quency by preferential segregation during cell
divisions including meiosis. However, little is
known about the meiotic transmission of fungal accessory chromosomes. For several fungal
accessory chromosomes, a non-Mendelian
mode of inheritance has been reported, which
appears to be similar to the mode in plants and
animals. We will therefore first describe some
of the well-understood examples of B chromosome transmission in plants and animals,
which may direct our research of accessory
chromosome inheritance in fungi.
B chromosome accumulation mechanisms, also termed
chromosome drive, involve non-Mendelian modes of
transmission and have been described in approximately 60% of the plant species that carry B chromosomes (Jones 2012). Chromosome drive can either
occur at the pre- or post-meiotic stages or during meiosis (Akera et al. 2017; Gregory 2011; Houben 2017;
Mroczek et al. 2006). The B chromosome of rye is a
well-characterized example for a chromosome drive
mechanism
acting
post-meiotically
(BanaeiMoghaddam et al. 2012; Endo et al. 2008; Hasegawa
1934; Houben 2017). Following meiosis the pollen
development involves two mitotic divisions resulting
in tri-cellular pollen. One pollen consists of two sperm
cells and a vegetative nucleus, which does not provide
genetic material to the offspring (Twell 2011). During
the first pollen mitosis, the two sister-chromatids of B
chromosomes show non-disjunction (Hasegawa 1934)
and will in most cases become part of the generative
nucleus. Thereby the resulting sperm cells will contain
two B chromosomes instead of the expected one
(Fig. 2.2a) (Hasegawa 1934; Houben 2017). What are
the underlying mechanisms that lead to the exploitation
of asymmetric cell divisions by B chromosomes? The
different segregation of A versus B chromosomes during mitotic or meiotic cell divisions predicts functional
differences between their centromeres (or the loci that
mediate attachment of the chromosomes to the spindle). Indeed, the centromeres of A and B chromosomes
in rye differ in their repeat composition, with the B
chromosome centromeres including additional classes
of repeats (Banaei-Moghaddam et al. 2012). Here, a
non-disjunction control region (NCR) acting in trans
controls chromosome segregation of the B chromosome, possibly by long noncoding RNAs which affect
centromere organization (Carchilan et al. 2007; Endo
et al. 2008; Houben 2017).
In general, centromeric sequences and the
centromere-associated histone CenH3 were
shown to evolve rapidly (reviewed in (Rosin
and Mellone 2017)), inspiring the centromere
drive hypothesis (Henikoff and Malik 2002;
Kursel and Malik 2018). Accordingly, centromeric DNAs act as selfish genetic elements promoting their own transmission. Originally, this
hypothesis considered this preferential transmission to only occur in asymmetrical female
meiosis. However, every asymmetrical cell division that eventually results in germline cells
should be susceptible to a non-random segregation of chromosomes as seen in the example
of the rye B chromosome. B chromosomes are
often considered selfish genetic elements. Other
selfish genetic elements have also been shown
to increase their relative frequency by killing or
disabling gametes or embryos that lack the selfish element (Hurst and Werren 2001). To date,
no example of such a killing mechanism has
been described for an accessory chromosome.
Yet, it is worth noting that drive of entire chromosomes has been described for the sex chromosomes in several species within the order
Rodentia and Diptera. Here these drives are
indeed caused either by asymmetrical segregation during mitotic or meiotic cell divisions or
by the selective killing of gametes that do not
carry the sex chromosomes (reviewed in (Helleu et al. 2014; Hurst and Werren 2001; Jaenike
2008)).
In fungi, little is known about the meiotic
transmission of accessory chromosomes. Those
few cases for which the inheritance of the accessory chromosomes was analyzed have shown
(i) loss of accessory chromosomes during meiotic and mitotic cell divisions and (ii) nonMendelian segregation with an increase of
chromosome frequencies (Balesdent et al.
2013; Camacho et al. 2011; Chuma et al. 2003;
Coleman et al. 2009; Fouche ´ et al. 2018; Goodwin et al. 2011; Miao et al. 1991; Orbach et al.
1996; Tzeng et al. 1992; Wittenberg et al. 2009).
Loss of accessory chromosomes during meiosis
was observed for many fungal accessory chromosomes and may, in part, explain the
observed presence/absence polymorphism.
Examples are the accessory mini-chromosome
of Magnaporthe oryzae that fails to segregate
during crosses (Orbach et al. 1996) and the
dispensable chromosome of Leptosphaeria
maculans, which is lost in approximately 5%
of the progeny following meiosis (Balesdent
et al. 2013; Leclair et al. 1996). In these cases,
2 Origin, Function, and Transmission of Accessory Chromosomes
37
divisions including meiosis. However, little is
known about the meiotic transmission of fungal accessory chromosomes. For several fungal
accessory chromosomes, a non-Mendelian
mode of inheritance has been reported, which
appears to be similar to the mode in plants and
animals. We will therefore first describe some
of the well-understood examples of B chromosome transmission in plants and animals,
which may direct our research of accessory
chromosome inheritance in fungi.
B chromosome accumulation mechanisms, also termed
chromosome drive, involve non-Mendelian modes of
transmission and have been described in approximately 60% of the plant species that carry B chromosomes (Jones 2012). Chromosome drive can either
occur at the pre- or post-meiotic stages or during meiosis (Akera et al. 2017; Gregory 2011; Houben 2017;
Mroczek et al. 2006). The B chromosome of rye is a
well-characterized example for a chromosome drive
mechanism
acting
post-meiotically
(BanaeiMoghaddam et al. 2012; Endo et al. 2008; Hasegawa
1934; Houben 2017). Following meiosis the pollen
development involves two mitotic divisions resulting
in tri-cellular pollen. One pollen consists of two sperm
cells and a vegetative nucleus, which does not provide
genetic material to the offspring (Twell 2011). During
the first pollen mitosis, the two sister-chromatids of B
chromosomes show non-disjunction (Hasegawa 1934)
and will in most cases become part of the generative
nucleus. Thereby the resulting sperm cells will contain
two B chromosomes instead of the expected one
(Fig. 2.2a) (Hasegawa 1934; Houben 2017). What are
the underlying mechanisms that lead to the exploitation
of asymmetric cell divisions by B chromosomes? The
different segregation of A versus B chromosomes during mitotic or meiotic cell divisions predicts functional
differences between their centromeres (or the loci that
mediate attachment of the chromosomes to the spindle). Indeed, the centromeres of A and B chromosomes
in rye differ in their repeat composition, with the B
chromosome centromeres including additional classes
of repeats (Banaei-Moghaddam et al. 2012). Here, a
non-disjunction control region (NCR) acting in trans
controls chromosome segregation of the B chromosome, possibly by long noncoding RNAs which affect
centromere organization (Carchilan et al. 2007; Endo
et al. 2008; Houben 2017).
In general, centromeric sequences and the
centromere-associated histone CenH3 were
shown to evolve rapidly (reviewed in (Rosin
and Mellone 2017)), inspiring the centromere
drive hypothesis (Henikoff and Malik 2002;
Kursel and Malik 2018). Accordingly, centromeric DNAs act as selfish genetic elements promoting their own transmission. Originally, this
hypothesis considered this preferential transmission to only occur in asymmetrical female
meiosis. However, every asymmetrical cell division that eventually results in germline cells
should be susceptible to a non-random segregation of chromosomes as seen in the example
of the rye B chromosome. B chromosomes are
often considered selfish genetic elements. Other
selfish genetic elements have also been shown
to increase their relative frequency by killing or
disabling gametes or embryos that lack the selfish element (Hurst and Werren 2001). To date,
no example of such a killing mechanism has
been described for an accessory chromosome.
Yet, it is worth noting that drive of entire chromosomes has been described for the sex chromosomes in several species within the order
Rodentia and Diptera. Here these drives are
indeed caused either by asymmetrical segregation during mitotic or meiotic cell divisions or
by the selective killing of gametes that do not
carry the sex chromosomes (reviewed in (Helleu et al. 2014; Hurst and Werren 2001; Jaenike
2008)).
In fungi, little is known about the meiotic
transmission of accessory chromosomes. Those
few cases for which the inheritance of the accessory chromosomes was analyzed have shown
(i) loss of accessory chromosomes during meiotic and mitotic cell divisions and (ii) nonMendelian segregation with an increase of
chromosome frequencies (Balesdent et al.
2013; Camacho et al. 2011; Chuma et al. 2003;
Coleman et al. 2009; Fouche ´ et al. 2018; Goodwin et al. 2011; Miao et al. 1991; Orbach et al.
1996; Tzeng et al. 1992; Wittenberg et al. 2009).
Loss of accessory chromosomes during meiosis
was observed for many fungal accessory chromosomes and may, in part, explain the
observed presence/absence polymorphism.
Examples are the accessory mini-chromosome
of Magnaporthe oryzae that fails to segregate
during crosses (Orbach et al. 1996) and the
dispensable chromosome of Leptosphaeria
maculans, which is lost in approximately 5%
of the progeny following meiosis (Balesdent
et al. 2013; Leclair et al. 1996). In these cases,
2 Origin, Function, and Transmission of Accessory Chromosomes
37