mitosis in plants and animals were described for
Aegilops speltoides and grasshoppers in which
the number of accessory chromosome differs
between organs of the organism (Mendelson
and Zohary 1972; Remis and Vilardi 2004).
In fungi, the differentiation between
somatic cells and germline cannot be defined.
Therefore, any differences in transmission of
accessory chromosomes affect their overall
propagation. Indeed, asexual fungi rely solely
on mitotic transmission. Accessory chromosomes in several fungi can be lost during
mitotic transmission. In Fusarium oxysporum
f. sp. lycopersici, the two smallest lineagespecific chromosomes (chr. 1, chr. 14) are lost
at a frequency of 1 in 35,000 spores. Interestingly, the core chromosome 12 could also be
lost but at a much lower frequency than the
accessory chromosomes (Vlaardingerbroek
et al. 2016a). Similarly, in Alternaria alternata
loss of the conditionally dispensable chromosome occurred spontaneously in vitro (Johnson
et al. 2001) and rendered the strain nonpathogenic. In Zymoseptoria tritici and its
closely related sister species Zymoseptoria ardabiliae, spontaneous loss of accessory chromosomes was observed at a very high frequency of
up to 1 in 50 spores (Mo ¨ller et al. 2018). Surprisingly, temperature had a dramatic effect on
the loss rate of accessory chromosomes in Z.
tritici. A rise in temperature from 18
C to 28
C
increased the losses of accessory chromosomes
to 1 in 2 spores (Mo ¨ller et al. 2018). Importantly, during mitotic growth in planta, which
results in the production of asexual pycnidiospores, losses of accessory chromosomes were
also observed at a similar rate to those in vitro
at 18
C (Mo ¨ller et al. 2018). This demonstrates
that accessory chromosome losses occur
throughout the asexual part of the life cycle of
Z. tritici. Interestingly, accessory chromosome
18, which was frequently lost during in planta
experiments, is also often absent in field isolates of Z. tritici (Croll et al. 2013; McDonald
et al. 2016). Hence, the presence/absence polymorphism for the accessory chromosomes
appears to be—at least partially—generated
by frequent losses during mitotic divisions.
Interestingly, in addition to frequent chromosome losses, the same study reported frequent
chromosome fusions, chromosome breakages,
and accessory chromosome duplications at elevated temperatures (Mo ¨ller et al. 2018). Chromosomal fusions involved core as well as
accessory chromosomes. This further highlights the putative plasticity of the Z. tritici
genome and the potential for bidirectional
sequence exchange between core and accessory
chromosomes.
Why do the accessory chromosomes show a
different transmission during mitosis? Interestingly, the accessory chromosomes in Z. tritici,
F. oxysporum, Fusarium asiaticum, and Gibberella fujikuroi are enriched in the histone modification H3K27me3 (Galazka and Freitag 2014;
Schotanus et al. 2015; Fokkens et al. 2018). On
core chromosomes this modification is
restricted to subtelomeric regions and involved
in the localization of these subtelomeric regions
to the nuclear envelope (Erlendson et al. 2017;
Harr et al. 2015, 2016). Therefore, entire accessory chromosomes might be localized at the
nuclear envelope. This different localization
would also be supported by the fact that in Z.
tritici centromeres do not co-localize in one
focus, as observed in many fungi, plants, and
animals (Dong and Jiang 1998; Ross et al. 2013;
Smith et al. 2012) but to several distinct foci in
the nucleus (Schotanus et al. 2015). We hypothesize that the different epigenetic marks on the
accessory chromosomes affect their location in
the nucleus and thereby influencing their DNA
replication and transmission. Recently, we
could show that removal of the H3K27me3 histone modification leads to an increased transmission fidelity of the accessory chromosomes,
supporting the pivotal role for histone modifications in distinguishing core and accessory
chromosomes (Mo ¨ller et al. 2019) (Habig
et al., in preparation).
VI. Accessory Chromosomes Are
Frequently Transmitted in a NonMendelian Way During Meiosis
By definition, accessory chromosomes are present in some but not all members of a population. During sexual mating this presence/
2 Origin, Function, and Transmission of Accessory Chromosomes
35
Aegilops speltoides and grasshoppers in which
the number of accessory chromosome differs
between organs of the organism (Mendelson
and Zohary 1972; Remis and Vilardi 2004).
In fungi, the differentiation between
somatic cells and germline cannot be defined.
Therefore, any differences in transmission of
accessory chromosomes affect their overall
propagation. Indeed, asexual fungi rely solely
on mitotic transmission. Accessory chromosomes in several fungi can be lost during
mitotic transmission. In Fusarium oxysporum
f. sp. lycopersici, the two smallest lineagespecific chromosomes (chr. 1, chr. 14) are lost
at a frequency of 1 in 35,000 spores. Interestingly, the core chromosome 12 could also be
lost but at a much lower frequency than the
accessory chromosomes (Vlaardingerbroek
et al. 2016a). Similarly, in Alternaria alternata
loss of the conditionally dispensable chromosome occurred spontaneously in vitro (Johnson
et al. 2001) and rendered the strain nonpathogenic. In Zymoseptoria tritici and its
closely related sister species Zymoseptoria ardabiliae, spontaneous loss of accessory chromosomes was observed at a very high frequency of
up to 1 in 50 spores (Mo ¨ller et al. 2018). Surprisingly, temperature had a dramatic effect on
the loss rate of accessory chromosomes in Z.
tritici. A rise in temperature from 18
C to 28
C
increased the losses of accessory chromosomes
to 1 in 2 spores (Mo ¨ller et al. 2018). Importantly, during mitotic growth in planta, which
results in the production of asexual pycnidiospores, losses of accessory chromosomes were
also observed at a similar rate to those in vitro
at 18
C (Mo ¨ller et al. 2018). This demonstrates
that accessory chromosome losses occur
throughout the asexual part of the life cycle of
Z. tritici. Interestingly, accessory chromosome
18, which was frequently lost during in planta
experiments, is also often absent in field isolates of Z. tritici (Croll et al. 2013; McDonald
et al. 2016). Hence, the presence/absence polymorphism for the accessory chromosomes
appears to be—at least partially—generated
by frequent losses during mitotic divisions.
Interestingly, in addition to frequent chromosome losses, the same study reported frequent
chromosome fusions, chromosome breakages,
and accessory chromosome duplications at elevated temperatures (Mo ¨ller et al. 2018). Chromosomal fusions involved core as well as
accessory chromosomes. This further highlights the putative plasticity of the Z. tritici
genome and the potential for bidirectional
sequence exchange between core and accessory
chromosomes.
Why do the accessory chromosomes show a
different transmission during mitosis? Interestingly, the accessory chromosomes in Z. tritici,
F. oxysporum, Fusarium asiaticum, and Gibberella fujikuroi are enriched in the histone modification H3K27me3 (Galazka and Freitag 2014;
Schotanus et al. 2015; Fokkens et al. 2018). On
core chromosomes this modification is
restricted to subtelomeric regions and involved
in the localization of these subtelomeric regions
to the nuclear envelope (Erlendson et al. 2017;
Harr et al. 2015, 2016). Therefore, entire accessory chromosomes might be localized at the
nuclear envelope. This different localization
would also be supported by the fact that in Z.
tritici centromeres do not co-localize in one
focus, as observed in many fungi, plants, and
animals (Dong and Jiang 1998; Ross et al. 2013;
Smith et al. 2012) but to several distinct foci in
the nucleus (Schotanus et al. 2015). We hypothesize that the different epigenetic marks on the
accessory chromosomes affect their location in
the nucleus and thereby influencing their DNA
replication and transmission. Recently, we
could show that removal of the H3K27me3 histone modification leads to an increased transmission fidelity of the accessory chromosomes,
supporting the pivotal role for histone modifications in distinguishing core and accessory
chromosomes (Mo ¨ller et al. 2019) (Habig
et al., in preparation).
VI. Accessory Chromosomes Are
Frequently Transmitted in a NonMendelian Way During Meiosis
By definition, accessory chromosomes are present in some but not all members of a population. During sexual mating this presence/
2 Origin, Function, and Transmission of Accessory Chromosomes
35