1992). Today we know that the genomes of a
wide range of fungal species, in particular
plant pathogenic fungi, comprise accessory
chromosomes (Bertazzoni et al. 2018; Mehrabi
et al. 2017; Soyer et al. 2018). Here, we will focus
on a few cases that more generally exemplify
properties of accessory chromosomes in fungi.
N. haematococca can be found in diverse
habitats: as a soil saprophyte, as a commensal
organism in the rhizosphere, as a pathogen of
many different plant species, and as an opportunistic pathogen in humans (Vanetten 1978;
Zhang et al. 2006). The ability to thrive in
these diverse habitats is partly determined by
the presence of accessory chromosomes which
have been called conditionally dispensable
chromosomes in this fungus (Han et al. 2001;
Miao et al. 1991). Three of the 17 chromosomes
found in N. haematococca mating population
VI (MPVI), namely, chromosome (chr.) 14, chr.
15, and chr. 17, were shown to be dispensable
(Coleman et al. 2009). Similar to the B chromosomes in plants and animals, the conditionally
dispensable chromosomes of N. haematococca
MPVI contain an increased abundance of repetitive sequences and show a lower GC content in
comparison to the core chromosomes (Coleman et al. 2009). They harbor more unique
genes (i.e., genes without homologs), and
these may reflect adaptation to different environmental niches of individual isolates (Coleman et al. 2009).
The accessory chromosomes of the economically important wheat pathogen Zymoseptoria tritici comprise 12% of the genome in the
reference isolate IPO323 with eight distinct
accessory chromosomes that range in size
from 409 to 773 kb (Goodwin et al. 2011). This
represents one of the largest complements of
accessory chromosomes described to date. In
comparison to the core chromosomes, the
accessory chromosomes of Z. tritici are relatively gene-poor (Goodwin et al. 2011; Grandaubert et al. 2015). The genes located on these
chromosomes show a distinct codon usage
which differs from the codon usage of the
genes located on the core chromosomes (Goodwin et al. 2011). Interestingly, only few genes on
the accessory chromosomes encode proteins of
known function, and most of the predicted
genes do not comprise any annotated functional domains (Grandaubert et al. 2015). In
contrast to accessory chromosomes of other
fungal pathogens, the accessory chromosomes
of Z. tritici contain a significantly lower number
of genes encoding secreted proteins and putative virulence determinants (Grandaubert et al.
2015; Rep et al. 2004; Vlaardingerbroek et al.
2016a). Only few genes belong to gene families
that include members on both the core and
accessory chromosomes, and a detailed survey
of gene duplicates showed a low number of
paralogous sequences on the accessory chromosomes (Kellner et al. 2014). The accessory
chromosomes of Z. tritici are enriched in repetitive DNA and transposable elements (Grandaubert et al. 2015) and, similar to the B
chromosomes in plants, show histone modifications associated with heterochromatin
(Schotanus et al. 2015). In comparison to the
core chromosomes, they are highly enriched in
post-translational modification of the histone
H3 by trimethylation of lysine 27 (H3K27me3)
(Schotanus et al. 2015). Sequencing of the
IPO323 genome led to the hypothesis that the
accessory chromosomes in this organism originated from horizontal chromosome transfer
from another organism (Goodwin et al. 2011).
However, the fact that closely related species of
Z. tritici like Zymoseptoria pseudotritici, Zymoseptoria ardabiliae, and Zymoseptoria brevis
also harbor accessory chromosomes including
regions syntenic to regions of the accessory
chromosomes of Z. tritici suggest that these
chromosomes represent an ancient trait in the
genus (Feurtey, Lorrain et al., in prep).
The characteristic structural features that
distinguish accessory from core chromosomes
are also present in Leptosphaeria maculans, a
pathogen that causes stem canker (blackleg) of
oilseed rape (Brassica napus) and related crucifers (Rouxel and Balesdent 2005; West et al.
2001). L. maculans contains a dispensable
mini-chromosome of 700–950 kb in size
(Leclair et al. 1996) which mostly comprises
AT-enriched isochores (>60% AT). Besides
being AT-rich, this mini-chromosome is genepoor (Balesdent et al. 2013; Rouxel et al. 2011)
and heterochromatic (Soyer et al. 2014). Interestingly, the AT isochores are enriched in trans2 Origin, Function, and Transmission of Accessory Chromosomes
29
wide range of fungal species, in particular
plant pathogenic fungi, comprise accessory
chromosomes (Bertazzoni et al. 2018; Mehrabi
et al. 2017; Soyer et al. 2018). Here, we will focus
on a few cases that more generally exemplify
properties of accessory chromosomes in fungi.
N. haematococca can be found in diverse
habitats: as a soil saprophyte, as a commensal
organism in the rhizosphere, as a pathogen of
many different plant species, and as an opportunistic pathogen in humans (Vanetten 1978;
Zhang et al. 2006). The ability to thrive in
these diverse habitats is partly determined by
the presence of accessory chromosomes which
have been called conditionally dispensable
chromosomes in this fungus (Han et al. 2001;
Miao et al. 1991). Three of the 17 chromosomes
found in N. haematococca mating population
VI (MPVI), namely, chromosome (chr.) 14, chr.
15, and chr. 17, were shown to be dispensable
(Coleman et al. 2009). Similar to the B chromosomes in plants and animals, the conditionally
dispensable chromosomes of N. haematococca
MPVI contain an increased abundance of repetitive sequences and show a lower GC content in
comparison to the core chromosomes (Coleman et al. 2009). They harbor more unique
genes (i.e., genes without homologs), and
these may reflect adaptation to different environmental niches of individual isolates (Coleman et al. 2009).
The accessory chromosomes of the economically important wheat pathogen Zymoseptoria tritici comprise 12% of the genome in the
reference isolate IPO323 with eight distinct
accessory chromosomes that range in size
from 409 to 773 kb (Goodwin et al. 2011). This
represents one of the largest complements of
accessory chromosomes described to date. In
comparison to the core chromosomes, the
accessory chromosomes of Z. tritici are relatively gene-poor (Goodwin et al. 2011; Grandaubert et al. 2015). The genes located on these
chromosomes show a distinct codon usage
which differs from the codon usage of the
genes located on the core chromosomes (Goodwin et al. 2011). Interestingly, only few genes on
the accessory chromosomes encode proteins of
known function, and most of the predicted
genes do not comprise any annotated functional domains (Grandaubert et al. 2015). In
contrast to accessory chromosomes of other
fungal pathogens, the accessory chromosomes
of Z. tritici contain a significantly lower number
of genes encoding secreted proteins and putative virulence determinants (Grandaubert et al.
2015; Rep et al. 2004; Vlaardingerbroek et al.
2016a). Only few genes belong to gene families
that include members on both the core and
accessory chromosomes, and a detailed survey
of gene duplicates showed a low number of
paralogous sequences on the accessory chromosomes (Kellner et al. 2014). The accessory
chromosomes of Z. tritici are enriched in repetitive DNA and transposable elements (Grandaubert et al. 2015) and, similar to the B
chromosomes in plants, show histone modifications associated with heterochromatin
(Schotanus et al. 2015). In comparison to the
core chromosomes, they are highly enriched in
post-translational modification of the histone
H3 by trimethylation of lysine 27 (H3K27me3)
(Schotanus et al. 2015). Sequencing of the
IPO323 genome led to the hypothesis that the
accessory chromosomes in this organism originated from horizontal chromosome transfer
from another organism (Goodwin et al. 2011).
However, the fact that closely related species of
Z. tritici like Zymoseptoria pseudotritici, Zymoseptoria ardabiliae, and Zymoseptoria brevis
also harbor accessory chromosomes including
regions syntenic to regions of the accessory
chromosomes of Z. tritici suggest that these
chromosomes represent an ancient trait in the
genus (Feurtey, Lorrain et al., in prep).
The characteristic structural features that
distinguish accessory from core chromosomes
are also present in Leptosphaeria maculans, a
pathogen that causes stem canker (blackleg) of
oilseed rape (Brassica napus) and related crucifers (Rouxel and Balesdent 2005; West et al.
2001). L. maculans contains a dispensable
mini-chromosome of 700–950 kb in size
(Leclair et al. 1996) which mostly comprises
AT-enriched isochores (>60% AT). Besides
being AT-rich, this mini-chromosome is genepoor (Balesdent et al. 2013; Rouxel et al. 2011)
and heterochromatic (Soyer et al. 2014). Interestingly, the AT isochores are enriched in trans2 Origin, Function, and Transmission of Accessory Chromosomes
29