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Abstract

Zymoseptoria tritici
is a fungal pathogen of wheat. T
he genome of the reference iso
late comprises 21 chromosomes of which eight are accessory. The
se
chromosomes are not key determina
nts for virulence, as in other
fungal pathogens, however, they ar
e partly conserved among dis
tinct
Zymoseptoria
species. Accessory chromosomes are highly instable during meios
is and mitosis, transcriptionally repressed and show enrichment
of repetitive elements
and heterochromatic histone marks
. To elucidate if heterochroma
tic histone modifications have an
impact on chromosome stabilit
y, we created deletion
mutants of the methyltransferases responsible for H3K27me3 and
H3K9me3. H3K27me3 is specifica
lly associated with accessory chr
omosomes and
subtelomeric regions in
Z. tritici
, while H3K9me3 is associated w
ith repetitive elements. We comb
ined experimental evolution, genetic and high-
resolution microscopic analyses t
o follow the impact of these d
eletions on chromosome and geno
me stability. We used ChIP-seq,
genome sequencing
and RNA-seq to compare changes in chromatin and genome structur
e and differences in gene expre
ssion between mutant and wild ty
pe strains. The loss
of H3K9me3 results in dramatic c
hromatin reorganization, transp
osable element activation, genom
e rearrangements, formation of
“neochromosomes”
and increased accessory chromos
ome instability. Loss of H3K27me
3, however, has little effect on
chromatin organization and tra
nsposon control, but
increases stability of the accessory chromosomes. We conclude t
hat H3K9me3 strongly impacts ch
romatin and genome organization
and that H3K27me3
has an important role in stab
ility of accessory chromosomes. Ep
igenetic regulation is an important driver of genome evolution
in this fungus and can
contribute to rapid adaptation.