Chromosome pairing and chiasma formation in spermatocytes and oocytes of Dendrocoelum lactem (Turbellaria, Tricladida); a cytogenetical and ultrastructural study

Abstract

The hermaphroditic flatworm Dendrocoelum lacteum shows a very pronounced sex difference in chiasma frequency; oocytes have 66 per cent more chiasmata than spermatocytes. The ultrastructural basis of this difference was investigated by three-dimensional reconstruction of synaptonemal complexes from ten oocytes and ten spermatocytes at pachytene and smaller numbers of zygotene nuclei. Oocyte nuclei at pachytene are larger and have longer synaptonemal complexes than the equivalent spermatocyte stage. The difference in synaptonemal complex length (60 per cent) corresponds very closely to the difference in chiasma frequency shown by oocytes and spermatocytes and suggests that synaptonemal complex (SC) length may contribute to the regulation of chiasma frequency. Recombination nodules were observed in both spermatocytes and oocytes but their quantitation was unreliable because they are small and differentiation from the unusually dense and prominent central region is difficult. Analysis of the few zygotene nuclei available shows that pairing is predominantly proterminal in both spermatocytes and oocytes, but oocytes may have several additional interstitial initiations. These extra initiations are likely to be necessary for efficient pairing of the longer oocyte chromosomes.

Evidence of a joint control of chiasma formation in spermatocytes and oocytes of a grasshopper

“…Therefore the apparent completely separate genetic control of the first meiotic division in the two sexes may be a consequence of the types of mutant screens that have been employed. In summary, evidences indicating that chiasma formation in male and female meiocytes is governed and regulated by a single controlling system of genes come from species as different as Dendrocoelum lacteum where females have 66 per cent more chiasmata than males (Jones and Croft, 1989), rye in which both sexes present similar chiasma frequencies and E. plorans (this paper) where males display the higher recombination frequencies. However, simultaneous occurrence of a general controlling system involved in the cellular control of recombination in both sexes and some sex-specific genes regulating particular features of meiotic process in male and female meiocytes cannot absolutely be discarded.…”

“…Differences in chiasma frequency between sexes seem to be a widespread phenomenon in animals since they have been observed in species from different taxonomic groups such as planarians (Pastor and Callan, 1952;Jones and Croft, 1989), grasshoppers (Cano and Santos, 1990 and referen-ces therein), urodele amphibians (Callan and Perry, 1977), marsupials (Bennett eta!., 1986; Hayman et a!., 1988) and eutherian mammals (Dunn and Bennett, 1967; Andersson and Sandberg, 1984).…”

Sex-dependent synaptic behaviour in triploid turbot, Scophthalmus maximus (Pisces, Scophthalmidae)

“…For instance, the basidiomycete Coprinus cinereus (Rasmussen et al, 1981), solanaceous plants (Sherma et al, 1989), domestic fowl (Solar et al, 1991), Lolium multiflorum (Thomas and Thomas, 1994), Saccharomyces cerevisiae (Loidl, 1995) and Nile Tilapia (Carrasco, 1998), although only Coprinus, fowl, yeast and turbot showed triple synapsis extended to the whole chromosome complement. The effect of sex on parameters such as SC length (Wallace and Hultén, 1985), chiasma frequency (Jones and Croft, 1989;Cano and Santos, 1990) and the triggering of the metaphase I checkpoint (Roeder and Bailis, 2000) is well known. Therefore, the sex differences observed in triploid turbot regarding the synaptic behaviour, ie, frequency of trivalents, amount of triple synapsis and behaviour of univalents, may not be surprising.…”

The relationship between synapsis and recombination: two different views

“…(v) Evidence that the mean SC length at pachytene and the mean chiasma frequency at diplotene-metaphase I (or mean crossover frequencies) are correlated. These indications emerge from analyses of differences in SC length and chiasma or crossover frequencies between sexes (male vs. female), among individuals of the same sex (Jones & Croft, 1989;Quevedo et al, 1997), or from analysing the effects of additional heterochromatin in meiocytes (Mogensen, 1977). In all cases, higher chiasma/crossover frequencies are associated with longer SCs.…”