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Transcriptional responses in developing lesions of European common ash (Fraxinus excelsior) reveal genes responding to infection by Hymenoscyphus fraxineus.

ABSTRACT: BACKGROUND:With the expanding ash dieback epidemic that has spread across the European continent, an improved functional understanding of the disease development in afflicted hosts is needed. The study investigated whether differences in necrosis extension between common ash (Fraxinus excelsior) trees with different levels of susceptibility to the fungus Hymenoscyphus fraxineus are associated with, and can be explained by, the differences in gene expression patterns. We inoculated seemingly healthy branches of each of two resistant and susceptible ash genotypes with H. fraxineus grown in a common garden. RESULTS:Ten months after the inoculation, the length of necrosis on the resistant genotypes were shorter than on the susceptible genotypes. RNA sequencing of bark samples collected at the border of necrotic lesions and from healthy tissues distal to the lesion revealed relatively limited differences in gene expression patterns between susceptible and resistant genotypes. At the necrosis front, only 138 transcripts were differentially expressed between the genotype categories while 1082 were differentially expressed in distal, non-symptomatic tissues. Among these differentially expressed genes, several genes in the mevalonate (MVA) and iridoid pathways were found to be co-regulated, possibly indicating increased fluxes through these pathways in response to H. fraxineus. Comparison of transcriptional responses of symptomatic and non-symptomatic ash in a controlled greenhouse experiment revealed a relatively small set of genes that were differentially and concordantly expressed in both studies. This gene-set included the rate-limiting enzyme in the MVA pathway and a number of transcription factors. Furthermore, several of the concordantly expressed candidate genes show significant similarity to genes encoding players in the abscisic acid- or Jasmonate-signalling pathways. CONCLUSIONS:A set of candidate genes, concordantly expressed between field and greenhouse experiments, was identified. The candidates are associated with hormone signalling and specialized metabolite biosynthesis pathways indicating the involvement of these pathways in the response of the host to infection by H. fraxineus.

SUBMITTER: Sahraei SE

PROVIDER: S-EPMC7541206 | biostudies-literature | 2020 Oct

REPOSITORIES: biostudies-literature

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Transcriptional responses in developing lesions of European common ash (Fraxinus excelsior) reveal genes responding to infection by Hymenoscyphus fraxineus.

Sahraei Shadi Eshghi SE Cleary Michelle M Stenlid Jan J Brandström Durling Mikael M Elfstrand Malin M

BMC plant biology 20201006 1

<h4>Background</h4>With the expanding ash dieback epidemic that has spread across the European continent, an improved functional understanding of the disease development in afflicted hosts is needed. The study investigated whether differences in necrosis extension between common ash (Fraxinus excelsior) trees with different levels of susceptibility to the fungus Hymenoscyphus fraxineus are associated with, and can be explained by, the differences in gene expression patterns. We inoculated seemin ...[more]

PMID: 33023496

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Project description:BackgroundKnowledge of genetic structure and the factors that shape it has an impact on forest management practices. European ash (Fraxinus excelsior L.) has declined dramatically throughout its range as a result of a disease caused by the fungus Hymenoscyphus fraxineus. Despite the need for conservation and restoration of the species, genetic data required to guide these efforts at the country level are scarce. Thereofore, we studied the chloroplast and nuclear genetic diversity of 26 natural common ash populations (1269 trees) in Poland.ResultsChloroplast polymorphisms grouped the populations into two geographically structured phylogenetic lineages ascribed to different glacial refugia (the Balkans and the Eastern Alps). However, the populations demonstrated high genetic diversity (mean AR = 12.35; mean Ho = 0.769; mean He = 0.542) but low differentiation based on nuclear microsatellites (FST = 0.045). Significant spatial genetic structure, consistent with models of isolation by distance, was detected in 14 out of 23 populations. Estimated effective population size was moderate-to-high, with a harmonic mean of 57.5 individuals per population.ConclusionsGenetic diversity was not homogeneously distributed among populations within phylogenetic gene pools, indicating that ash populations are not equal as potential sources of reproductive material. Genetic differences among populations could be related to their histories, including founder effects or gene flow between evolutionary lineages (admixture). Our results suggest that ash stands across Poland could be treated as two main management units (seed zones). Therefore, despite the homogenizing effect of pollen gene flow known for this species, the genetic structure should be taken into account in the management of the genetic resources of the common ash. Although ash dieback poses an additional challenge for the management of genetic resources, efforts should be directed towards protecting populations with high genetic diversity within defined phylogenetic units, as they may be an important source of adaptive variation for future stands.

Project description:Five species of Hymenoscyphus that fruit on black stromatized parts of dead leaves of deciduous trees are presented, giving details on their morphological and ecological characteristics. Several of these species have previously been misplaced in rutstroemiaceous genera because of the presence of a substratal stroma. However, the heteropolar, scutuloid ascospores with an often hook-like lateral protrusion at the rounded apex and the ascus apical ring of the Hymenoscyphus-type represent two reliable morphological characteristics that, together with molecular data, provide clear evidence for their placement in the genus Hymenoscyphus (Helotiaceae). Among the species treated is Hymenoscyphus fraxineus (=Hymenoscyphus pseudoalbidus), the causal agent of the European ash dieback disease. Since 1992 this species started within Europe to replace the rather uncommon Hymenoscyphus albidus, which is likewise confined to leaves of Fraxinus. Hy. fraxineus has been recorded already since 1990 in Eastern Asia (Japan, Korea, northeast of China), where it had been initially misidentified as Lambertella albida (?Hy. albidus). In these regions, it occurs as a harmless saprotroph on Fraxinus mandshurica and Fraxinus rhynchophylla, suggesting that those populations are native while the European ash dieback disease has a recent Eastern Asiatic origin. The distinctly higher genetic diversity found in Japanese Hy. fraxineus in contrast to European Hy. fraxineus supports this view. Genetic similarities between Japanese Hy. fraxineus and European Hy. albidus suggest that also Hy. albidus might be a descendant of Asian Hy. fraxineus, though having invaded Europe much earlier. However, consistent genetic deviation between European and Asian Hy. fraxineus at two nucleotide positions of the ITS region indicates that the European ash disease originates from a region different from the presently known areas in Eastern Asia. Our results underline the importance of detailed morphological studies in combination with molecular work. Hy. fraxineus was described from Europe as a cryptic species that differed from Hy. albidus by molecular data alone. However, the Hy. albidus/Hy. fraxineus species complex represents one of many examples within the ascomycetes in which subtle microscopic differences between closely related species, in this case the presence or absence of croziers at the ascus base, are strictly correlated with molecular characteristics. Two species that closely resemble Hy. albidus and Hy. fraxineus form pseudosclerotia in Aesculus leaves and again differ from each other mainly in the ascus base: Hymenoscyphus aesculi on Aesculus hippocastanum from Europe lacks croziers, whereas Hymenoscyphus honshuanus from Japan on Aesculus turbinata possesses croziers. Other taxa treated here include Hymenoscyphus vacini, a European species growing on stromatized net veins of skeletonized leaves of Acer, and Hymenoscyphus torquatus, a Chinese species on unidentified herbaceous stems. An equivalent stroma-forming North American species on leaves of Fraxinus, Rutstroemia longipes (Rutstroemiaceae), is discussed and compared. A key to the Hymenoscyphus species that form a dark stroma on leaves of Acer, Aesculus, Fraxinus, and Picrasma is provided.

Dataset Information

Transcriptional responses in developing lesions of European common ash (Fraxinus excelsior) reveal genes responding to infection by Hymenoscyphus fraxineus.

Publications

Transcriptional responses in developing lesions of European common ash (Fraxinus excelsior) reveal genes responding to infection by Hymenoscyphus fraxineus.

Similar Datasets

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