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Abstract

The invasive alien pathogenic fungus Hymenoscyphus fraxineus causing ash dieback (ADB) has devastated European ash (Fraxinus excelsior) populations across Europe. Breeding for resistance is the most feasible measure to reduce future losses of ash, and the presence of resistance, albeit at low level, has been demonstrated in numerous genetic trials around Europe. This study is a continuation of the inventories tracking the vitality status of different clones, which started in 2006 at two ash seed orchards in southern Sweden. A new inventory conducted in the summer of 2021 revealed that the ten clones previously identified as the most tolerant to ADB based on periodic surveys from 2006 and onwards still remain the most tolerant, while susceptible clones continued to decline and are completely disappearing from the orchards. Browsing caused mortality in some of the most tolerant clones in one of the orchards during the last assessment period. Despite the animal damage, the stable resistance observed in tolerant clones over a 15 years period forms a solid basis for the continuation of the breeding programme where good candidates are selected for further study.
Forest Pathology. 2022;00:e12773. 
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https://doi.org/10.1111/efp.12773
wileyonlinelibrary.com/journal/efp
1 | INTRODUCTIO N
Hymenoscyphus fraxineus (T. Kowalski Baral, Queloz & Hosoya) is
an invasive fungal pathogen originating from East Asia where it is
seemingly non- pathogenic on native ash in its natural distribution
range (Cleary et al., 2016). The fungus is now widespread through-
out most of Europe and has dramatically reduced the host popu-
lation size of European ash (Fraxinus excelsior L.) in most countries.
Since ash is known as a keystone species in temperate broadleaved
forests and has huge importance for biodiversity, the continu-
ous loss of ash is expected to have negative ecological impacts of
other vulnerable ecosystem elements including a large number of
species that are highly dependent on ash in the landscape (Hultberg
et al., 2020).
Tolerance against the disease has been recorded in several
European ash populations where healthy trees have been observed
to survive well among the affected ones, showing relatively little die-
back damage (McKinney et al., 2014 and references within). The high
vitality of such trees has also been observed over longer periods.
Estimations of genetic heritability show that between 30 and
50% of the variation in tolerance to ADB may be explained by
genetic components of the host species (Plumb et al., 2020). In
Sweden, Stener (2013, 2018) surveyed two clonal seed orchards
5,10 and15 yearsaf terthefirstreportof ADB inthecountr yand
Received:23May2022 
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Revised:5September2022 
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Accepted:7September2022
DOI : 10.1111/efp.127 73
SHORT COMMUNICATION
Monitoring of long- term tolerance of European ash to
Hymenoscyphus fraxineus in clonal seed orchards in Sweden
Mateusz Liziniewicz1| Beatrice Tolio1,2 | Michelle Cleary2
This is an open access ar ticle under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited.
© 2022 The Authors. Forest Patholog y published by Wiley-VCH GmbH.
1Skogforsk - The Forestry Research
Institute of Sweden, Svalöv, Sweden
2Southern Swedish Forest Research
Centre, Swedish University of Agricultural
Sciences, Alnarp, Sweden
Correspondence
Mateusz Liziniewicz, Skogforsk - The
Forestry Research Institute of Sweden,
Ekebo 2250, 26890 Svalöv, Sweden.
Email: mateusz.liziniewicz@skogforsk.se
Funding information
Föreningen skogsträdförädling; Sveaskog
Abstract
The invasive alien pathogenic fungus Hymenoscyphus fraxineus causing ash dieback
(ADB) has devastated European ash (Fraxinus excelsior) populations across Europe.
Breeding for resistance is the most feasible measure to reduce future losses of ash,
and the presence of resistance, albeit at low level, has been demonstrated in nu-
merous genetic trials around Europe. This study is a continuation of the inventories
tracking the vitality status of different clones, which started in 2006 at two ash seed
orchards in southern Sweden. A new inventory conducted in the summer of 2021
revealed that the ten clones previously identified as the most tolerant to ADB based
on periodic surveys from 2006 and onwards still remain the most tolerant, while sus-
ceptible clones continued to decline and are completely disappearing from the or-
chards. Browsing caused mortality in some of the most tolerant clones in one of the
orchards during the last assessment period. Despite the animal damage, the stable
resistanceobservedin tolerantclones overa15 years period forms asolidbasis for
the continuation of the breeding programme where good candidates are selected for
further study.
KEY WORDS
disease type, disease type— shoot disease, fraxinus, host genus— dieback
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substantiated other European investigations reporting a large geno-
typic variation in susceptibility to ADB. The numerous reports show-
ing the genetic basis of resistance to ADB across Europe suggest
that selective breeding can mitigate the disease impact (McKinney
et al., 2014; Stener, 2013, 2018).
The main aim of this study was to investigate the stability of vi-
tality scores on F. excelsior clones in two seed orchards in southern
Sweden, with a special emphasis on the performance of tolerant
clones initially identified during earlier surveys. Knowledge about
stability of resistance is needed to validate the assumption of the
current breeding programmes that have been initiated in European
countries.
2 |MATERIALS AND METHODS
TwoseedorchardslocatedatSnogeholm(55°32′ N,13°32′ E,50 m)
andTrolleholm(55°57′ N,13°12′ E,100 m)insouthernSwedenwere
established in 1992 and 1995, respectively, to produce seeds for
commercial forestry purposes. The selection criteria for the clones
were growth and stem quality properties aiming to increase produc-
tion of valuable ash timber. There were 100 and 106 clones planted
in Snogeholm and Trolleholm, respectively. The clones came from
27 stands f rom souther n Sweden betwe en latitudes 55°41′ Nan d
58°02′ N.Thenumberoframetsperclonewasbetween40and60
at Snogeholm and up to 10 at Trolleholm.
Assessments of damage caused by ADB were initially con-
ducted in September 2006 and in the middle of August in 2007
at Snogeholm, and thereafter in 2010, 2011 and 2016 at both
Snogeholm and Trolleholm sites, as reported by Stener (2013, 2018).
There was also an inventory of living ramets done in Trolleholm in
1996, one year after planting.
In summer of 2021, assessment s of damage caused by ADB were
made according to the protocol of Stener (2018). Tree vitality was
scored using a scale from 1 to 9, where 1 indicated low vitality and 9
very good vitality. The crown damage was scored as a percentage of
crown dieback where class 0 indicated no damage, class 1 indicated
low damage (up to 10% of the crown exhibited dieback), and class
9 indicated very serious damage (up to 90% of the crown exhibited
dieback) (e.g. Figure 1a).
In addition, the occurrence of damage caused by fallow deer and
wild boar was recorded for all trees in Snogeholm. The type of dam-
age was scored as 0— no damage, 1— damage to the bark (layers of
periderm removed) and 2— damage to the vascular cambium (layers
of cambial tissue removed exposing underlying sapwood). Estimates
of damage severity were calculated as the per cent circumference of
girdling, in 10% classes (0%– 10%, 11%– 20% and so on).
In the analysis, the focus was on the overall long- term dynamics
of ADB symptoms including all clones in orchards as well as on mor-
tality of individuals among the ten most tolerant or most suscepti-
ble clones previously selected by Stener (2013, 2018). The selection
of tolerant, intermediate and susceptible clones was based on the
genetic breeding values known as best linear unbiased predictor
(BLUP) estimated for vitality and crown damage jointly for both or-
chards. For any tolerant tree that died, the cause of mortality was in-
vestigated to determine whether it was due to ADB or other factors.
The data from all available inventories are presented as descriptive
statistics and in figures.
3 |RESULTS AND DISCUSSION
The cumulative mortality for all clones between the first and last
assessm ent was 68% at Trolleholm (11 years af ter the firs t inven-
toryin2010)and89%atSnogeholm(15 yearsafterthefirstinven-
tory in 20 06), giving an average mortality rate of approximately 6%
annually. The rate of mortality was similar over the years in both
orchards (Figure 1b).Notsurprisingly,therelativemortalityratebe-
tween 2016 and 2021 decreased in comparison with the previous
assessment period (2011– 2016) as many susceptible genotypes had
already succumbed to the disease and the ongoing natural selec-
tion favours only the most tolerant individuals. At the last assess-
ment conducted in 2021, it was observed that 22 clones (21% of all
planted) at Trolleholm and 8 clones (8% of all planted) at Snogeholm
had died. Of these clones that died, three were common to both
orchards.
In the year 2021, for all clones, the mean number of living ramets
per clone was 3.3 ± 2.2 and2.3± 1.8 inSnogeholmandTrolleholm
seed orchards, respectively. Considering tolerant clones only,
the mean number of living ramets per clone was twofold higher;
6.5 ± 3.4inSnogeholmand4.5± 1.4inTrolleholm.
In the most recent assessment period (2016– 2021), the absolute
number of dead trees among the ten most tolerant clones previ-
ously identified by Stener (2013, 2018) varied between orchards. In
the summer of 2016, there were 89 and 50 living ‘tolerant’ ramets
at Snogeholm and Trolleholm, respectively. In the smaller orchard
(Trolleholm), four of the 50 ramets (8%) died in 2016. There, mor-
tality was registered for just two out of ten tolerant clones. In one
of those clones, three out of six ramets died and in the other clone
just one ramet died. Mor tality at Snogeholm was observed in seven
of the tolerant clones including the same two clones with observed
mortality at Trolleholm. For three clones, just one ramet died. In the
most extreme case, eight out of 13 ramets died. In total, 23 of 89 (or
approximately 26%) of living ‘tolerant’ ramets in 2016 died since the
last assessment (Figure 1c).
In general, the mortality among clones in the tolerant group was
associated with smaller tree size. The average diameter of all dead
treesinthisgroupwas127 ± 29 mm,whiletheaverageofallremain-
ingtreeswas195 ± 36 mmregardlessoftheseedorchard.
The average vitality score of the ten most tolerant clones fluc-
tuated slightly over time (Figure 1d), which may be attributable to
temporal variability in damage severity related to variable weather
conditions across seasons, especially precipitation that is an im-
portant factor for ash vitality. On the contrary, the scores had not
shifted more than one grade in the nine- grade scale over the years
(Figure 1d). There were some clones that had a score close to the
   
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LIZINIEWICZ et al.
average score for other intermediate living clones. Some within-
clone variation was evident across phenotype groups. In 2021,
the mean vitality scores of the remaining intermediate/suscepti-
ble clones were relatively high in both seed orchards (6.2 and 7.5
at Snogeholm and Trolleholm, respectively) compared with the ten
most tolerant clones. However, the average number of living ramets
for these intermediate/susceptible clones was three with 42 clones
having only one or two living ramets, which had a great effect on the
calculated mean.
Some variation may have also occurred between assessment
years due to subjectivity in the assessment that was conducted by
different people. Among the 23 ‘tolerant’ ramets that died between
2016 and 2021 at both seed orchards, 16 were characterized as hav-
ing highest vitality scores (8 or 9) in 2016.
From the time of the first available inventory, cumulative mortal-
ity of ramets belonging to the group of ten most tolerant clones was
66% and 39% in Snogeholm and Trolleholm, respectively. Most of
this mortality should be attributed to ADB. However, at Snogeholm,
other causes, namely fallow deer and wild boar, damaged large por-
tions of the main stem causing direct mor tality by girdling, but also
indirectly contributed to mortality by inducing stress over several
years of continuous browsing. Animal damage was observed on 84%
(n = 296) of trees at Snogeholm after the opening of the fence in
2018. Of those, about 41% (n = 144) had only minor bark damage
with removal of the periderm and some inner phloem, while 43%
(n = 152) had severe damage to the stem with complete removal of
the bark and vascular cambium. Exposed wounds were up to 1 m in
length on the stem, affecting approximately 40% of stem circumfer-
ence. In the group of ten most tolerant clones, for 14 ramets (out of
23 that were recorded to have died during the period 2016– 2021),
animal damage was determined to be the main reason for mortality.
NobrowsingdamagewasobservedatTrolleholm.In somepartsof
the seed orchard at Snogeholm, natural regeneration filled in gaps
created by the loss of ash trees. In some cases, the naturally regen-
erated trees have caused significant competition to ash, overshad-
owing its tree crowns. Some stand management activities have been
carried out at both seed orchards to remove this competing vege-
tation and at the same time some ash trees, which were deemed to
have poor vitality could also have been removed.
Between 2006 and 2016, 89% (160 out of 180) of ramets rep-
resenting the 10 most susceptible clones according to Stener (2013,
2018) died; 103 at Snogeholm and 57 at Trolleholm. Of the 20
FIGURE 1 (a)Representativesofsusceptible(left)andtolerant(right)ashclonesatTrolleholmseedorchard,(b)Changesinmortalit yrate
over time from the first assessments in Snogeholm (red) and Trolleholm (blue) seed orchards, (c) the number of living ramets of the ten most
tolerant clones (red and solid lines), the ten most susceptible (black and solid lines) and clones with intermediate susceptibility (grey and
dashed lines) (d) the vitality score of ten best (most tolerant) clones in both seed orchards at the different assessments conducted between
2011 and 2021; here, lines of different colours represent different clones; the dashed line shows the average vitality score of all living clones
with intermediate susceptibility.
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susceptible ramets remaining in 2016, 9 died during the last assess-
ment period and only 11 ramets remained, three susceptible clones
with each two ramets and five clone with just one ramet each.
The long- term monitoring of the oldest genetic trial of European
ash in Sweden indicate that there is considerable within- clone vari-
ation in tolerance to ADB. At both Snogeholm and Trolleholm, there
was continued mortality of clones previously identified as being ge-
netically superior due to low severity of damage caused by ADB,
albeit at a ver y low level compared with susceptible clones.
Careful monitoring of other mortality agents should be imple-
mented in future assessments to improve tolerance assessments.
In forests in Sweden, species of Armillaria are opportunistic on the
roots of diseased ash trees, causing decay and increasing tree sus-
ceptibility to windthrow. Observations from annual field surveys in
ashforestsinSwedenduringthelast10 yearssuggesttheincidence
of root infection caused by Armillaria spp., and tree mortality as a
result of girdling of mycelial fans at the root collar and/or subsequent
windthrow is increasing. Both seed orchards in this study are, how-
ever, located on former agricultural land where Armillaria spp. are
less prevalent and the main contributing mortality factor appears
to be animals. Contributing agents of mortality other than ADB
represent a potential problem for the breeding programme where
long- term tolerance stability to ADB is needed to secure the estab-
lishment of a tolerant breeding population.
ACKNOWLEDGEMENTS
The inventor y of the seed orchards has been done with the finan-
cial support of the Föreningen skogsträdförädling (project 20- 448
Uppföljning av förädling för motståndskraft mot askskottsjuka). The
project was also financially suppor ted by Sveaskog within the frame-
work of the project aimed at ash and elm preservation.
DATA AVAIL ABILI TY STATEMENT
The data that support the findings of this study are available from
the corresponding author upon reasonable request.
ORCID
Beatrice Tolio https://orcid.org/0000-0002-3137-3040
Michelle Cleary https://orcid.org/0000-0002-0318-5974
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How to cite this article: Liziniewicz, M., Tolio, B., & Cleary, M.
(2022). Monitoring of long- term tolerance of European ash to
Hymenoscyphus fraxineus in clonal seed orchards in Sweden.
Forest Pathology, 00, e12773. https://doi .org/10.1111/
efp.12773
... However, the successful growth of ash seedlings and juveniles into healthy adults depends on the combination of genetic, abiotic, and biotic factors and their interactions. If these juveniles grow into healthy adults, their tolerance should endure (Liziniewicz et al., 2022). Therefore, allowing ash dieback to "run its course" without human intervention aligns with the concept of natural selection, favouring trees with high disease tolerance (Skovsgaard et al., 2017). ...
... Dynamic ex situ conservation units could be the logical consequence from any ash breeding program aiming to produce forest reproductive material with higher resilience against ash dieback (e.g. Liziniewicz et al., 2022), because it would allow to assemble fieldresistant mother trees on a relatively small area in order to increase cross-pollination and panmixia. The strength of this approach clearly lies in the ability to control effective population size without much monitoring effort by making sure that seed is only harvested when a minimum number of trees is flowering or bearing seed. ...
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... Dynamic ex situ conservation units could be the logical consequence from any ash breeding program aiming to produce forest reproductive material with higher resilience against ash dieback (e.g. Liziniewicz et al. 2022), because it would allow to assemble field-resistant mother trees on a relatively small area in order to increase cross-pollination and panmixia. The strength of this approach clearly lies in the ability to control effective population size without much monitoring effort by making sure that seed is only harvested when a minimum number of trees is flowering or bearing seed. ...
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Ash dieback (ADB) is threatening populations of European ash (Fraxinus excelsior & F. angustifolia) for more than three decades. Although much knowledge has been gathered in the recent past, practical conservation measures have been mostly implemented at local scale. Since range contraction in both ash species will be exacerbated in the near future by westward expansion of the emerald ash borer and climate change, systematic conservation frameworks need to be developed to avoid long-term population-genetic consequences and depletion of genomic diversity. In this article, we address the advantages and obstacles of conservation approaches aiming to conserve genetic diversity in-situ or ex-situ during tree pandemics. We are reviewing 47 studies which were published on ash dieback to unravel three important dimensions of ongoing conservation approaches or perceived conservation problems: i) conservation philosophy (i.e. natural selection, resistance breeding or genetic conservation), ii) the spatial scale (ecosystem, country, continent), and iii) the integration of genetic safety margins in conservation planning. Although nearly equal proportions of the reviewed studies mention breeding or active conservation as possible long-term solutions, only 17% consider that additional threats exist which may further reduce genetic diversity in both ash species. We also identify and discuss several knowledge gaps and limitations which may have limited the initiation of conservation projects at national and international level so far. Finally, we demonstrate that there is not much time left for filling these gaps, because European-wide forest health monitoring data indicates a significant decline of ash populations in the last 5 years.
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... The Save the Ash Citizen Science program 11 in Sweden aimed to encourage citizens to help locate rare "vital" ash trees within landscapes devastated by ash dieback. European ash populations have been significantly reduced following the introduction of the non-native fungus Hymenoscyphus fraxineus, and in Sweden the tree species is endangered (Hultberg et al., 2020), though a small proportion of the natural population shows high resistance to the disease Liziniewicz et al., 2022). Citizen participation was ideal for identifying resistant phenotypes for breeding because ash in Sweden is found at very low proportions within forests (<1% of the forest inventory stock), usually mixed with other temperate broadleaved tree species, and is sparsely distributed across the country . ...
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Common ash ( Fraxinus excelsior L.) is a keystone tree species in Europe. However, since the 1990s, this species has been experiencing widespread decline and mortality due to ash dieback [ Hymenoscyphus fraxineus (T. Kowalski) Baral, Queloz and Hosoya]. Besides H. fraxineus , emerald ash borer ( Agrilus planipennis Fairmaire), an invasive alien pest already devastating ash trees in western Russia, is spreading westward and becoming an emerging threat to the remaining European ash populations. While efforts to control ash dieback continue to be a priority, it is becoming crucial to compensate for the loss of ash and its ecosystem services by elaborating restoration strategies, including the search for alternative native and non-native tree species. This review summarizes available knowledge on potential alternative tree species to common ash to help forest managers to cope with ash dieback. Although using natural regeneration and promoting tree species diversity can reduce the impacts of ash dieback in European forests, our review indicates that no native species alone or in combination can fully replace the ecological niche of common ash and its associated ecosystem services (e.g., biodiversity and timber). To fill this gap, forest managers have considered using non-native ash species that are tolerant to both H. fraxineus and A. planipennis and have similar ecological and forestry values as common ash. Of the 43 ash species reviewed, few non-native ash species (e.g., Fraxinus mandshurica Rupr. and Fraxinus platypoda Oliv.) have similar ecological characteristics to common ash and are tolerant to H. fraxineus and A. planipennis . However, the performance of non-native ash species in European forests, their invasiveness potential, and the risk of hybridization with native ash species are still unknown. With the current state of knowledge, it is thus too early to recommend the use of non-native ash species as a suitable option to deal with ash dieback. The priority should be the conservation, regeneration, and breeding of tolerant common ash populations to H. fraxineus , as well as the use of the natural regeneration of other native tree species. Our review highlights the need for controlled experimental plantations to better understand the regeneration ecology and invasiveness potential of non-native ash species prior to their utilization in natural forests.
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Large-scale decline in populations of European ash (Fraxinus excelsior) are occurring throughout Europe due to the invasive fungus Hymenoscyphus fraxineus. This has grave ecological implications not only for ash trees, but also for the biodiversity supported by, and in some cases solely dependent on ash. Here we used data on the tree-species associations of biodiversity in Sweden, to predict extinction risks for ash-associated organisms, and the potential for combinations of other tree species to sustain ash-associated biodiversity. Of the 483 ash-associated species identified, 11% are exclusive to ash, and a further 23% prefer mainly ash. Notably, many ash-associated species are shared with wych elm (Ulmus glabra) which is similarly threatened by an invasive fungus. Considering the level of host association and the species' conservation status, 115 species were deemed at high risk of regional extinction. Using a mathematical optimization model we found that up to nine additional tree species would be needed to sustain all non-obligate ash dependent/preferring species in the absence of ash and elm. We discuss mitigation and adaption options to reduce the potential for an extinction cascade and conserve ash-associated biodiversity, but all pose unique challenges.
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Societal Impact Statement The current ash dieback epidemic in Europe caused by Hymenoscyphus fraxineus poses a key question to policy makers: whether or not to commit time and resources to the initiation of a breeding programme for the development of more resistant ash, as a long‐term policy of adaptation to the epidemic. Here we review current evidence on the potential viability of such a programme, from a biological perspective. We conclude that a breeding programme for ash aimed at resistance to current strains of H. fraxineus in the British Isles is biologically feasible. Summary To evaluate the viability and feasibility of a future breeding programme to produce trees resistant to an emerging pest or pathogen, it is helpful to ask the following questions: How much variation in resistance exists in tree populations? To what extent is this resistance heritable? How many genetic loci are involved? What level of resistance is found in other species of the same genus? Here, we survey current knowledge of these issues in relation to the degree of resistance of European ash (Fraxinus excelsior) to H. fraxineus, the fungus causing ash dieback (ADB). Several studies have found a low frequency of heritable resistance in F. excelsior populations, which seems to be determined by many genetic loci. This suggests that a breeding programme is viable and that natural selection may also increase the mean resistance of populations over time. More research is needed on the genetic basis of resistance to ADB to understand how quickly natural selection can operate in woodlands and what acceleration may be possible in breeding programmes, including via use of genetic markers. Hybrid breeding programmes may also be a possibility, as some ash species appear to be more resistant to ADB than is F. excelsior, but more research is needed on this issue. We do not yet know if it will be possible to breed F. excelsior to have resistance to both ADB and the emerging threat of emerald ash borer. We recommend short‐term mitigation measures for the ADB epidemic and future research directions.
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Hymenoscyphus fraxineus, an introduced ascomycete fungus and primary causal agent of European ash dieback, was investigated on Fraxinus mandshurica trees in its native range in Primorye region of Far East Russia. This evidence is the first report of H. fraxineus on healthy, asymptomatic F. mandshurica trees. High-throughput sequencing revealed 49 distinct fungal taxa associated with leaves of F. mandshurica, 12 of which were identified to species level. Phyllosphere fungal assemblages were similar among sites despite being largely geographically distant. Many organisms comprising the foliar fungal community on F. mandshurica in Far East Russia have similarity to those reported inhabiting F. excelsior in Europe based on previous studies. However, Mycosphaerella sp., the most dominant species in this study and detected in nearly all samples, was associated only with F. mandshurica. Genetic diversity of H. fraxineus was significantly higher in the Far East Russian population than in Europe. In contrast to its aggressive behaviour on Fraxinus excelsior in Europe, H. fraxineus appears to be a benign associate of indigenous F. mandshurica that initially induces quiescent and asymptomatic infections in healthy trees prior to active host colonization normally associated with modification of host tissue during senescence.
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Damage caused by Hymenoscyphus fraxineus, the causal agent of ash dieback, was genetically evaluated based on scorings made on five occasions during the years 2006–2016 at two seed orchards of ash (Fraxinus excelsior L.) established in southern Sweden in 1992 and 1995, respectively. The studied population included grafts originating from 106 plus-tree clones selected from 27 stands in southern Sweden. The study verified previous results of (1) high genetic control of damage traits, (2) high genotypic variation in disease susceptibility and (3) that only a small proportion of the natural population are at least partly resistant. The clonal response for dieback damage was stable over the 10-year period, i.e. the least susceptible clones selected in 2006 still belong to the healthiest ones after several years of heavy infection pressure. There were no clear trends in the development of damage over time for trees being alive at each assessment. However, the proportion of trees that died was substantial (7–8% per year), but this estimation was influenced by other factors than the disease, such as wild game and sanitary cuttings. Altogether, the results are promising for initiating breeding programs to improve the dieback resistance. However, this is a heavy and costly task, since only a very small proportion of the ash trees are partially resistant to the dieback disease. Thus, a joint breeding program involving all the northern European countries is justified.
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Over the last two decades, ash dieback has become a major problem in Europe, where the causative fungus has invaded the continent rapidly. The disease is caused by the invasive pathogenic fungus Hymenoscyphus pseudoalbidus (anamorph Chalara fraxinea), which causes severe symptoms and dieback in common ash, Fraxinus excelsior. It is becoming a significant threat to biodiversity in forest ecosystems and the economic and aesthetic impacts are immense. Despite the presence of the disease for at least 10 years in Scandinavia, a small fraction of F. excelsior trees have remained vigorous, and these trees exhibit no or low levels of symptoms even where neighbouring trees are very sick. This gives hope that a fraction of the ash trees will retain a sufficiently viable growth to survive. Following a period of high mortality in natural populations, selection and breeding of remaining viable ash trees could therefore provide a route for restoring the role of ash in the landscape. This paper reviews the available data on disease dissemination, and the consequences thereof in terms of symptom severity and mortality, and appraises studies that have tested the hypothesis that less affected trees have genetically based resistance. We discuss the implications of the results for the adaptive potential of common ash to respond to the disease through natural or assisted selection. We consider the risks of adverse fitness effects of population fragmentation due to high mortality. Finally, we recommend that resistant trees (genotypes) should be selected to facilitate conservation of the species. This article is protected by copyright. All rights reserved.
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Ash dieback damage was assessed and analysed on 16–22 year-old grafts in two ash seed orchards (Fraxinus excelsior L.). The grafts originated from 106 plus-tree clones selected from 27 stands in southern Sweden based on their phenotypes. The results obtained indicate that ash dieback disease is strongly genotypically controlled. There was considerable genotypic variation among individuals. None of the clones seemed to be totally resistant, but some exhibited reduced susceptibility and retained this resistance after 6 years under heavy infection pressure. Autumn phenology based on leaf coloration was subject to moderate genetic control (H 2 = 0.19). The genetic correlation between autumn phenology and damage was weak to moderate (r G from 0.38 to 0.60) and positive, indicating that susceptible clones have a prolonged growing season. There was no evidence suggesting that stands differed in susceptibility. Together with the high heritability of resistance, strong age×age correlations and weak genotype×environment interactions, this suggests there is good scope for breeding less susceptible trees for the future.