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Fungal Evolution Symposium
Haeckel (1904) Kunstformen der Natur
8-9 November 2016
Max Planck Institute for Evolutionary
Biology, Plön
Tuesday
9:00
Introductory remarks
9:15
Jaqueline Hess
Examining genomic changes sustaining ecological transitions in fungi – or
learning how to talk to plants
10:00
Inger Skrede
The fungus that came in from the cold: evolutionary necessities for invading
buildings
10:45
Coffee break
10:15
Joana Bernardes
Heterozygosity influences hybrid fitness
11:35
Sundy Maurice
Fungi on the move: Don’t stand so close to me!
12:20
Lunch
14:45
Hanna Johannesson
Genomic conflict as a driver of genome evolution: insights from the fungal spore
killers
15:00
David Rogers
Beauty and the yeast: translational control of Saccharomyces pheromone
production and mating success
15:20
Primrose Boynton
Survival, bet-hedging, and sex: What's a spore for?
15:40
Social hike with discussion
18:30
Barbecue for all participants
Wednesday
9:00
Marie Davey
Who’s driving? Host-parasite evolution in the bryophilous genus Lizonia
9:45
Chaitanya Gokhale
Host-parasite coevolution in a domesticated world
10:05
Christoph Eschenbrenner
Evolutionary genomics and population genetic analyses of the Zymoseptoria
species complex
10:25
Coffee break
11:00
Ezgi Özkurt
Genome Evolution of the Fungal Grass Pathogen Zymoseptoria pseudotritici
11:20
Frank Kempken
Marine Fungi - identification, genomics and transcriptomics
12:05
Lunch and discussion
Paid for by the workshop program of the MPI for Evolutionary Biology
Abstracts:
Examining genomic changes sustaining ecological transitions in fungi – or learning
how to talk to plants
Jaqueline Hess, University of Vienna
Fungi are evolutionary shape shifters, harbouring the ability to rapidly adapt to new
environments. Many fungal ecotypes, for example mycorrhizal symbionts, plant and
animal pathogens or finely tuned wood decayers that have shunted the need for costly
enzymatic machinery have evolved repeatedly and independently across the fungal
tree of life. These remarkable instances of convergent evolution suggest both, the
presence of a strong intrinsic property of fungal genomes to form these reoccurring
ecotypes, and the ability to reconfigure their genome content and its expression
accordingly. Here, I will use two examples at different evolutionary time-scales to
illustrate how various mechanisms of genome evolution have shaped genomes across
such ecological transitions, and where superficially distinct ecologies may have
common evolutionary starting points. Examples will include the transition from
asymbiotic to ectomycorrhizal ecology in the genus Amanita and specialisation of
wood decay mechanisms in the invasive brown rot fungus Serpula lacrymans, in its
adaptation to the human built environment.
The fungus that came in from the cold: evolutionary necessities for invading buildings
Inger Skrede, University of Oslo
Many organisms benefit from being adapted to niches shaped by human activity, and
have successfully invaded human-made habitats. One such species is the dry-rot
fungus Serpula lacrymans that decomposes coniferous construction wood. This
species has spread from its natural high mountain habitat in Asia to houses in
temperate regions worldwide. In this study we analyse which physiological and
genomic features separate S. lacrymans from close relatives growing in forests, and
which features that divide different S. lacrymans populations growing in houses. We
demonstrate that S. lacrymans is more specialized in which wood species it prefers
and is a poorer competitor than its wild relative S. himantioides, which encounters
many more competitors in its natural habitat. Further, genomic mechanisms related to
intracellular transport, specialized metabolism and wood decomposition mechanisms
seem to have been important to shape the different Serpula species. Nevertheless, the
different populations of S. lacrymans behave differently and have a different
evolutionary history. Thus, in order to understand what makes a successful invader of
the built environment the population history is also an important part of the puzzle. I
will present recent results of these analyses.
Heterozygosity influences hybrid fitness
Joana Bernardes, MPI Plön
Domesticated yeast diploids will tend to accumulate recessive deleterious mutations,
which cannot be purged from the population because they are never exposed to
selection. Domesticated diploid strains are therefore expected to have numerous
masked recessive deleterious alleles, consistent with the high levels of heterozygosity
previously described. Wild strains of S. cerevisiae and S. paradoxus have low levels
of heterozygosity and therefore are likely to carry fewer recessive deleterious alleles.
When domesticated isolates are brought to the laboratory, the heterozygosity is
eliminated, because most studies are done with haploid strains, or with diploid strains
that were derived from a single spore (autodiplodized or selfed), so the resulting
diploid is completely homozygous, masking the true heterozygous nature of the
isolates. This loss of heterozygosity exposes the accumulated recessive deleterious
alleles, resulting in low fitness. When two domesticated strains are crossed together,
much of the heterozygosity is restored and the fitness of the resulting diploid will
increase relative to the homozygous “parent”. We argue if the hybrid fitness was
compared to that of the original heterozygous diploid parents, the fitness difference
would be much reduced if there is any. On the other hand, when wild isolates are
made homozygous, there will be few recessive alleles exposed. Consequently, we
expect little fitness differences between the wild diploid strains and their homozygous
derivatives, so there would be no fitness advantage of hybrid when compared to either
parent.
Fungi on the move: Don’t stand so close to me!
Sundy Maurice, University of Oslo
Dispersal is key process that underpins ecological genetics, it plays an important role
in population dynamics and consequently in the maintenance of species diversity and
genetic variation. Fungi producing large quantities of spores are supposed to have
greater capacity for dispersal and hence giving rise to large and widespread
populations. Despite this high potential to disperse, macrofungi, known to produce
billions of spores a day, are threatened in many European forests, hence resulting in
an increase in awareness and establishment of Red-Lists of threatened fungal species.
Forest loss and habitat fragmentation is one of the main causes of biodiversity loss. In
Fennoscandia, considerable loss and fragmentation of natural forests have taken place
during the last centuries due to intensive forest management and short rotation times,
together combined with a substantial reduction in the amount of dead wood on
ground. The aim of my research is to reveal how the genetic variation within species
has been affected by habitat fragmentation. Given the diversity and ecological
importance of fungi, there is however a lack of population genetic research. The main
reason for this can be explained by the cryptic nature of fungi and the difficulty of
delimiting the individuality boundaries. In this study, the ability of restriction-site
associated DNA (RAD) sequencing to generate SNPs in polypore species was
examined. Different trends of the genetic diversity among the species are observed.
The data were analyzed using tests of Hardy-Weinburg equilibrium, population
genetic statistics and population structure were inferred using the program
fineRADstructure. Differences in allelic frequencies and populations sizes exhibited
among species suggest that the abilities to persist as an isolated population could be
threatened while species presenting larger population size may present higher fitness.
This study brings insights about genetic variation of fungi at a finer geographic scale
and indicates the potential to address population genetics and evolutionary questions
at broader geographic scales.
Genomic conflict as a driver of genome evolution: insights from the fungal spore
killers
Hanna Johannesson, Uppsala University
Conflicts caused by selfish genetic elements is expected to be a driving force for
evolutionary innovation, and hence, of fundamental importance for all aspects of
evolution. In my research group, we use the filamentous ascomycete Neurospora as a
study system of the impact on meiotic drive on genome evolution. In this genus, the
meiotic drive element Spore killer is found. In sexual crosses between strains carrying
a Spore killer element and wild-type strains, half of the spores will die and all the
surviving spores will carry the killer element. We have investigated direct and indirect
effects of carrying the element and preliminary data suggest that it is reducing the
fitness of the carrier. Furthermore, we have undertaken a genomic approach to
identify the killer elements and to analyze their effect on genome architecture. This
data has revealed a complex pattern of inversions, insertions and deletions that may
play an essential role in maintaining the region of suppressed recombination between
the killer elements and their resistance factors, and in explaining the birth and death of
new Spore killers over evolutionary time. Taken in combination, results emerging
from this project suggest that meiotic drive has evolved multiple times independently
in Neurospora and in spite of host genome defense, it has had a profound effect of
genomic architecture in this genus.
Beauty and the yeast: translational control of Saccharomyces pheromone production
and mating success
David Rogers, Ellen McConnell, Duncan Greig, MPI Plön
Many complex behaviours, including those of unicellular organisms, are regulated by
peptides derived from polyproteins: large prohormones that are cleaved to release
multiple bioactive peptides. Despite their importance, very little is known about
polyprotein evolution. The MFα1 gene of the baker's yeast Saccharomyces cerevisiae
is a model polyprotein-encoding gene: the prohormone product is processed to release
a variable number of copies of the mating pheromone α-factor. MFα1 is the source of
nearly all of the α-factor produced by a yeast cell, but is not necessary for mating as
the small amount of pheromone produced from its paralog MFα2 is sufficient for
conjugation. However, when yeast cells compete for mates, cells producing the
highest level of α-factor are most likely to be successful. Thus, synthesis of the MFα1
gene product is directly related to yeast sexual fitness. We show that the number of
mature pheromone repeats encoded by MFα1 varies considerably between even
closely related strains, and that repeat number is positively correlated with both the
amount of pheromone secreted by a cell and its competitive mating success. However,
increasing repeat number beyond the maximum observed in nature fails to further
improve pheromone production or mating success. The basis of these diminishing
returns is not associated with MFα1 transcript levels or with bottlenecks in protein
processing or secretion. Instead, we propose that transcripts with more repeats are
translated less efficiently than those with fewer repeats, a widespread phenomenon
termed "length-dependent translation". Consistent with this hypothesis, we show that
pheromone production and mating success are influenced both by MFα1 synonymous
codon usage and by the putative regulator of length-dependent translation Asc1.
Survival, bet-hedging, and sex: What's a spore for?
Primrose Boynton, MPI Plön
In fungal spores, recombination is often coupled to resistance to environmental stress.
Both sex and resistance are possible adaptations to unpredictable environmental
selection, but it is not obvious why they would be coupled. Why would a fungus not
produce resistant asexual spores or susceptible sexual spores, especially if resistance
and sex are costly? We investigated interactions between spore resistance and sex in
the life cycle of the model yeast Saccharomyces cerevisiae, which produces resistant
haploid ascospores from diploid parent cells. Each S. cerevisiae genotype has its own
heritable sporulation efficiency--sporulation efficiency is the percentage of
genetically identical cells which form spores in response to starvation. Once a food
source is reintroduced, non-sporulated cells have the opportunity to grow quickly,
while sporulated cells must germinate and mate before reaching their optimal growth
rates. Sporulation efficiency is therefore a bet-hedging trait, and theory predicts that it
evolves as a function of the frequency of strong selective events. The theoretical
prediction disregards the influence of sex, which may further influence sporulation
efficiency in unpredictable environments. We explored the evolution of sporulation
efficiency by selecting S. cerevisiae populations under unpredictable conditions. We
expected sporulation efficiency to closely match the frequency of strong selection, but
not the absolute number of selective treatments, if resistance and bet-hedging were
important to life cycle completion. Sporulation efficiency did indeed evolve to match
selective treatment frequency in many selective lines. However, some lines that had
experienced high selection also evolved vegetative resistance and low sporulation
efficiencies; sporulation efficiency became decoupled to selection frequency in these
lines. The selective treatments most likely increased the frequency of sexual
recombination until cells with resistant gene combinations appeared, and the resulting
populations subsequently evolved low sporulation efficiencies. In our selective
regime, sporulation was only advantageous until sexual recombination could produce
a cell that needed neither resistant spores nor further recombination.
Who’s driving? Host-parasite evolution in the bryophilous genus Lizonia
Marie Davey, University of Oslo
The genus Lizonia is an exclusively bryophilous lineage with a unique life history.
The fungus is a parasite occurring specifically on the male reproductive structures of
polytrichaceous mosses. A single fungal perithecium completely replaces each male
antheridium, effectively castrating the plant and diverting the resources the plant has
allocated to reproduction. The genus was historically thought to be a member of the
Pseudoperisporiaceae, but recent phylogenetic studies have pointed towards an
affinity to the Pleosporales. A three gene phylogeny was built, confirming Lizonia’s
membership in the Didymellaceae (Pleosporales). The genus-level phylogeny did not
fully reflect traditional morphology-based classifications, and was strongly structured
by host specificity. Two new species are described accordingly, and the traditional
definitions of the previous species are made more strict. Cophylogenetic analysis
between the host family (Polytrichaceae) and Lizonia identifies some co-phylogentic
events where host evolution may have driven diversification in the parasite. However,
host-switch and duplication events were more frequent and more likely for the
majority of species, indicating that the primary force driving speciation in Lizonia is
the expansion and adaptation to new polytrichaceous hosts, a scenario that is
consistent with a relatively modern shift to bryophilous hosts, rather than an
evolutionarily long association.
Host-parasite coevolution in a domesticated world
Chaitanya Gokhale, MPI Plön
Host-parasite interactions are often studied in great detail both theoretically and
experimentally as standard example of co-evolutionary dynamics. When
domesticating animals or plants, via directed breeding or intensive agricultural
techniques, the genetic makeup of the organisms is being modified. Especially
focusing on plants and their pathogens, this can often neglect a major component
capable of modifying this co-evolutionary process, agriculture. This certainly has an
impact on the pathogens which have coevolved with these hosts of interest. Through
theoretical studies we analyse how the co-evolutionary process between plants and
their pathogens is affected by agriculture and how, unwittingly, we might be
domesticating not just the plants but their pathogens as well.
Evolutionary genomics and population genetic analyses of the Zymoseptoria species
complex
Christoph Eschenbrenner, Ines Braker, Jonathan Grandaubert, Eva H. Stukenbrock,
Christian-Albrechts University
One major biological thread for wheat production worldwide is the hemibiotrophic
fungal wheat pathogen Zymoseptoria tritici, the causal agent of Septoria tritici blotch
(STB). This highly specialized wheat pathogen causes high economical damages
worldwide. With three closely related wild grass pathogens Z. ardabiliae, Z.
pseudotritici and the recently identified Z. brevis, Z. tritici forms the Zymoseptoria
species complex. Their recent divergence on different hosts, make this species
complex an excellent model system for the analysis of pathogen speciation, species
evolution and host specialization. We here aim to link genome wide population
genetics parameters (Fixation index, FST and Tajima’s D) with patterns of positive
selection (gene-wise ratios of non- synonymous and synonymous substitutions,
dN/dS) assessed by maximum likelihood analyses in Z. tritici, Z. ardabiliae and Z.
brevis . This procedure will enable us to identify patterns of selection across genomes
within each species. Comparisons of positively selected genes in Z. brevis, Z.
ardabiliae and Z. tritici will provide insight into different genetic components
important for host specialization in these species. Genome wide analyses of Tajima’s
D will provide information about the impact of different demographic events on the
evolution of these pathogen species.
Genome Evolution of the Fungal Grass Pathogen Zymoseptoria pseudotritici
Ezgi Özkurt, MPI Plön
Hybridization is proposed to be a major force in the speciation of fungal plant
pathogens. The ascomycete grass pathogen Zymoseptoria pseudotritici emerged
recently from an interspecifc cross between yet unknown parental species. In a previous
study, the genomes of ve individuals of Z. pseudotritici were sequenced and revealed a
peculiar nucleotide diversity pattern: The genome consists of segments of high
nucleotide diversity but comprising only two diverged haplotypes. The other segments
comprising more than 40% of the genome are completely depleted of variation. This
particular genome structure results from a cross between only two parental individuals
that gave rise to a hybrid swarm that has recombined but never back-crossed to the
parental species. Z. pseudotritici provides a unique model system to study genomics of
a young hybrid species. Hence we set out to investigate patterns of selection and
distribution of derived mutations by sequencing additional 22 individuals. Re-analyzing
the new sequence alignment, we could confirm the diversity patterns of the genome as
found among only five individuals. We assessed the site frequency spectrum to further
investigate the distribution of variation in our population sample. The distribution of the
allele frequencies was found to be remarkably different from the pattern in close
relative species Z. tritici reflecting the different evolutionary histories of the species.
Moreover, we assessed genome-wide signatures of positive selection. Some of the
genes identified to be evolving under positive selection encode secreted proteins, and
are putative effector candidates involved in host-pathogen interactions. We are
currently applying additional analyses to estimate age the hybridization and the amount
of variation in the whole population.
Marine Fungi - identification, genomics and transcriptomics
Frank Kempken, Christian-Albrechts University
The number of species and distribution of marine fungi is largely unknown. Likewise
their role in marine ecology is mostly ignored so far. Yet, from a few model studies it
is clear that marine fungi provide a fresh resource for secondary metabolites, which
differs from terrestrial fungi. My research aims to identify cultivatable marine fungi
from marine sources, as this environment appears to contain many fungal species with
presumably unique adaptions to deep-sea conditions. While we are awaiting a large
sample set from the Mid-Atlantic ridge, we already did identify more than 60 fungal
species from 16 seafloor samples from the Baltic Sea. We analyzed secondary
metabolite genes of marine-derived fungi, including a marine sponge-derived fungal
strain of Scopulariopsis brevicaulis (Kumar et al., 2015) producing the anticancer
drugs scopularids A and B (Lukassen et al., 2015). Two fungi from the North Sea
mudflats, Calcarisporium sp. and Pestalotiopsis sp. contain 60 and 67 predicted
secondary metabolite gene clusters respectively. This is the highest number of
secondary metabolite gene clusters predicted so far (Kumar and Kempken, n.d.).
Likewise a very large number of secondary metabolite gene clusters was identified in
a Fusarium isolate from the Baltic Sea, that is currently under investigation as part of
an ITN EU project “QUANT FUNG” (Phule and Kempken, unpublished).