases in Plant Signal Transduction, pp. 95–117. Springer-Verlag, Berlin Heidelberg.
Brown, R.C. & B.E. Lemmon, 1988. Microtubules associated with simultaneous cytokinesis of coenocytic microsporocytes. Am J Bot 75: 1848–1856.
Brown, R.C. & B.E. Lemmon, 1991. The cytokinetic apparatus in meiosis: control of division plane in the absence of a preprophase band of microtubules. In: C.W. Lloyd (Ed.), The Cytoskeletal Basis of Plant Growth and Form, pp. 259–273. Academic Press Limited, London.
Brown, R.C. & B.E. Lemmon, 1996. Nuclear cytoplasmic domains, microtubules and organelles in microsporocytes of the slipper orchid Cypripedium californicum A. Gray dividing by simultaneous cytokinesis. Sex Plant Reprod 9: 145–152.
Dawe, R.K., 1998. Meiotic chromosome organization and segregation in plants. Annu Rev Plant Physiol Plant Mol Biol 49: 371–395.
Field, C., R. Li & K. Oegema, 1999. Cytokinesis in eukaryotes: a mechanistic comparison. Curr Opin Cell Biol 11: 68–80.
Genualdo, G., A. Errico, A. Tiezzi, & C. Conicella, 1998. α-tubulin and F-actin distribution during microsporogenesis in a 2n pollen producer of Solanum. Genome 41: 636–641.
Heslop-Harrison, J., 1971. Wall pattern formation in angiosperm microsporogenesis. Symp Soc Exp Biol 25: 277–300.
Hogan, C.J., 1987. Microtubule patterns during meiosis in two higher plant species. Protoplasma 138: 126–136.
Jongedijk, E. & M.S. Ramanna, 1989. Synaptic mutants in potato, Solanum tuberosum L. II. Concurrent reduction of chiasma frequencies in male and female meiosis of ds-1 (desynapsis) mutants. Genome 32: 1054–1062.
Mok, D.W.S. & S.J. Peloquin, 1975a. Three mechanisms of 2n pollen formation in diploid potatoes. Can J Genet Cytol 17: 217–225.
Mok, D.W.S. & S.J. Peloquin, 1975b. The inheritance of three mechanisms of diplandroid (2n pollen) formation in diploid potatoes. Heredity 35: 295–302.
Otegui, M. & L.A. Staehelin, 2000. Cytokinesis in flowering plants: more than one way to divide a cell. Curr Opin Pl Biol 3: 493–502.
Quinn, A.A., D.W.S. Mok & S.J. Peloquin, 1974. Distribution and significance of diplandroids among the diploid Solanums. Am Potato J 51: 16–21.
Ramanna, M.S., 1974. The origin of unreduced microspores due to aberrant cytokinesis in the meiocytes of potato and its genetic significance. Euphytica 23: 20–30.
Ramanna, M.S., 1979. A re-examination of the mechanisms of 2n gamete formation in potato and its implications for breeding. Euphytica 28: 537–561.
Ramanna, M.S., 1983. First division restitution gametes through fertile desynaptic mutants of potato. Euphytica 32: 337–350.
Rieder, C.L., A. Khodjakov, L.V. Paliulis, T.M. Fortier, R.W. Cole & G. Sluder, 1997. Mitosis in vertebrate somatic cells with two spindles: implications for the metaphase/anaphase transition checkpoint and cleavage. Proc Natl Acad Sci 94: 5107–5112.
Savoian, M.S., W.C. Earnshaw, A. Khodjakov & C.L. Rieder, 1999. Cleavage furrows formed between centrosomes lacking an intervening spindle and chromosomes contain microtubule bundles, INCEP, and CHO1 but not CENP-E. Mol Biol Cell 10: 297–311.
Schmit, A.C., M.C. Endle & A.M. Lambert, 1996. The perinuclear microtubule-organizing center and the synaptonemal complex of higher plants share a common antigen: its putative transfer and role in meiotic chromosomal ordering. Chromosoma 104: 405–413.
Tavoletti, S., P. Pesaresi, G. Barcaccia, E. Albertini & F. Veronesi, 2000. Map** the jp (jumbo pollen) gene and QTLs involved in multinucleate microspore formation in diploid alfalfa. Theor Appl Genet 101: 372–378.
Veilleux, R.E., N.A. McHale & F.I. Lauer, 1982. 2n gametes in diploid Solanum: frequency and types of spindle abnormalities. Can J Genet Cytol 24: 301–314.
Wada, B. & F. Kusunoki, 1964. Spindle membrane in meiosis of pollen mother cells of Tradescantia and mitosis in endosperm cells of Zephyranthes. Cytologia (Tokyo) 29: 109–117.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Conicella, C., Capo, A., Cammareri, M. et al. Elucidation of meiotic nuclear restitution mechanisms in potato through analysis of microtubular cytoskeleton. Euphytica 133, 107–115 (2003). https://doi.org/10.1023/A:1025636321757
Issue Date:
DOI: https://doi.org/10.1023/A:1025636321757