Some genes directly influence pathogenicity
and host range. One of the conditionally dispensable chromosomes of Nectria haematococca, the PDA1-CD chromosome, carries, for
example, a cluster of genes required for pea
pathogenicity (PEP) (Han et al. 2001). N. haematococca isolates with the PDA1-CD chromosome are highly virulent on pea plants due to
the presence of the PDA1 gene which is part of
the PEP cluster and codes for a cytochrome
P450 enzyme that detoxifies the pea phytoalexin pisatin (Maloney and VanEtten 1994).
By contrast, N. haematococca isolates lacking
the PDA1-CD chromosome are strongly attenuated in the ability to cause lesions on pea (Han
et al. 2001). The dispensable chromosome of
Leptosphaeria maculans also contains genes
that affect its host range. These include the
avirulence gene AvrLm11 conferring avirulence
on Brassica rapa (Balesdent et al. 2013) located
on one of the dispensable chromosomes of L.
maculans as well as five additional putative
effector genes (Rouxel et al. 2011). The loss of
the dispensable chromosome of L. maculans
leads to susceptibility of B. rapa carrying the
resistance gene Rlm11 (Rouxel and Balesdent
2017). However, the reason for the continued
maintenance of the accessory chromosome
encoding the AvrLm11 in L. maculans populations remains unclear to date. Individuals with
this accessory chromosome are avirulent on
Rlm11 carrying hosts and therefore would
have a substantial fitness disadvantage. We
speculate that a counteracting selection, possibly a transmission advantage during meiotic or
mitotic reproduction, maintains this chromosome in the population.
In Zymoseptoria tritici, the functional role
of the accessory chromosomes is less clear.
Based on quantitative trait loci mapping, small
but significant fitness benefits for certain accessory chromosomes were detected (Stewart et al.
2016). However, isogenic Z. tritici strains with
deletions of whole accessory chromosomes
could produce more pycnidia than the wild
type, and therefore the accessory chromosomes
14, 16, 18, 19, and 21 rather confer a fitness cost
(Habig et al. 2017). Interestingly, this fitness
cost was dependent on the host wheat cultivar
suggesting an interaction of host genotypespecific traits and traits encoded by the accessory chromosomes. Z. tritici switches to necrotrophic growth after a prolonged period of
symptomless, biotrophic growth. Several accessory chromosomes of Z. tritici influence the
timing of this lifestyle switch (Habig et al.
2017), but yet it is unclear how this affects the
fitness of the pathogen in the field.
Host specificity is also influenced by the
accessory chromosomes in lineages of the
genus Alternaria. These plant-pathogenic
fungi infect a remarkably broad range of hosts
(Rotem 1994). Accessory chromosomes, which
are called conditionally dispensable chromosomes in Alternaria, are carried by several
Alternaria lineages (Akamatsu et al. 1999;
Hatta et al. 2002; Johnson et al. 2001). These
are generally smaller than 2.0 MB in size (Akagi
et al. 2009b; Salamiah et al. 2001a, b) and represent a prominent example of how host specificity is determined by traits encoded on
accessory chromosomes. Several genes that
are encoding host-specific toxins (HSTs) or
are involved in the biosynthesis of toxins are
located within gene clusters on the conditionally dispensable chromosomes (Nakatsuka
et al. 1986; Nakashima et al. 1985; Kohmoto
1993; Johnson et al. 2001; Akamatsu et al.
1997). Thereby, these genes confer a strong
selection advantage during host-pathogen
interaction, and this selection appears to maintain these chromosomes in the Alternaria
populations.
Fusarium oxysporum reproduces asexually
and consists of many pathogenic clonal
lineages which are grouped into host-specific
formae speciales (Baayen et al. 2000; Lievens
et al. 2008; O’Donnell et al. 1998; Recorbet
et al. 2003). The ability of F. oxysporum to infect
and avoid recognition in its host plant depends
on small Secreted-in-xylem (SIX) proteins that
are secreted into the host xylem during the
infection (Rep et al. 2004). In the tomatopathogen F. oxysporum f. sp. lycopersici, the
lineage-specific chromosome 14 harbors six
SIX genes, and the lineage-specific chromosomes in general are enriched in genes coding
for secreted effectors and virulence factors (Ma
et al. 2010; Schmidt et al. 2013). In the peapathogen F. oxysporum f. sp. pisi, homologs of
2 Origin, Function, and Transmission of Accessory Chromosomes
31
and host range. One of the conditionally dispensable chromosomes of Nectria haematococca, the PDA1-CD chromosome, carries, for
example, a cluster of genes required for pea
pathogenicity (PEP) (Han et al. 2001). N. haematococca isolates with the PDA1-CD chromosome are highly virulent on pea plants due to
the presence of the PDA1 gene which is part of
the PEP cluster and codes for a cytochrome
P450 enzyme that detoxifies the pea phytoalexin pisatin (Maloney and VanEtten 1994).
By contrast, N. haematococca isolates lacking
the PDA1-CD chromosome are strongly attenuated in the ability to cause lesions on pea (Han
et al. 2001). The dispensable chromosome of
Leptosphaeria maculans also contains genes
that affect its host range. These include the
avirulence gene AvrLm11 conferring avirulence
on Brassica rapa (Balesdent et al. 2013) located
on one of the dispensable chromosomes of L.
maculans as well as five additional putative
effector genes (Rouxel et al. 2011). The loss of
the dispensable chromosome of L. maculans
leads to susceptibility of B. rapa carrying the
resistance gene Rlm11 (Rouxel and Balesdent
2017). However, the reason for the continued
maintenance of the accessory chromosome
encoding the AvrLm11 in L. maculans populations remains unclear to date. Individuals with
this accessory chromosome are avirulent on
Rlm11 carrying hosts and therefore would
have a substantial fitness disadvantage. We
speculate that a counteracting selection, possibly a transmission advantage during meiotic or
mitotic reproduction, maintains this chromosome in the population.
In Zymoseptoria tritici, the functional role
of the accessory chromosomes is less clear.
Based on quantitative trait loci mapping, small
but significant fitness benefits for certain accessory chromosomes were detected (Stewart et al.
2016). However, isogenic Z. tritici strains with
deletions of whole accessory chromosomes
could produce more pycnidia than the wild
type, and therefore the accessory chromosomes
14, 16, 18, 19, and 21 rather confer a fitness cost
(Habig et al. 2017). Interestingly, this fitness
cost was dependent on the host wheat cultivar
suggesting an interaction of host genotypespecific traits and traits encoded by the accessory chromosomes. Z. tritici switches to necrotrophic growth after a prolonged period of
symptomless, biotrophic growth. Several accessory chromosomes of Z. tritici influence the
timing of this lifestyle switch (Habig et al.
2017), but yet it is unclear how this affects the
fitness of the pathogen in the field.
Host specificity is also influenced by the
accessory chromosomes in lineages of the
genus Alternaria. These plant-pathogenic
fungi infect a remarkably broad range of hosts
(Rotem 1994). Accessory chromosomes, which
are called conditionally dispensable chromosomes in Alternaria, are carried by several
Alternaria lineages (Akamatsu et al. 1999;
Hatta et al. 2002; Johnson et al. 2001). These
are generally smaller than 2.0 MB in size (Akagi
et al. 2009b; Salamiah et al. 2001a, b) and represent a prominent example of how host specificity is determined by traits encoded on
accessory chromosomes. Several genes that
are encoding host-specific toxins (HSTs) or
are involved in the biosynthesis of toxins are
located within gene clusters on the conditionally dispensable chromosomes (Nakatsuka
et al. 1986; Nakashima et al. 1985; Kohmoto
1993; Johnson et al. 2001; Akamatsu et al.
1997). Thereby, these genes confer a strong
selection advantage during host-pathogen
interaction, and this selection appears to maintain these chromosomes in the Alternaria
populations.
Fusarium oxysporum reproduces asexually
and consists of many pathogenic clonal
lineages which are grouped into host-specific
formae speciales (Baayen et al. 2000; Lievens
et al. 2008; O’Donnell et al. 1998; Recorbet
et al. 2003). The ability of F. oxysporum to infect
and avoid recognition in its host plant depends
on small Secreted-in-xylem (SIX) proteins that
are secreted into the host xylem during the
infection (Rep et al. 2004). In the tomatopathogen F. oxysporum f. sp. lycopersici, the
lineage-specific chromosome 14 harbors six
SIX genes, and the lineage-specific chromosomes in general are enriched in genes coding
for secreted effectors and virulence factors (Ma
et al. 2010; Schmidt et al. 2013). In the peapathogen F. oxysporum f. sp. pisi, homologs of
2 Origin, Function, and Transmission of Accessory Chromosomes
31