Therefore, many B chromosomes of plants and
animals are considered to be selfish genetic
elements propagating themselves at a cost for
the organism (Houben 2017). Similarly, in
fungi, the accessory chromosomes of Botrytis
cinerea, Cochliobolus heterostrophus, Gibberella fujikuroi mating population A, Leptosphaeria maculans, Magnaporthe oryzae, N.
haematococca mating population VI, and Z.
tritici show non-Mendelian inheritance during
meiosis (Table 2.1). This non-Mendelian inheritance involves either frequent losses or transmission advantages, i.e., transmission of an
accessory chromosome to more progeny than
predicted by Mendelian segregation (Coleman
et al. 2009; Croll et al. 2013; He et al. 1998;
Mehrabi et al. 2017; Orbach et al. 1996; Soyer
et al. 2018; Wittenberg et al. 2009; Xu and Leslie
1996). In this respect, it is likely that accessory
chromosomes are also propagated by a drive
mechanism in fungi. In support of this, we
recently demonstrated a meiotic chromosome
drive of accessory chromosomes in Z. tritici
(Habig et al. 2018).
For fungi without a sexual cycle, only
mitotic transmission of accessory chromosomes is relevant. In these cases, fungal accessory chromosomes can again show distinct
mitotic transmission patterns with extremely
high frequencies of chromosome losses and
chromosome rearrangements (Mo ¨ller et al.
2018; Vlaardingerbroek et al. 2016a). We
argue that the distinct transmission patterns
of accessory chromosomes during mitosis and
meiosis determine the distribution and frequency of accessory chromosomes in fungal
populations. A plausible explanation for this
chromosome variation is the ability of fungi to
rapidly generate new phenotypes in changing
environments. However, there is no direct evidence for this hypothesis in natural populations
of fungi.
We here address the origin, function, and
transmission of accessory chromosomes in
fungi. A main focus of our review is the mitotic
and meiotic transmission of accessory chromosomes, which in many fungi clearly differs
from the transmission of core chromosomes.
Since the accessory chromosomes of fungi,
plants, and animals share characteristics, we
first briefly discuss the B chromosomes of
plants and animals where previous findings
can complement the knowledge available on
the accessory chromosomes of fungi. We first
give an overview on the occurrence and characteristics of fungal accessory chromosomes
with a focus on their function and possible
origin. We use the term accessory chromosome
as a general term and only mention the specific
names used in distinct species when referring
to examples in detail. Similarly, we will use the
term core chromosomes to specify the chromosomes that are shared by all members of a
population.
II. Accessory Chromosomes Are
Widespread and Diverse but Share
Specific Characteristics
In plants, accessory chromosomes are often
described as B chromosomes contrasting to
the essential A chromosomes shared by all individuals of a species. One of the best-studied
examples is the rye (Secale cereale) B chromosome of which up to eight copies can be found
within a single cell. In animals, B chromosomes
have been described, among others, in fish,
amphibian, and insects, including a recent
example from the model system Drosophila
melanogaster (Bauerly et al. 2014). These plant
and animal B chromosomes share some characteristics: they usually comprise highly repetitive DNA sequences which show sequence
similarities to either A chromosomes within
the same genome or A chromosomes in closely
related species (Pansonato-Alves et al. 2014).
These sequences can be derived from mobile
genetic elements, satellite DNA, or ribosomal
DNA (Bougourd and Jones 1997; Dhar et al.
2002; Houben et al. 2001; Houben 2017; Lamb
et al. 2007; Pansonato-Alves et al. 2014) and are
usually found to be heterochromatic (Cheng
2010; O ¨ stergren 1947) and gene-poor (BanaeiMoghaddam et al. 2015).
The first fungal accessory chromosomes
were described for two plant pathogenic species: Nectria haematococca (Miao et al. 1991)
and Cochliobolus heterostrophus (Tzeng et al.
2 Origin, Function, and Transmission of Accessory Chromosomes
27
animals are considered to be selfish genetic
elements propagating themselves at a cost for
the organism (Houben 2017). Similarly, in
fungi, the accessory chromosomes of Botrytis
cinerea, Cochliobolus heterostrophus, Gibberella fujikuroi mating population A, Leptosphaeria maculans, Magnaporthe oryzae, N.
haematococca mating population VI, and Z.
tritici show non-Mendelian inheritance during
meiosis (Table 2.1). This non-Mendelian inheritance involves either frequent losses or transmission advantages, i.e., transmission of an
accessory chromosome to more progeny than
predicted by Mendelian segregation (Coleman
et al. 2009; Croll et al. 2013; He et al. 1998;
Mehrabi et al. 2017; Orbach et al. 1996; Soyer
et al. 2018; Wittenberg et al. 2009; Xu and Leslie
1996). In this respect, it is likely that accessory
chromosomes are also propagated by a drive
mechanism in fungi. In support of this, we
recently demonstrated a meiotic chromosome
drive of accessory chromosomes in Z. tritici
(Habig et al. 2018).
For fungi without a sexual cycle, only
mitotic transmission of accessory chromosomes is relevant. In these cases, fungal accessory chromosomes can again show distinct
mitotic transmission patterns with extremely
high frequencies of chromosome losses and
chromosome rearrangements (Mo ¨ller et al.
2018; Vlaardingerbroek et al. 2016a). We
argue that the distinct transmission patterns
of accessory chromosomes during mitosis and
meiosis determine the distribution and frequency of accessory chromosomes in fungal
populations. A plausible explanation for this
chromosome variation is the ability of fungi to
rapidly generate new phenotypes in changing
environments. However, there is no direct evidence for this hypothesis in natural populations
of fungi.
We here address the origin, function, and
transmission of accessory chromosomes in
fungi. A main focus of our review is the mitotic
and meiotic transmission of accessory chromosomes, which in many fungi clearly differs
from the transmission of core chromosomes.
Since the accessory chromosomes of fungi,
plants, and animals share characteristics, we
first briefly discuss the B chromosomes of
plants and animals where previous findings
can complement the knowledge available on
the accessory chromosomes of fungi. We first
give an overview on the occurrence and characteristics of fungal accessory chromosomes
with a focus on their function and possible
origin. We use the term accessory chromosome
as a general term and only mention the specific
names used in distinct species when referring
to examples in detail. Similarly, we will use the
term core chromosomes to specify the chromosomes that are shared by all members of a
population.
II. Accessory Chromosomes Are
Widespread and Diverse but Share
Specific Characteristics
In plants, accessory chromosomes are often
described as B chromosomes contrasting to
the essential A chromosomes shared by all individuals of a species. One of the best-studied
examples is the rye (Secale cereale) B chromosome of which up to eight copies can be found
within a single cell. In animals, B chromosomes
have been described, among others, in fish,
amphibian, and insects, including a recent
example from the model system Drosophila
melanogaster (Bauerly et al. 2014). These plant
and animal B chromosomes share some characteristics: they usually comprise highly repetitive DNA sequences which show sequence
similarities to either A chromosomes within
the same genome or A chromosomes in closely
related species (Pansonato-Alves et al. 2014).
These sequences can be derived from mobile
genetic elements, satellite DNA, or ribosomal
DNA (Bougourd and Jones 1997; Dhar et al.
2002; Houben et al. 2001; Houben 2017; Lamb
et al. 2007; Pansonato-Alves et al. 2014) and are
usually found to be heterochromatic (Cheng
2010; O ¨ stergren 1947) and gene-poor (BanaeiMoghaddam et al. 2015).
The first fungal accessory chromosomes
were described for two plant pathogenic species: Nectria haematococca (Miao et al. 1991)
and Cochliobolus heterostrophus (Tzeng et al.
2 Origin, Function, and Transmission of Accessory Chromosomes
27