be conferred by a meiotic transmission advantage (Balesdent et al. 2013; Fouche ´ et al. 2018;
Goodwin et al. 2011; Tzeng et al. 1992; Wittenberg et al. 2009). In Cochliobolus heterostrophus
two-thirds of randomly selected ascospores
contained the accessory chromosome 16,
although only one of the parental strains carried the chromosome (Tzeng et al. 1992). Similarly, in L. maculans 83% of the progeny
received an accessory chromosome that was
unpaired during meiosis (Balesdent et al.
2013). However, the mechanistic basis for
these transmission advantages has not been
described. Transmission rates higher than
50% for unpaired accessory chromosomes
have also been determined for Z. tritici with
frequent observation of meiotically produced
ascospores containing disomic accessory chromosomes (Fouche ´ et al. 2018; Goodwin et al.
2011; Wittenberg et al. 2009). Tetrad analysis,
in which all meiotic products of a single meiosis
were isolated and analyzed, revealed that the Z.
tritici accessory chromosomes are subject to a
meiotic drive mechanism (Habig et al. 2018).
Interestingly, the meiotic drive appears to be
restricted to those chromosomes that are inherited from the female parent (considered to be
the parent that also provides the mitochondria
to the offspring). Inheritance of the accessory
chromosome from the male parent does not
lead to a chromosome drive. Moreover, the
meiotic drive only affected those accessory
chromosomes without a homolog resulting in
transmission of the unpaired chromosomes to
all meiotic products when inherited from the
female. If the chromosomes were inherited
from the male or had a homolog, they showed
Mendelian inheritance. This unique transmission pattern of unpaired accessory chromosomes might be explained by a feedback
mechanism during meiosis that initiates an
additional round of DNA replication for
unpaired accessory chromosomes inherited
from the female parent (Fig. 2.2b). Alternatively, a pre-meiotic DNA replication is followed by a regulated loss of the redundant
copies of paired accessory chromosomes
(Fig. 2.2c). The centromeres of the accessory
and the core chromosomes of Z. tritici do not
show significant differences in size, location,
and sequence characteristics (Schotanus et al.
2015). Therefore, it appears that, in contrast to
the rye B chromosome, the centromeres are not
involved in the chromosome drive in Z. tritici.
Although other mechanisms could be
involved, this particular transmission pattern
may explain some of the observed characteristics of the accessory chromosomes in Z. tritici.
The meiotic drive may cause the observed
lower recombination rate on the accessory
chromosomes (Croll et al. 2015; Stukenbrock
and Dutheil 2017). The lower recombination
rate would in turn account for the accumulation of transposable elements on these chromosomes (Goodwin et al. 2011) and the observed
lower efficacy of selection in removing nonadaptive mutations from the coding sequences
on the accessory chromosomes (Stukenbrock
et al. 2010). Most importantly, their additional
amplification could explain the maintenance of
accessory chromosomes in this fungus despite
their fitness costs (Habig et al. 2017). Z. tritici
therefore represents the first example for fungal
accessory chromosomes that show meiotic
chromosome drive similar to the transmission
pattern of B chromosomes in plants and animals.
Tetrad analyses to decipher the meiotic transmission of
accessory chromosomes have also been performed in
Nectria haematococca MP VI carrying the accessory
chromosome PDA1-CDC (Miao et al. 1991). In contrast
to the meiotic drive observed in Z. tritici, tetrad analysis
of N. haematococca MP VI showed Mendelian segregation of unpaired and paired PDA1-CDC. Interestingly,
when both parental strains contained one PDA1-CDC,
losses were frequent (10–19% of the progeny), but also
progenies disomic for PDA1-CDC were highly abundant (Garmaroodi and Taga 2015). Moreover, when a
strain with four copies of the accessory chromosome
was crossed with a strain lacking PDA1-CDC, only
about 50% of the progeny inherited the accessory chromosome (Garmaroodi and Taga 2015). Therefore, even
when several copies of an accessory chromosome are
present in the zygote, their transmission varies between
cases where all copies are inherited from one parent
and cases where each parent contributed one copy of
the accessory chromosome.
In conclusion, meiotic instability and nonMendelian inheritance appear to be common
among accessory chromosomes in fungi. Losses
and disomies are frequent, and for Z. tritici
2 Origin, Function, and Transmission of Accessory Chromosomes
39
Goodwin et al. 2011; Tzeng et al. 1992; Wittenberg et al. 2009). In Cochliobolus heterostrophus
two-thirds of randomly selected ascospores
contained the accessory chromosome 16,
although only one of the parental strains carried the chromosome (Tzeng et al. 1992). Similarly, in L. maculans 83% of the progeny
received an accessory chromosome that was
unpaired during meiosis (Balesdent et al.
2013). However, the mechanistic basis for
these transmission advantages has not been
described. Transmission rates higher than
50% for unpaired accessory chromosomes
have also been determined for Z. tritici with
frequent observation of meiotically produced
ascospores containing disomic accessory chromosomes (Fouche ´ et al. 2018; Goodwin et al.
2011; Wittenberg et al. 2009). Tetrad analysis,
in which all meiotic products of a single meiosis
were isolated and analyzed, revealed that the Z.
tritici accessory chromosomes are subject to a
meiotic drive mechanism (Habig et al. 2018).
Interestingly, the meiotic drive appears to be
restricted to those chromosomes that are inherited from the female parent (considered to be
the parent that also provides the mitochondria
to the offspring). Inheritance of the accessory
chromosome from the male parent does not
lead to a chromosome drive. Moreover, the
meiotic drive only affected those accessory
chromosomes without a homolog resulting in
transmission of the unpaired chromosomes to
all meiotic products when inherited from the
female. If the chromosomes were inherited
from the male or had a homolog, they showed
Mendelian inheritance. This unique transmission pattern of unpaired accessory chromosomes might be explained by a feedback
mechanism during meiosis that initiates an
additional round of DNA replication for
unpaired accessory chromosomes inherited
from the female parent (Fig. 2.2b). Alternatively, a pre-meiotic DNA replication is followed by a regulated loss of the redundant
copies of paired accessory chromosomes
(Fig. 2.2c). The centromeres of the accessory
and the core chromosomes of Z. tritici do not
show significant differences in size, location,
and sequence characteristics (Schotanus et al.
2015). Therefore, it appears that, in contrast to
the rye B chromosome, the centromeres are not
involved in the chromosome drive in Z. tritici.
Although other mechanisms could be
involved, this particular transmission pattern
may explain some of the observed characteristics of the accessory chromosomes in Z. tritici.
The meiotic drive may cause the observed
lower recombination rate on the accessory
chromosomes (Croll et al. 2015; Stukenbrock
and Dutheil 2017). The lower recombination
rate would in turn account for the accumulation of transposable elements on these chromosomes (Goodwin et al. 2011) and the observed
lower efficacy of selection in removing nonadaptive mutations from the coding sequences
on the accessory chromosomes (Stukenbrock
et al. 2010). Most importantly, their additional
amplification could explain the maintenance of
accessory chromosomes in this fungus despite
their fitness costs (Habig et al. 2017). Z. tritici
therefore represents the first example for fungal
accessory chromosomes that show meiotic
chromosome drive similar to the transmission
pattern of B chromosomes in plants and animals.
Tetrad analyses to decipher the meiotic transmission of
accessory chromosomes have also been performed in
Nectria haematococca MP VI carrying the accessory
chromosome PDA1-CDC (Miao et al. 1991). In contrast
to the meiotic drive observed in Z. tritici, tetrad analysis
of N. haematococca MP VI showed Mendelian segregation of unpaired and paired PDA1-CDC. Interestingly,
when both parental strains contained one PDA1-CDC,
losses were frequent (10–19% of the progeny), but also
progenies disomic for PDA1-CDC were highly abundant (Garmaroodi and Taga 2015). Moreover, when a
strain with four copies of the accessory chromosome
was crossed with a strain lacking PDA1-CDC, only
about 50% of the progeny inherited the accessory chromosome (Garmaroodi and Taga 2015). Therefore, even
when several copies of an accessory chromosome are
present in the zygote, their transmission varies between
cases where all copies are inherited from one parent
and cases where each parent contributed one copy of
the accessory chromosome.
In conclusion, meiotic instability and nonMendelian inheritance appear to be common
among accessory chromosomes in fungi. Losses
and disomies are frequent, and for Z. tritici
2 Origin, Function, and Transmission of Accessory Chromosomes
39