the pisatin-detoxifying PDA and PEP genes of
N. haematococca are located on chromosomes
considered to be dispensable (Coleman et al.
2011; Milani et al. 2012; Williams et al. 2016).
Furthermore, in F. oxysporum f. sp. medicaginis and F. oxysporum f. sp. ciceris genes with
possible pathogenicity-related functions are
located on dispensable sequences (Williams
et al. 2016). Although a direct link between
pathogenicity and host specificity is lacking
for Magnaporthe oryzae, it is remarkable that
the accessory sequences in this fungus harbor
316 candidate effector genes, defined as genes
encoding secreted proteins (Yoshida et al.
2009). In addition, the avirulence gene AVRPita was found to be located at multiple genomic locations including loci on the accessory
chromosome (Chuma et al. 2011; Yoshida et al.
2009). Hence, the presence/absence of the
accessory chromosome may influence the ability to infect different host genotypes. Polymorphic localization of AVR-Pita (including on the
accessory chromosomes) was proposed to be
an adaptive strategy by allowing loss and
rapid recovery of this avirulence gene, consistent with the idea that the accessory chromosomes might serve as a particular genomic
environment allowing the rapid evolution of
new adaptive traits (Chuma et al. 2011).
In conclusion, genes located on accessory
chromosomes of fungi have often been associated with a fitness benefit—in many cases by
encoding traits that directly influence pathogenicity and host specificity. In contrast to the B
chromosomes in plants and animals, fungal
accessory chromosomes are rarely associated
with a fitness cost. Nevertheless, they can confer a fitness cost under some conditions as
demonstrated in Z. tritici and the potential
effects of avirulence factors present on the
accessory chromosomes in L. maculans and
M. oryzae.
IV. The Origin of Fungal Accessory
Chromosomes
How did accessory chromosomes originate in
fungal genomes? Genome data has shed light on
the possible origin of accessory chromosomes,
and experimental studies have revealed
mechanisms of de novo chromosome acquisition. Thereby evidence for two distinct scenarios have accumulated: (i) accessory
chromosomes can be derived from essential
core chromosomes, and (ii) they can be
acquired by horizontal chromosome transfer
from closely or distantly related taxa.
Initially, plant and animal B chromosomes were
thought to be non-homologous to the essential A chromosomes. This view later changed due to their mosaiclike composition of sequences derived from essential A
chromosomes and organelles, and therefore, they are
now mainly considered to originate from A chromosomes (Banaei-Moghaddam et al. 2015; Houben et al.
2014; Martis et al. 2012). The origin of B chromosomes
has been addressed using genomic data in rye, barley,
dogs, and several fish species (Banaei-Moghaddam
et al. 2015; Martis et al. 2012; Mayer et al. 2011;
Pansonato-Alves et al. 2014; Valente et al. 2014; Valente
et al. 2017). These analyses suggested a multi-step
model for the origin of accessory chromosomes from
several core chromosomes where initial genome duplication (either partial or comprising the whole genome)
has been followed by reductive chromosome translocations decreasing the size of the B chromosome (BanaeiMoghaddam et al. 2015; Houben et al. 2014). Chromosomes that have evolved in this way diverged over time
by the accumulation of repetitive sequences and further
structural variation that impaired homologous recombination with the original core chromosome (Galazka
and Freitag 2014; Houben et al. 2014). Alternatively,
small accessory chromosomes could be generated by
mis-segregation or Robertsonian translocations at or
near the centromeres of two acrocentric A chromosomes. This could result in the duplication of a short
region of A chromosomes that, if it contains a functional centromere and origin of replication, could be
considered a very small B chromosome and later may
increase in size by acquiring additional sequences
(Galazka and Freitag 2014).
In some fungal species, there is evidence that
accessory chromosomes have originated from
core chromosomes. In other species, it is conceivable that fusion of hyphae has mediated
horizontal transfer of chromosomes between
lineages or even species. So far, little is known
about the exact mechanism that transforms
core chromosome copies into accessory chromosomes. In Zymoseptoria tritici, experimental
mating and karyotyping of progeny strains
revealed the evolution of a new accessory chro32
M. Habig and E. H. Stukenbrock
N. haematococca are located on chromosomes
considered to be dispensable (Coleman et al.
2011; Milani et al. 2012; Williams et al. 2016).
Furthermore, in F. oxysporum f. sp. medicaginis and F. oxysporum f. sp. ciceris genes with
possible pathogenicity-related functions are
located on dispensable sequences (Williams
et al. 2016). Although a direct link between
pathogenicity and host specificity is lacking
for Magnaporthe oryzae, it is remarkable that
the accessory sequences in this fungus harbor
316 candidate effector genes, defined as genes
encoding secreted proteins (Yoshida et al.
2009). In addition, the avirulence gene AVRPita was found to be located at multiple genomic locations including loci on the accessory
chromosome (Chuma et al. 2011; Yoshida et al.
2009). Hence, the presence/absence of the
accessory chromosome may influence the ability to infect different host genotypes. Polymorphic localization of AVR-Pita (including on the
accessory chromosomes) was proposed to be
an adaptive strategy by allowing loss and
rapid recovery of this avirulence gene, consistent with the idea that the accessory chromosomes might serve as a particular genomic
environment allowing the rapid evolution of
new adaptive traits (Chuma et al. 2011).
In conclusion, genes located on accessory
chromosomes of fungi have often been associated with a fitness benefit—in many cases by
encoding traits that directly influence pathogenicity and host specificity. In contrast to the B
chromosomes in plants and animals, fungal
accessory chromosomes are rarely associated
with a fitness cost. Nevertheless, they can confer a fitness cost under some conditions as
demonstrated in Z. tritici and the potential
effects of avirulence factors present on the
accessory chromosomes in L. maculans and
M. oryzae.
IV. The Origin of Fungal Accessory
Chromosomes
How did accessory chromosomes originate in
fungal genomes? Genome data has shed light on
the possible origin of accessory chromosomes,
and experimental studies have revealed
mechanisms of de novo chromosome acquisition. Thereby evidence for two distinct scenarios have accumulated: (i) accessory
chromosomes can be derived from essential
core chromosomes, and (ii) they can be
acquired by horizontal chromosome transfer
from closely or distantly related taxa.
Initially, plant and animal B chromosomes were
thought to be non-homologous to the essential A chromosomes. This view later changed due to their mosaiclike composition of sequences derived from essential A
chromosomes and organelles, and therefore, they are
now mainly considered to originate from A chromosomes (Banaei-Moghaddam et al. 2015; Houben et al.
2014; Martis et al. 2012). The origin of B chromosomes
has been addressed using genomic data in rye, barley,
dogs, and several fish species (Banaei-Moghaddam
et al. 2015; Martis et al. 2012; Mayer et al. 2011;
Pansonato-Alves et al. 2014; Valente et al. 2014; Valente
et al. 2017). These analyses suggested a multi-step
model for the origin of accessory chromosomes from
several core chromosomes where initial genome duplication (either partial or comprising the whole genome)
has been followed by reductive chromosome translocations decreasing the size of the B chromosome (BanaeiMoghaddam et al. 2015; Houben et al. 2014). Chromosomes that have evolved in this way diverged over time
by the accumulation of repetitive sequences and further
structural variation that impaired homologous recombination with the original core chromosome (Galazka
and Freitag 2014; Houben et al. 2014). Alternatively,
small accessory chromosomes could be generated by
mis-segregation or Robertsonian translocations at or
near the centromeres of two acrocentric A chromosomes. This could result in the duplication of a short
region of A chromosomes that, if it contains a functional centromere and origin of replication, could be
considered a very small B chromosome and later may
increase in size by acquiring additional sequences
(Galazka and Freitag 2014).
In some fungal species, there is evidence that
accessory chromosomes have originated from
core chromosomes. In other species, it is conceivable that fusion of hyphae has mediated
horizontal transfer of chromosomes between
lineages or even species. So far, little is known
about the exact mechanism that transforms
core chromosome copies into accessory chromosomes. In Zymoseptoria tritici, experimental
mating and karyotyping of progeny strains
revealed the evolution of a new accessory chro32
M. Habig and E. H. Stukenbrock