high similarity in sequence composition
between core and accessory chromosomes suggests an origin within the same genome, while
in other species significant differences in
sequence composition may indicate horizontal
transfer (Akagi et al. 2009a; Ma et al. 2010).
Phylogenetic analyses of fungal plant pathogens, for example, indicate that the accessory
chromosomes of Fusarium oxysporum f. sp.
lycopersici causing Fusarium wilt of tomato
have a different origin than the core chromosome (Ma et al. 2010). Similarly, the accessory
chromosomes in asexual Alternaria alternata
strains appear to have been horizontally transferred between lineages (Akagi et al. 2009a).
The presence of mechanisms that allow horizontal transfer of entire chromosomes between
distinct lineages has furthermore been experimentally demonstrated (Akagi et al. 2009a, b;
He et al. 1998; Ma et al. 2010; Masel 1996). It is
therefore possible that mechanisms of both
models are involved in the origin of new accessory chromosomes in different taxa, although
their relative importance appears to vary
between species.
In plants and animals, B chromosomes are
widespread, and no unifying pattern of taxonomic distribution is apparent. In contrast,
accessory chromosomes in fungi are restricted
almost exclusively to plant symbionts with a
large fraction of these being plant pathogens
(Bertazzoni et al. 2018; Mehrabi et al. 2017;
Soyer et al. 2018). Why are fungal accessory
chromosomes mainly found in plant pathogens? Fungal plant pathogens represent a very
intensively studied group of organisms, and
notably genetic and genomic variation has
been a focus of research (Mo ¨ller and Stukenbrock 2017). It is therefore possible that the
excess of examples in this group of organisms
simply reflects the research coverage. J. Taylor
and colleagues have moreover suggested that
the enrichment of accessory chromosomes in
plant-associated fungi may reflect the need to
rapidly adapt to changes in plant defense (Taylor et al. 2017). Host specificity determinants of
several plant-associated fungi locate on accessory chromosomes (Ahn and Walton 1996;
Coleman et al. 2009; Condon et al. 2013; Johnson et al. 2001; Ma et al. 2010). Possibly, this
particular genomic location provides an advantage for virulence-related traits as they can be
modified readily without affecting core processes. In this way, accessory chromosomes
may represent specific genome compartments
that allow these fungi to rapidly respond to
changes in host plant defenses (Taylor et al.
2017).
The function of accessory chromosomes
appears to be highly variable. B chromosomes
in plants and animals often have no known
function, and the fitness effect is assumed to
be neutral or even negative (Houben et al.
2014). However, a few examples demonstrate
that B chromosomes in plants and animals
can also confer a fitness advantage (Jones
1995; Pereira et al. 2017; Yoshida et al. 2011).
In several pathogenic fungi, accessory chromosomes directly influence pathogenicity as
they are required for the infection of specific
hosts and hence provide a benefit (Ahn and
Walton 1996; Coleman et al. 2009; Condon
et al. 2013; Johnson et al. 2001; Ma et al. 2010).
In these cases, the respective chromosomes
encode traits that confer a fitness advantage
and natural selection should favor individuals
carrying these chromosomes. By contrast, the
accessory chromosomes of the wheat pathogen
Zymoseptoria tritici were shown to cause a fitness disadvantage (Habig et al. 2017), highlighting the variety of fitness effects associated
with accessory chromosomes. However, for
many fungal accessory chromosomes, function
and fitness effects have yet to be determined,
and the influence of selection on the presence of
these chromosomes still remains unclear (Soyer
et al. 2018).
How are accessory chromosomes transmitted during cell division? Based on cytological
studies, much more is known about the transmission of accessory chromosomes during
mitosis and meiosis in plants and animals
than in fungi. Many B chromosomes in plant
and animals appear to offset their negative fitness effect by increasing their relative frequency during cell divisions compared to the
essential A chromosomes. This increase in frequency has been described as chromosome
drive which results from segregation distortion
before, during, or after meiosis (Houben 2017).
26
M. Habig and E. H. Stukenbrock
between core and accessory chromosomes suggests an origin within the same genome, while
in other species significant differences in
sequence composition may indicate horizontal
transfer (Akagi et al. 2009a; Ma et al. 2010).
Phylogenetic analyses of fungal plant pathogens, for example, indicate that the accessory
chromosomes of Fusarium oxysporum f. sp.
lycopersici causing Fusarium wilt of tomato
have a different origin than the core chromosome (Ma et al. 2010). Similarly, the accessory
chromosomes in asexual Alternaria alternata
strains appear to have been horizontally transferred between lineages (Akagi et al. 2009a).
The presence of mechanisms that allow horizontal transfer of entire chromosomes between
distinct lineages has furthermore been experimentally demonstrated (Akagi et al. 2009a, b;
He et al. 1998; Ma et al. 2010; Masel 1996). It is
therefore possible that mechanisms of both
models are involved in the origin of new accessory chromosomes in different taxa, although
their relative importance appears to vary
between species.
In plants and animals, B chromosomes are
widespread, and no unifying pattern of taxonomic distribution is apparent. In contrast,
accessory chromosomes in fungi are restricted
almost exclusively to plant symbionts with a
large fraction of these being plant pathogens
(Bertazzoni et al. 2018; Mehrabi et al. 2017;
Soyer et al. 2018). Why are fungal accessory
chromosomes mainly found in plant pathogens? Fungal plant pathogens represent a very
intensively studied group of organisms, and
notably genetic and genomic variation has
been a focus of research (Mo ¨ller and Stukenbrock 2017). It is therefore possible that the
excess of examples in this group of organisms
simply reflects the research coverage. J. Taylor
and colleagues have moreover suggested that
the enrichment of accessory chromosomes in
plant-associated fungi may reflect the need to
rapidly adapt to changes in plant defense (Taylor et al. 2017). Host specificity determinants of
several plant-associated fungi locate on accessory chromosomes (Ahn and Walton 1996;
Coleman et al. 2009; Condon et al. 2013; Johnson et al. 2001; Ma et al. 2010). Possibly, this
particular genomic location provides an advantage for virulence-related traits as they can be
modified readily without affecting core processes. In this way, accessory chromosomes
may represent specific genome compartments
that allow these fungi to rapidly respond to
changes in host plant defenses (Taylor et al.
2017).
The function of accessory chromosomes
appears to be highly variable. B chromosomes
in plants and animals often have no known
function, and the fitness effect is assumed to
be neutral or even negative (Houben et al.
2014). However, a few examples demonstrate
that B chromosomes in plants and animals
can also confer a fitness advantage (Jones
1995; Pereira et al. 2017; Yoshida et al. 2011).
In several pathogenic fungi, accessory chromosomes directly influence pathogenicity as
they are required for the infection of specific
hosts and hence provide a benefit (Ahn and
Walton 1996; Coleman et al. 2009; Condon
et al. 2013; Johnson et al. 2001; Ma et al. 2010).
In these cases, the respective chromosomes
encode traits that confer a fitness advantage
and natural selection should favor individuals
carrying these chromosomes. By contrast, the
accessory chromosomes of the wheat pathogen
Zymoseptoria tritici were shown to cause a fitness disadvantage (Habig et al. 2017), highlighting the variety of fitness effects associated
with accessory chromosomes. However, for
many fungal accessory chromosomes, function
and fitness effects have yet to be determined,
and the influence of selection on the presence of
these chromosomes still remains unclear (Soyer
et al. 2018).
How are accessory chromosomes transmitted during cell division? Based on cytological
studies, much more is known about the transmission of accessory chromosomes during
mitosis and meiosis in plants and animals
than in fungi. Many B chromosomes in plant
and animals appear to offset their negative fitness effect by increasing their relative frequency during cell divisions compared to the
essential A chromosomes. This increase in frequency has been described as chromosome
drive which results from segregation distortion
before, during, or after meiosis (Houben 2017).
26
M. Habig and E. H. Stukenbrock