Growth, Differentiation and Sexuality

426 D. Zickler
Fig. 20.5. A–C Synaptonemal complex and recombination
nodules of S. macrospora. A Pachytene synaptonemal complex.
LE indicates maternal and paternal lateral elements,
and CE the central element of the complex. The arrow points
to a late recombination nodule (RN)locatedontheCE.B At
zygotene, the central element (CE) initiates between converging
lateral elements (LE). C The arrow points to an early
recombination nodule. Note the difference in size and density,
compared to the late nodule shown in A.Bar= 100 nm
Transverse filaments span the width of the central
region, and the central element (CE) runs longitudinally
along the SC, equidistant between the LEs
(Fig. 20.5A). This morphology and the distance between
the LEs are remarkably conserved: the two
LEs are held in register about 100 nm apart in all
studied organisms (review in Zickler and Kleckner
1999). Only one LE is formed along the two
sister chromatids, and corresponds to a rod-like
structure along which sister-chromatid loops are
organized and co-oriented (e.g., illustrations in
Pukkila and Lu 1985; Moens and Pearlman 1988;
Lu 1993). LE and CE proteins have been identified
in rat, mouse, Drosophila, C. elegans and
budding yeast. Intriguingly, despite sharing broad
secondary structure, they lack sequence conservation
(review in Page and Hawley 2004). The condensin
complex, required for metaphase axial compaction,
is also required for efficient assembly of
the SC (Yu and Koshland 2003). SC is shed progressively
from the homologues in the transition from
pachytene to diplotene when homologues start to
separate.
Because of the universal conservation of SC
along each pair of homologues, reconstruction of
SC complements is a powerful tool to estimate the
chromosome number and to detect chromosome
aberrations in organisms, such as fungi, with small
chromosomes (e.g., Carmi et al. 1978; Zickler et al.
1984; Leblon et al. 1986; review in Pukkila 1994).
A. Synaptonemal Complex Formation
SCs form progressively between homologues
during zygotene (Fig. 20.5B) and are seen along
their entire lengths during pachytene (Fig. 20.5A).
Despite a general tendency for SC to initiate near
chromosome ends, SC can also initiate interstitially,
excluding a zipper-like mechanism from
the telomeres (examples in Zickler et al. 1992).
SCs form preferentially between homologous
chromosomes but they can also form between
axial elements (AEs) of non-homologous regions
or chromosomes. In heterozygotes for chromosome
inversions, duplications and reciprocal
translocations, SC formation is initially strictly
homologous. At mid-pachytene, homologous SCs
formed in inversion or duplication loops as well
as in the typical translocation crosses can be
gradually eliminated to form straight SCs with
regions of non-homologous synapsis (examples in
Bojko 1990 for inversion loops of N. crassa,andin
Rasmussen et al. 1981 for reciprocal translocations
of C. cinereus). Extensive non-homologous SC
formation is also observed in haploid meioses
and in plant hybrids with chromosomes of different
lengths (review in Zickler and Kleckner
1999). At least two proteins, Hop2p and Mnd1p,
are required for preventing synapsis between
non-homologous chromosomes (Leu et al. 1998;
Chen et al. 2004 and references therein). DNA
replication is not required for SC formation
in C. cinereus: SCs form between unreplicated
homologues in the spo22/msh5 mutant (Pukkila
et al. 1995).
B. Ascomycetes Exhibit Several Peculiarities
in the Synaptonemal Complex Formation
and Morphology
Although evolutionarily conserved with respect
to basic structure, some organisms show clear
substructures in either the CEs or the LEs. LE
substructures are particularly prominent in discomycetes,
which exhibit a characteristic, banded
pattern with species-specific replicate units of
alternating thick and thin bands (von Wettstein
1971; Gillies 1972; Zickler 1973). Interestingly, the
spacing of the bands is constant at about 25 per
micron of LE, and the same periodicity is also