Unique Biological Features of Sciara
The numerous unique biological strategies employed by Sciara revolve around chromosome dynamics as follows:
Chromosome movement on spindles
(a). A monopolar spindle in the first meiotic division of Sciara spermatogenesis (Metz 1925 and 1926, Metz et al. 1926; Kubai 1982). How chromosomes move on this spindle (Abbott et al. 1981) could shed light on chromosome movement on more canonical spindles.
(b). Non-disjunction of the X dyad occurs in the second meiotic division of spermatogenesis (Metz 1925, 1930 and 1934; Schmuck 1934; Abbott and Gerbi 1981), creating a nullo-X product that is eliminated. The resulting sperm have two copies of the X chromosome. After fertilization of the haploid egg, the zygote has three X chromosomes. The genetic locus ("controlling element") responsible for X dyad non-disjunction (the kinetochore fails to form; D. Kubai, personal communication) has been mapped (Crouse 1960b). It may regulate kinetochore function and/or sister chromatid cohesion and further elucidate these processes.
(c). Chromosome elimination of the L and one or two of the X chromosomes occurs during the fifth and seventh embryonic cleavage divisions, respectively (DuBois 1932 and 1933; reviewed by Metz 1938, Gerbi 1986, and Goday and Esteban 2001). One X is eliminated from the soma of female embryos and two X chromosomes from the male soma. Through an unknown mechanism of chromosome imprinting, the eliminated X chromosomes are always of paternal origin; the maternally derived X' chromosome is never eliminated (Metz 1938). The same "controlling element" that was responsible for X dyad non-disjunction in spermatogenesis also regulates X chromosome elimination in the embryo (Crouse 1960a and 1960b). Some results suggest that the elimination may be due to prolonged sister chromatid cohesion, as the arms of the X fail to separate in anaphase (de Saint Phalle and Sullivan 1996).
(d). A cell-cycle control checkpoint ensures that all chromosomes are attached to spindle fibers from both poles (equal and opposite tension) at metaphase before anaphase is allowed to begin. Such a control must be overridden by Sciara for the monopolar spindle of male meiosis I and in male meiosis II when the X dyad does not associate with spindle fibers. Moreover, in early embryogenesis the L or X chromosomes seem unable to progress past this checkpoint and they lag on the metaphase plate before allowing anaphase to begin. How this is accomplished remains enigmatic.
(e). The term chromosome "imprinting" was first coined in Sciara where chromosome ancestry is marked. In the Sciara male meiosis I monopolar spindle, all the maternally-derived chromosomes move to the single pole, and the paternally-derived chromosomes are discarded (Crouse 1960b; Rieffel and Crouse 1966; Crouse et al. 1971). Thus, the chromosomes are marked with regard to their maternal or paternal origin (Chandra and Brown 1975; Chandra and Nanjundiah 1990; Gerbi 2007). Imprinting has since been studied in mammalian genomes, yet understanding it in Sciara still has much to offer the field at large.
Centrioles and centrosomes
(a). A giant centriole of 20-50 singlet microtubules occurs in the Sciara germ line (Phillips 1967), likely arising from canonical nine-membered centrioles.
(b). Intermediate stages leading to parthenogenesis can be studied in Sciara. Although fertilization is the usual case in Sciara, unfertilized embryos of Sciara initiate parthenogenetic development without centrosomes (de Saint Phalle and Sullivan 1998), offering information for centrosome biology.
Determination of germ-line/soma and sex determination
(a). Germ-line limited ("L") chromosomes are in the gametes but not in the soma (reviewed by Gerbi 1986). The function of the L chromosomes is unknown but correlates with determination of germ-line vs. soma.
(b). Through the unique sex determination mechanism, one (in females) or two (in males) X chromosomes are eliminated from the 3X embryo (where the sperm contributed 2 Xs) (reviewed by Metz 1938 and Gerbi 1986). There is no Y chromosome, and the sex of the offspring is determined by the mother (Metz 1931; Metz and Schmuck 1931), perhaps by conditioning the ooplasm. There is an X and X' chromosome; the latter has a long paracentric inversion (Crouse 1977) that inhibits crossing-over between the X and X' (Metz and Schmuck 1929; Crouse 1960a). Mothers that are X'X will have only daughters, whereas mothers that are XX will have only sons (Metz and Schmuck 1929). This unique system is important for the understanding of the evolution of sex determination (Haig 1993).
(a). Little is known about higher order organization of tandemly repeated genes. Currently, such regions of repetitious DNA are usually ignored in genomic analyses. There are about 65 copies of the ribosomal RNA (rRNA) genes in Sciara at the end of the X (and X') chromosome (Gerbi 1971; Gerbi and Crouse 1976), and this tandem array has been subdivided by translocation break points, allowing a study of its higher order organization. Interestingly, the middle block contains the "controlling element" (Crouse et al. 1977; Crouse 1979) inserted within the tandem array of rRNA genes.
(b). Telomeres seem to be absent at the end of the polytene X chromosome containing the rRNA genes that splay out, forming micronucleoli that bleb off and associate with other loci of the genome (Gabrusewycz-Garcia and Kleinfeld 1964; Pardue et al. 1970; Gerbi 1971).
DNA replication and repair
(a). Control of initiation of replication so that an origin fires only once/cell cycle is overridden in developmentally programmed DNA amplification in Sciara salivary gland polytene chromosome "DNA puffs" (Crouse and Keyl 1968; Rasch 1970a, reviewed by Gerbi et al. 1993 and 2002). The Sciara DNA puff II/9A replication origin is now among the best mapped (to the nucleotide level). In addition, the binding site for the origin recognition complex (ORC) has also been mapped for Sciara II/9A (Bielinsky et al. 2001). Sciara DNA puff amplification appears to be under the control of the steroid hormone ecdysone, providing the first example of a role for a hormone receptor in DNA replication.
(b). DNA repair. Sciara is far more resistant to chromosomal damage by X-irradiation than Drosophila (Metz and Boche 1939; Bozeman and Metz 1949; Crouse 1949), suggesting that Sciara may have a remarkable DNA repair system.