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Organization and Behavior of the Synaptonemal Complex during Achiasmatic

Meiosis of Four Buthid Scorpions

Article  in  Cytogenetic and Genome Research · February 2015

DOI: 10.1159/000375388 · Source: PubMed

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 Original Article
Cytogenet Genome Res
DOI: 10.1159/000375388
Organization and Behavior of the
Synaptonemal Complex during Achiasmatic
Meiosis of Four Buthid Scorpions
Marielle C. Schneider a Viviane F. Mattos b Leonardo S. Carvalho c
Doralice M. Cella b
a
Departamento de Ciências Biológicas, Universidade Federal de São Paulo (UNIFESP), Diadema, b Departamento de
Biologia, Instituto de Biociências, Universidade Estadual Paulista (UNESP), Rio Claro, and c Universidade Federal do
Piauí (UFPI), Floriano, Brasil
Key Words
Chromosomal rearrangements · Holocentric chromosomes ·
Multivalent associations · Rhopalurus · Tityus
Abstract
Testicular cells of 4 buthid scorpions, Rhopalurus agamem-
non (2n = 28), R. rochai (2n = 28), Tityus bahiensis (2n = 6), and
T. fasciolatus (2n = 14), which show different types of chro-
mosomal configurations in meiosis I, were subjected to cel-
lular microspreading in order to (1) obtain knowledge about
the organization and behavior of the synaptonemal com-
plex (SC), and (2) acquire data about the mechanisms re-
sponsible for inter- and intraindividual chromosomal varia-
tion within Buthidae. Ultrastructural analysis of microspread
nuclei revealed SCs with a well-preserved structure until late
substages of prophase I, but did not detect kinetochore
plates and recombination nodules. Pachytene cells of R.
agamemnon, R. rochai and T. bahiensis exhibited single and
unsynapsed axes continuous with totally synapsed SCs, indi-
cating the occurrence of heterozygous chromosomal rear-
rangements. Although chromosome chains were not ob-
served in T. fasciolatus, the presence of gaps and interlocks
points out that this species also carries heterozygous rear-
rangements, involving a small chromosome segment. Espe-
© 2015 S. Karger AG, Basel
1424–8581/15/0000–0000$39.50/0
E-Mail karger@karger.com
www.karger.com/cgr
Accepted: January 7, 2015
by M. Schmid
Published online: February 28, 2015
cially in R. rochai, the cellular microspreading analysis was
useful to clarify the origin of inter- and intraindividual varia-
tion in the number of bivalent-like elements and in the num-
ber of chromosomes involved in multivalent associations. It
was found that more chromosomes were involved in rear-
rangements than previously established through investiga-
tions using light microscopy alone. © 2015 S. Karger AG, Basel
The synaptonemal complex (SC) is a proteinaceous
structure evolutionarily conserved across a variety of
taxa. It is related to specific events of meiosis such as pair-
ing, synapsis, recombination, and chromosome disjunc-
tion [Kleckner, 1996; Hernández-Hernández et al., 2008;
Viera et al., 2009]. The SC forms during prophase I and
possesses a tripartite ultrastructural organization with 2
lateral elements and 1 central element. Chromatin is as-
sociated with the lateral elements by a series of loops
[Zickler and Kleckner, 1999; Page and Hawley, 2004;
Yang and Wang, 2009; Hernández-Hernández et al.,
2012].
In memory of Doralice Maria Cella.
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Universidade Federal de Sao Paulo
Marielle Cristina Schneider
Departamento de Ciências Biológicas, Universidade Federal de São Paulo (UNIFESP)
Av. Prof. Artur Riedel, 275
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Diadema, SP 09972-270 (Brazil)
E-Mail marielle.unifesp @ gmail.com
 The SC begins to form in zygotene and, after complet-
ing its functions, is gradually degraded in diplotene [Zick-
ler and Kleckner, 1999; Bogdanov, 2003]. During lepto-
tene and zygotene the homologous chromosomes initiate
the process of pairing. The axial elements, which are as-
sociated with a pair of sister chromatids, are organized
and progressively connected to the central element by
transverse filaments. In pachytene, the SC is fully formed
and the axial elements are referred to as lateral elements.
During this substage of prophase I, homologous chromo-
somes become totally synapsed and recombination of the
genetic material occurs. In diplotene, the SC is disassem-
bled, but the homologous chromosomes remain connect-
ed at the chiasmata, which, in addition to providing cyto-
logical evidence of crossing over in the previous prophase
I substage, prevent premature and incorrect segregation
of the chromosomes [Suja and Barbero, 2009; Yang and
Wang, 2009].
Although the SC is a prerequisite for genetic recombi-
nation, its presence does not necessarily indicate the oc-
currence of crossing over. In species with achiasmatic
meiosis, the SC may exhibit similar behavior as in organ-
isms that possess chiasmatic meiosis or, instead of being
degraded during diplotene, remain until metaphase I or
anaphase I. This maintenance of the SC until the late stag-
es of meiosis I helps to maintain the connection between
homologous chromosomes, which is necessary for bal-
anced chromosome disjunction. In other organisms with
achiasmatic meiosis, the SC is formed during leptotene
but does not persist until pachytene or, alternatively, it is
entirely absent [John, 1990; Zickler and Kleckner, 1999;
Bogdanov, 2003].
Among dioecious animals, Lepidoptera and Trichop-
tera (Insecta) as well as Scorpiones (Arachnida) so far are
the only groups in which all species cytogenetically ana-
lyzed to date seem to have achiasmatic meiosis in at least
one of the sexes [John, 1990; Schneider et al., 2009a, b].
Many species of scorpions also exhibit a high level of
chromosomal rearrangements arising from reciprocal
translocations or fissions/fusions. These rearrangements,
when present in a heterozygous condition, result in mul-
tiple chromosomal associations during meiosis I, which
can even involve all the chromosomes of the diploid set.
As an additional peculiarity, all species of the family
Buthidae have holocentric chromosomes [Shanahan,
1989a, b; Mattos et al., 2013; Schneider et al., 2014].
The aim of this work was to obtain knowledge about
the organization and behavior of the SC and acquire data
for the interpretation of inter- and intraindividual chro-
mosomal variation within Buthidae. This work provides
2 Cytogenet Genome Res
DOI: 10.1159/000375388
additional evidence regarding the multivalent chromo-
some associations previously observed in buthid scorpi-
ons. Specifically, 4 species of this family with different
types of chromosomal configurations in meiosis I (deter-
mined through analysis of meiotic testicular cells under
light microscopy) were examined: (1) Rhopalurus
agamemnon (C.L. Koch, 1839), 2n = 28, which showed a
complex chain involving all chromosomes of the comple-
ment; (2) Rhopalurus rochai Borelli, 1910, 2n = 28, which
exhibited interindividual variation, i.e. 10 ‘bivalents’ [for
definition, see Mattos et al., 2013] plus 1 chain of 8 chro-
mosomes, or 9 ‘bivalents’ plus 1 chain of 10 chromo-
somes; (3) Tityus bahiensis (Perty, 1833), 2n = 6, which
revealed 1 chain of 6 chromosomes, and (4) Tityus fascio-
latus Pessôa, 1935, 2n = 14, which exhibited 7 bivalent-
like elements [for definition, see Mattos et al., 2013].
Material and Methods
The sample of male adult scorpions from Brazil examined in
this study included 2 specimens of R. agamemnon, from Mateiros,
TO (10°33′S, 46°27′W); 2 specimens of R. rochai, from Guanambi,
BA (14°18′S, 42°44′W); 4 specimens of T. bahiensis, from Ilha
Grande, Parque Nacional de Ilha Grande, Guaíra, PR (24°01′S,
54°10′W); and 4 specimens of T. fasciolatus, from Ituiutaba, MG
(18°58′S, 49°28′W). All specimens were deposited in the Labo-
ratório Especial de Coleções Zoológicas, Instituto Butantan (IBSP,
curator D.M. Barros-Battesti), São Paulo, SP, Brazil. The speci-
mens were dissected in saline solution (128.3 mM NaCl, 16.7 mM
Na2HPO4, 19.9 mM KH2PO4), and the testes were removed and
divided into 2 parts. One part of each testis was used for light mi-
croscopy analyses [Mattos et al., 2013] and the other part was sub-
jected to cellular microspreading to visualize the SCs and associ-
ated structures under transmission electron microscopy (TEM),
according to Loidl and Jones [1986]. The microspread cells were
silver-impregnated following Kodama et al. [1980]. Ultrastructur-
al analyses were carried out with a Philips CM100 TEM operated
at 80 kV, and the images were recorded on 4489 film plates (Ko-
dak).
Results
Ultrastructural analyses of the microspread cells of the
4 buthid species studied in this work revealed SCs with a
typical and well-preserved structure that was maintained
until late substages of prophase I. Kinetochore plate and
recombination nodules were not detected in all examined
cells. In pachytene nuclei of R. agamemnon and R. rochai,
the total length of the SCs was difficult to determine due
to the occurrence of discontinuous or single axes that
connected completely synapsed lateral elements; these
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 A B

C D E

F G H I

Fig. 1. Prophase I microspreading of R. agamemnon (A–C) and R. rochai (D–I) after silver impregnation. A,
B Pachytene nucleus with its respective schematic interpretation showing SCs with unsynapsed axes (fine lines),
gaps (broken line) and multivalent associations (dotted lines) (indicated by arrows). C Postpachytene cells with
multivalent associations involving a variable number of chromosomes. D, E Postpachytene cells with 10 bivalent-
like elements and 1 chain of 8 chromosomes (D), and 8 bivalent-like elements plus 1 chain of 8 and another with
4 chromosomes (E). F–I Details of the chromosome chains with 12 elements and their respective schematic in-
terpretations. Scale bars = 5 μm.

single axes were frequently not preserved by the cellular
microspreading methodology employed. In both Rhopa-
lurus species, 3 or more SCs were continuous with non-
synapsed axes, forming a multivalent association (fig. 1A,
B).
In postpachytene cells of R. agamemnon, the number
of chromosomes in the multivalent association as well as
the number of bivalent-like elements were extremely vari-
able, certainly due to the early dissociation of some chro-
mosomes of the chain (fig. 1C). Postpachtyene nuclei of
R. rochai showed inter- and intraindividual variability in
the chromosomal associations, i.e. one individual exhib-
ited (1) 10 bivalent-like elements plus 1 chain composed
of 8 chromosomes (fig. 1D), and (2) 8 bivalent-like ele-
ments plus 1 chain of 12 chromosomes. Another individ-
ual revealed (1) 9 bivalent-like elements plus 1 chain of 10
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Synaptonemal Complex in Achiasmatic Cytogenet Genome Res 3

Meiosis of Four Buthid Scorpions DOI: 10.1159/000375388
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Fig. 2. Pachytene microspreading of T. ba-
hiensis (A–D) and T. fasciolatus (E, F) after
silver impregnation. A–D Nuclei with their
respective schematic interpretations show-
ing SCs with single filaments (fine lines),
gaps (broken lines), multivalent associa-
tions (dotted lines) (indicated by arrows),
and interlock (gray lines; arrowhead). De-
tails in C and D depict interlocks. E, F Nu-
clei with 7 SCs revealing gap regions (ar-
row) and interlocks (arrowhead). Scale
bars = 5 μm.
chromosomes, (2) 8 bivalent-like elements plus 2 chromo-
some chains, one with 8 and the other with 4 elements
(fig. 1E), and (3) 8 bivalent-like elements plus 1 chromo-
some chain composed of 12 elements. A careful examina-
tion of these postpachytene cells of both individuals
showed that in the multivalent association of 12 chromo-
somes, 1 chain of 8 and another with 4 chromosomes were
joined together (fig.  1F–I). Moreover, a prominent gap
was observed between both lateral elements of a complete-
ly synapsed chromosomal segment of the chain; this seg-
ment seemed to be a typical bivalent without connection
with the chromosome chain (fig. 1F, G).
4 Cytogenet Genome Res
DOI: 10.1159/000375388
A B
C D
E F
TEM investigation of pachytene cells of T. bahiensis
showed 2 short and 2 or 3 long SCs, which generally ex-
hibited some unsynapsed or discontinuous axes. How-
ever, the presence of unsynapsed axes continuous with
fully paired lateral elements indicated that all elements
were part of 1 multivalent association (fig. 2A–D). Addi-
tionally, the entanglement of non-synapsed axes indicat-
ed the occurrence of interlocking between 2 or 3 SCs
(fig. 2C, D). Ultrastructurally, pachytene nuclei of T. fas-
ciolatus revealed total assembly of the lateral elements,
permitting the recognition of 7 SCs. Furthermore, up to
2 SCs exhibited a gap in the interstitial region, and the
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 A B
Fig. 3. Silver-impregnated microspread postpachytene nuclei of T. bahiensis (A) and T. fasciolatus (B, C). A Mul-
tivalent association of 6 chromosomes. B, C Cells with 7 bivalent-like elements. The arrows indicate gaps in a
lateral element of a small (B) and a large-sized (C) SC. Scale bars = 5 μm.
unsynapsed segment of one SC was intertwined with an-
other bivalent, forming an interlock (fig. 2E, F).
Postpachytene cells of the 2 Tityus species showed
well-preserved SCs constituting a multivalent association
composed of 6 chromosomes in T. bahiensis and 7 biva-
lent-like elements in T. fasciolatus (fig.  3). In the latter
species, a discontinuous segment in 1 lateral element of 1
large and/or 1 small SC was observed (fig. 3B, C).
Discussion
Ultrastructural analyses of the SC had previously been
accomplished in only 6 species of scorpions: Bothriurus
araguayae, B. rochensis (Bothriuridae) and Urodacus
manicatus (Urodacidae, sensu Prendini and Wheeler
[2005]) which possess monocentric chromosomes, and
Lychas marmoreus, L. variatus and T. bahiensis (Buthi-
dae) with holocentric chromosomes [Benavente, 1982;
Shanahan and Hayman, 1990; Schneider et al., 2009a, b].
In these works, the SCs were investigated using cellular or
surface microspreading techniques, with the exception of
the study of Benavente [1982], which was carried out us-
ing histological sections. In the scorpions with holocen-
tric chromosomes, including those investigated here, ki-
netochore plates associated with the SCs were not seen
when the cellular or surface microspreading methodolo-
gies were employed and the nuclei were silver-impregnat-
ed or contrasted with phosphotungstic acid [Shanahan
and Hayman, 1990; Schneider et al., 2009a]. Although the
SCs of T. bahiensis were examined using cellular micro-
spreading, surface spreading [Schneider et al., 2009a] and
histological sections [Benavente, 1982], only this latter
Synaptonemal Complex in Achiasmatic
Meiosis of Four Buthid Scorpions
C
technique revealed the presence of an extensive kineto-
chore plate, which covered almost all the chromosome
surface. On the other hand, an electron-dense structure
identified as kinetochore plate was clearly visible in mi-
crospread prophase I cells of scorpions that possessed
monocentric chromosomes [Shanahan and Hayman,
1990; Schneider et al., 2009b]. Thus, we concluded that
the absence of a kinetochore plate in nuclei subjected to
microspreading is common to species with holocentric
chromosomes. Additionally, all these ultrastructural cy-
togenetic studies in Scorpiones showed the absence of re-
combination nodules, corroborating the occurrence of
achiasmatic meiosis in males of this group.
TEM analyses of cellular microspreading of R. aga-
memnon, R. rochai, T. bahiensis, and T. fasciolatus re-
vealed well-formed and well-preserved SCs until the late
substages of prophase I, despite having achiasmatic meio-
sis. Similar results were sporadically recorded for species
of other taxa that possess both holocentric chromosomes
and achiasmatic meiosis, e.g. Lepidoptera, Mantodea and
Trichoptera [Gassner, 1969; Rasmussen, 1977; Rasmus-
sen and Holm, 1979; John, 1990; Marec and Traut, 1993;
Wolf et al., 1997]. In Scorpiones, the maintenance of SCs
in late meiosis I likely provides the connection required
for the correct and balanced segregation of bivalent-like
elements and chromosome chains during meiosis I, such
as suggested by Rasmussen [1977] for Bombyx mori (Lep-
idoptera).
Occasionally, SC formation does not require chromo-
somal homology, and pairing of nonhomologous chro-
mosome segments may occur. This nonhomologous
chromosomal pairing can be facilitated in the absence of
crossing over and achiasmatic meiosis [Rasmussen and
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DOI: 10.1159/000375388
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Holm, 1979] as observed in all scorpions cytogenetically
examined [Shanahan, 1989a, b; Mattos et al., 2013; Schnei-
der et al., 2014]. Thus, we suggest that, while in early
pachytene cells of R. agamemnon, R. rochai and T. ba-
hiensis there are only specific synapses between homolo-
gous chromosome regions, which generally appeared as
short filaments, in late pachytene nuclei, synapsis is inde-
pendent of chromosome homology, allowing for the for-
mation of long SCs involving almost the entire chromo-
some length.
The methodology used here to obtain cellular micro-
spreading may occasionally fail to preserve single or
unsynapsed axes, resulting in gaps between regions of
totally synapsed SCs. SCs with gaps were previously
described for scorpions of the families Bothriuridae,
Buthidae and Urodacidae, all carriers of heterozygous
chromosomal rearrangements [Shanahan and Hayman,
1990; Schneider et al., 2009a, b]. Although multivalent as-
sociations were not observed in prophase I cells of T. fas-
ciolatus, heterozygous rearrangements probably occurred
in the specimens examined because gaps were verified in
up to 2 ‘bivalents’. However, considering that these non-
homologous chromosomal regions were located in the in-
terstitial region of the SC and probably involved a small
chromosome segment, in T. fasciolatus only completely
synapsed bivalents were observed in the sample of post-
pachytene cells investigated.
Interlocks were observed in cellular microspreads of T.
bahiensis and T. fasciolatus; they involved 1 bivalent-like
element or 1 completely synapsed chromosome segment
and unsynapsed axial elements of 1 SC. In certain species,
e.g. Chorthippus jacobsi (grasshopper), Zea mays (maize)
and Sordaria macrospora (fungus), the interlock was ver-
ified during zygotene and early pachytene, and it proba-
bly originated during the pairing of homologous chromo-
somes. In pachytene, most interlocks were resolved since
they were absent or appeared in reduced frequency in this
substage of prophase I [Santos et al., 1993; Wang et al.,
2009; Storlazzi et al., 2010]. Nevertheless, according to
Zickler and Kleckner [1999], a distinctly increased fre-
quency of interlocks has been found during the late sub-
stage of prophase I in individuals that are carriers of het-
erozygous chromosome rearrangements. Therefore, in
the 2 species of Tityus, mainly in T. fasciolatus, the inter-
locks were further evidence of the occurrence of hetero-
zygous chromosomal rearrangements.
In R. rochai, the ultrastructural studies of prophase I
microspreading provided additional information regard-
ing the multivalent associations observed in cells exam-
ined under light microscopy, in which interindividual
6 Cytogenet Genome Res
DOI: 10.1159/000375388
variability in the number of bivalent-like elements and
chromosomes involved in chains has been reported [Mat-
tos et al., 2013]. TEM investigations of prophase I nuclei
were useful for showing both inter- and intraindividual
variability. Based on these results, we concluded that in
all specimens of R. rochai studied here, the total number
of elements involved in heterozygous rearrangements
was 12. Intraindividual differences regarding the number
of chromosomal chains and elements involved in the
multivalent associations in R. rochai (1 chain with 12, 10
or 8 chromosomes; or 2 chains, 1 with 8 and the other
with 4 elements) was probably related to the degree of
homology between the chromosomes. Thus, the chromo-
somes that often formed 1 chain of 8 elements likely had
a greater extension of homology with each other than
those elements that constituted 1 chain of 4 chromo-
somes. The variable number of bivalent-like elements (8,
9 or 10) certainly originated by premature dissociation of
some chromosomes of the chain, which behave as ‘biva-
lents’. This proposition can also be supported by the de-
tection of a prominent ‘gap’ in both lateral elements of
chromosomes involved in the multivalent association.
In conclusion, the analyses of the SCs in buthid scor-
pions were extremely important for demonstrating the
holocentric nature of the chromosomes, understanding
the organization of complex multivalent associations and
clarifying the events responsible for inter- and intraindi-
vidual variability observed in meiosis I.
Acknowledgements
We would like to thank Dr. Douglas Araujo from Universidade
Federal de Mato Grosso do Sul, Campo Grande, for critical reading
of and valuable suggestions for the manuscript. We are also grate-
ful to the Centro de Controle de Zoonoses from Ituiutaba, MG, for
collecting some of the Buthidae specimens, and Antonio T. Ya-
buki, from Centro de Microscopia Eletrônica, Universidade Es-
tadual Paulista, Rio Claro, for technical assistance in the ultrastruc-
tural analyses. This research was supported by the Fundação de
Amparo a Pesquisa do Estado de São Paulo, FAPESP (2010/14226-
2, 2011/21643-1) and Conselho Nacional de Desenvolvimento
Científico e Tecnológico, CNPq (478630/2010-7). This work was
also part of the ‘Programa de Pesquisas em Biodiversidade do
Semiárido – PPBio Semiárido’ (CNPq 558317/2009-0). Collection
permits were granted by Instituto Brasileiro de Meio Ambiente e
dos Recursos Naturais Renováveis (IBAMA) and the Instituto Chi-
co Mendes de Conservação e Biodiversidade (ICMBio) (25471-1;
25472-1; 15157-1).
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