Abstract:This review considers current knowledge surrounding species boundaries of the Armillaria root-rot pathogens and their distribution. In addition, a phylogenetic tree using translation elongation factor subunit 1-alpha (tef-1α) from isolates across the globe are used to present a global phylogenetic framework for the genus. Defining species boundaries based on DNA sequence-inferred phylogenies has been a central focus of contemporary mycology. The results of such studies have in many cases resolved the biogeogra… Show more
“…A. solidipes grouped with A. borealis, while A. sinapina and A. gallica seemed to be more distantly related. The protein changes are consistent with the established phylogenetic relationships of the four species [48, 49]. Fig.…”
Section: Resultssupporting
confidence: 87%
“…In A. sinapina the cox3 and atp6 genes were transposed and rearranged. The rearrangements are consistent with A. borealis and A. solidipes being sister species and A. sinapina and A. gallica being more distantly related [48, 49].…”
Background
Species in the genus
Armillaria
(fungi, basidiomycota) are well-known as saprophytes and pathogens on plants. Many of them cause white-rot root disease in diverse woody plants worldwide. Mitochondrial genomes (mitogenomes) are widely used in evolutionary and population studies, but despite the importance and wide distribution of
Armillaria
, the complete mitogenomes have not previously been reported for this genus. Meanwhile, the well-supported phylogeny of
Armillaria
species provides an excellent framework in which to study variation in mitogenomes and how they have evolved over time.
Results
Here we completely sequenced, assembled, and annotated the circular mitogenomes of four species:
A. borealis, A. gallica
,
A. sinapina,
and
A. solidipes
(116,443, 98,896, 103,563, and 122,167 bp, respectively). The variation in mitogenome size can be explained by variable numbers of mobile genetic elements, introns, and plasmid-related sequences. Most
Armillaria
introns contained open reading frames (ORFs) that are related to homing endonucleases of the LAGLIDADG and GIY-YIG families. Insertions of mobile elements were also evident as fragments of plasmid-related sequences in
Armillaria
mitogenomes. We also found several truncated gene duplications in all four mitogenomes.
Conclusions
Our study showed that fungal mitogenomes have a high degree of variation in size, gene content, and genomic organization even among closely related species of
Armillara
. We suggest that mobile genetic elements invading introns and intergenic sequences in the
Armillaria
mitogenomes have played a significant role in shaping their genome structure. The mitogenome changes we describe here are consistent with widely accepted phylogenetic relationships among the four species.
Electronic supplementary material
The online version of this article (10.1186/s12864-019-5732-z) contains supplementary material, which is available to authorized users.
“…A. solidipes grouped with A. borealis, while A. sinapina and A. gallica seemed to be more distantly related. The protein changes are consistent with the established phylogenetic relationships of the four species [48, 49]. Fig.…”
Section: Resultssupporting
confidence: 87%
“…In A. sinapina the cox3 and atp6 genes were transposed and rearranged. The rearrangements are consistent with A. borealis and A. solidipes being sister species and A. sinapina and A. gallica being more distantly related [48, 49].…”
Background
Species in the genus
Armillaria
(fungi, basidiomycota) are well-known as saprophytes and pathogens on plants. Many of them cause white-rot root disease in diverse woody plants worldwide. Mitochondrial genomes (mitogenomes) are widely used in evolutionary and population studies, but despite the importance and wide distribution of
Armillaria
, the complete mitogenomes have not previously been reported for this genus. Meanwhile, the well-supported phylogeny of
Armillaria
species provides an excellent framework in which to study variation in mitogenomes and how they have evolved over time.
Results
Here we completely sequenced, assembled, and annotated the circular mitogenomes of four species:
A. borealis, A. gallica
,
A. sinapina,
and
A. solidipes
(116,443, 98,896, 103,563, and 122,167 bp, respectively). The variation in mitogenome size can be explained by variable numbers of mobile genetic elements, introns, and plasmid-related sequences. Most
Armillaria
introns contained open reading frames (ORFs) that are related to homing endonucleases of the LAGLIDADG and GIY-YIG families. Insertions of mobile elements were also evident as fragments of plasmid-related sequences in
Armillaria
mitogenomes. We also found several truncated gene duplications in all four mitogenomes.
Conclusions
Our study showed that fungal mitogenomes have a high degree of variation in size, gene content, and genomic organization even among closely related species of
Armillara
. We suggest that mobile genetic elements invading introns and intergenic sequences in the
Armillaria
mitogenomes have played a significant role in shaping their genome structure. The mitogenome changes we describe here are consistent with widely accepted phylogenetic relationships among the four species.
Electronic supplementary material
The online version of this article (10.1186/s12864-019-5732-z) contains supplementary material, which is available to authorized users.
“…Basidiomycetes provide a rich source of complex, structurally diverse, and bioactive sesquiterpenoids, and certain protoilludene-type sesquiterpene aryl esters produced by the genus Armillaria (class Agaricomycetes, family Physalacriaceae) are promising leads for the development of new drugs. There are~130 Armillaria species, most of which are root pathogens that attack hardwood trees, conifers, fruit trees, and grapevines, thus threatening both timber and agronomic plantations (Kile et al 1994;Baumgartner et al 2011;Coetzee et al 2018). Most Armillaria species are facultative necrotrophs, with parasitic and saprotrophic phases (Rishbeth 1985).…”
Melleolides and armillyl orsellinates are protoilludene-type aryl esters that are synthesized exclusively by parasitic fungi of the globally distributed genus Armillaria (Agaricomycetes, Physalacriaceae). Several of these compounds show potent antimicrobial and cytotoxic activities, making them promising leads for the development of new antibiotics or drugs for the treatment of cancer. We recently cloned and characterized the Armillaria gallica gene Pro1 encoding protoilludene synthase, a sesquiterpene cyclase catalyzing the pathway-committing step to all protoilludene-type aryl esters. Fungal enzymes representing secondary metabolic pathways are sometimes encoded by gene clusters, so we hypothesized that the missing steps in the pathway to melleolides and armillyl orsellinates might be identified by cloning the genes surrounding Pro1. Here we report the isolation of an A. gallica gene cluster encoding protoilludene synthase and four cytochrome P450 monooxygenases. Heterologous expression and functional analysis resulted in the identification of protoilludene-8α-hydroxylase, which catalyzes the first committed step in the armillyl orsellinate pathway. This confirms that ∆-6-protoilludene is a precursor for the synthesis of both melleolides and armillyl orsellinates, but the two pathways already branch at the level of the first oxygenation step. Our results provide insight into the synthesis of these valuable natural products and pave the way for their production by metabolic engineering.
Key points
• Protoilludene-type aryl esters are bioactive metabolites produced by Armillaria spp.
• The pathway-committing step to these compounds is catalyzed by protoilludene synthase.
• We characterized CYP-type enzymes in the cluster and identified novel intermediates.
“…The basidiomycete genus Armillaria plays a very important role in forest ecosystems worldwide and currently includes more than 40 officially described species [2,3]. Armillaria species differ significantly in virulence, for example, some species, such as A. ostoyae, are the main cause of tree death while other species colonize plants already damaged by various factors (drought, pests, etc.)…”
Section: Introductionmentioning
confidence: 99%
“…They attack hundreds of different tree species (e.g., Abies, Picea, Pinus, Betula, Sorbus, Juglans, Malus, etc.) in both hemispheres under different climatic conditions, and are among the most destructive forest pathogens [2,14,15].…”
Background
Massive forest decline has been observed almost everywhere as a result of negative anthropogenic and climatic effects, which can interact with pests, fungi and other phytopathogens and aggravate their effects. Climatic changes can weaken trees and make fungi, such as Armillaria more destructive. Armillaria borealis (Marxm. & Korhonen) is a fungus from the Physalacriaceae family (Basidiomycota) widely distributed in Eurasia, including Siberia and the Far East. Species from this genus cause the root white rot disease that weakens and often kills woody plants. However, little is known about ecological behavior and genetics of A. borealis. According to field research data, A. borealis is less pathogenic than A. ostoyae, and its aggressive behavior is quite rare. Mainly A. borealis behaves as a secondary pathogen killing trees already weakened by other factors. However, changing environment might cause unpredictable effects in fungus behavior.
Results
The de novo genome assembly and annotation were performed for the A. borealis species for the first time and presented in this study. The A. borealis genome assembly contained ~ 68 Mbp and was comparable with ~ 60 and ~ 79.5 Mbp for the A. ostoyae and A. mellea genomes, respectively. The N50 for contigs equaled 50,544 bp. Functional annotation analysis revealed 21,969 protein coding genes and provided data for further comparative analysis. Repetitive sequences were also identified. The main focus for further study and comparative analysis will be on the enzymes and regulatory factors associated with pathogenicity.
Conclusions
Pathogenic fungi such as Armillaria are currently one of the main problems in forest conservation. A comprehensive study of these species and their pathogenicity is of great importance and needs good genomic resources. The assembled genome of A. borealis presented in this study is of sufficiently good quality for further detailed comparative study on the composition of enzymes in other Armillaria species. There is also a fundamental problem with the identification and classification of species of the Armillaria genus, where the study of repetitive sequences in the genomes of basidiomycetes and their comparative analysis will help us identify more accurately taxonomy of these species and reveal their evolutionary relationships.
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