The atspo11-1 mutation rescues atxrcc3 meiotic chromosome
Jean-Yves Bleuyard, Maria E. Gallego and Charles I. White*
CNRS UMR6547, Universite
Blaise Pascal, 24, avenue des Landais, 63177 Aubie
re, France (*author for
correspondence; e-mail firstname.lastname@example.org)
Received 23 July 2004; accepted in revised form 2 September 2004
Key words: Arabidopsis, meiosis, recombination, Spo11, Xrcc3
Homologous recombination events occurring during meiotic prophase I ensure the proper segregation of
homologous chromosomes at the ﬁrst meiotic division. These events are initiated by programmed double-
strand breaks produced by the Spo11 protein and repair of such breaks by homologous recombination
requires a strand exchange activity provided by the Rad51 protein. We have recently reported that the
absence of AtXrcc3, an Arabidopsis Rad51 paralogue, leads to extensive chromosome fragmentation during
meiosis, ﬁrst visible in diplotene of meiotic prophase I. The present study clearly shows that this frag-
mentation results from un- or mis-repaired AtSpo11-1 induced double-strand breaks and is thus due to a
speciﬁc defect in the meiotic recombination process.
Pairing and synapsis of homologous chromo-
somes, as bivalents, are essential to promote
accurate segregation at the ﬁrst meiotic division.
This bivalent formation is dependent on homolo-
gous recombination (HR) events occurring during
meiotic prophase I and/or synaptonemal complex
assemblage (Page and Hawley, 2003; Petronczki
et al., 2003). Meiotic recombination has been
shown to be initiated by DNA double-strand
breaks (DSBs) produced by the Spo11 protein in
many eukaryotes (Bergerat et al., 1997; Keeney
et al., 1997; Dernburg et al., 1998; McKim and
Hayashi-Hagihara, 1998; Baudat et al., 2000;
Romanienko and Camerini-Otero, 2000; Grelon
et al., 2001). The ensuing recombination process
requires a number of proteins, including the
eukaryotic recombinase Rad51 and Dmc1, a mei-
osis speciﬁc Rad51-like protein (Symington, 2002).
In vitro, these two proteins have the ability to
catalyse the strand exchange reaction, which is the
motor of HR (Sung, 1994; Hong et al., 2001).
In vivo, Dmc1 is required to promote meiotic HR
events, while Rad51 is required in almost all HR
events (Masson and West, 2001) and mutations in
either of these two proteins impair fertility (Bishop
et al., 1992; Shinohara et al., 1992; Pittman et al.,
1998; Takanami et al., 1998; Couteau et al., 1999;
Staeva-Vieira et al., 2003; Li et al., 2004).
In addition to Rad51 and Dmc1, the ﬁve par-
alogues of Rad51 (Rad51B, Rad51C, Rad51D,
Xrcc2 and Xrcc3) have been shown to play roles in
mitotic recombination, DNA repair and chromo-
some stability in vertebrate cells (Thompson and
Schild, 2001). As is the case for Rad51, these
proteins are essential for embryonic viability in
vertebrates and this fact has meant that under-
standing of their roles in meiosis is relatively lim-
ited (Tsuzuki et al., 1996; Shu et al., 1999; Deans
et al., 2000; Pittman and Schimenti, 2000).
Homologues of these proteins have been found in
plants (Arabidopsis thaliana) and invertebrates
(Drosophila melanogaster) and shown to play roles
in DNA repair and meiosis (Ghabrial et al., 1998;
Abdu et al., 2003; Bleuyard and White, 2004).
Plant Molecular Biology 56: 217–224, 2004.
Ó 2004 Kluwer Academic Publishers. Printed in the Netherlands.