Growth, Differentiation and Sexuality

mechanism whereby homologues locate each
other in the nucleus is not yet understood. The
term juxtaposition or pairing is used to refer to the
coming together of the homologous chromosomes,
whereas the term synapsis is used to mean the
intimate juxtaposition that culminates with the
formation of the SC.
A. Mycelial Fungi Offer Unique Opportunities
for the Analysis of Homologous Pairing
First, contrary to most eukaryotes, the two sets of
homologous chromosomes are in separated nuclei
before meiosis starts (Fig. 20.1C). The first contacts
occur after karyogamy, thus after or during S-phase
(e.g., Lu and Raju 1970; Zickler 1977; Raju 1980; Li
et al. 1999). The progression of homologue juxtaposition
can therefore be conveniently described
with respect to two major landmarks: karyogamy
and SC formation.
Second, although premeiotic pairing is often
presumed to simplify the process of meiotic pairing,
in mycelial fungi, homologue juxtaposition
does not involve simple retention of premeiotic
Fig. 20.3. A,B Computer EM reconstruction from a serially
sectionedleptotene nucleus of S. macrospora. A The 14 chromosomes
can be distinguished by their size and centromere
location. No obvious alignment can be seen. B Rotation of
the nucleus allows us to see that homologue pair 1-1 ∗ (red
and pink) is, in fact, completely aligned whereas pair 7-7 ∗
(dark and light violet) is only partially aligned.
Fungal Meiosis 423
pairing plus reinforcement by meiosis-specific processes
(review in Zickler and Kleckner 1999).
Third, the SC axial elements are formed just
after karyogamy, which allows an accurate analysis
of chromosome disposition and movements during
the recognition and juxtaposition processes (see
Holm et al. 1981; Rasmussen et al. 1981; Pukkila and
Lu 1985; Pukkila 1994; Pukkila et al. 1995; Celerin
et al. 2000; Gerecke and Zolan 2000; Merino et al.
2000 for C. cinereus; Zickler 1977; Zickler et al. 1992;
Storlazzi et al. 2003; Tesse et al. 2003 and Fig. 20.3 for
S. macrospora; Gillies 1979; Bojko 1988, 1989, 1990;
Lu 1993 for N. crassa). Moreover, ascus growth and
nuclear volume increase give easy landmarks for
staging.
Fourth, the development of molecular assays
based on FISH and GFP tagging of single loci, combined
with mutant analyses of C. cinereus and S.
macrospora,haveyieldedagreatdealofnewinformation
about meiotic pairing (e.g., Li et al. 1999;
van Heemst et al. 1999; Cummings et al. 2002; Storlazzi
et al. 2003; Tesse et al. 2003).
B. How Does Pairing Occur?
Three-dimensional EM reconstructions of postkaryogamy
and leptotene nuclei of S. macrospora
reveal that homologous chromosomes come
together in three distinct steps (Figs. 20.3 and
20.4). In very early leptotene, they are far apart
and show no evidence of any specific relationship
(Fig. 20.4A). By mid-leptotene, each homologous
pair has moved from its previous configuration
into a spatial domain of the nucleus (Figs. 20.3B
and 20.4B). Then, all homologous pairs progressively
co-align along their entire length at
adistanceof∼400 nm (Figs. 20.3B and 20.4D).
Upon completion of SC formation, homologues are
uniformly 100 nm apart (see Sect. V.). In budding
yeast, homologue recognition and alignment
occurs in the absence of Zip1p, the SC central
component (Fung et al. 2004). Also, in polyploids
the unsynapsed homologues remain mostly in
parallel association with their synapsed partners
(e.g., triploid C. cinereus; Rasmussen et al. 1981).
Recombination is an important determinant
of stable homologue juxtaposition. Absence of
DSBs results in a dramatic reduction in homologous
alignment in budding and fission yeasts, S.
macrospora and C. cinereus (Celerin et al. 2000;
Keeney 2001; Storlazzi et al. 2003). Interestingly,
there is a quantitative correlation between DSB