Genomic Comparisons of Two Armillaria Species with Different Ecological Behaviors and Their Associated Soil Microbial Communities

Abstract

Armillaria species show considerable variation in ecological roles and virulence, from mycorrhizae and saprophytes to important root pathogens of trees and horticultural crops. We studied two Armillaria species that can be found in coniferous forests of northwestern USA and southwestern Canada. Armillaria altimontana is considered as a weak, opportunistic pathogen of coniferous trees, but it also appears to exhibit in situ biological control against A. solidipes, formerly North American A. ostoyae, which is considered a virulent pathogen of coniferous trees. Here, we describe their genome assemblies and present a functional annotation of the predicted genes and proteins for the two Armillaria species that exhibit contrasting ecological roles. In addition, the soil microbial communities were examined in association with the two Armillaria species within a 45-year-old plantation of western white pine (Pinus monticola) in northern Idaho, USA, where A. altimontana was associated with improved tree growth and survival, while A. solidipes was associated with reduced growth and survival.ostoyae) is considered one of the more virulent pathogens [13], although virulence varies depending on isolate, host age and other factors [14]. Armillaria mellea and A. borealis are also considered virulent pathogens, while A. gallica, A. cepistipes, A. gemina, A. calvescens, A. sinapina, and A. nabsnona are considered less virulent or secondary pathogens [10, 12,15, 16]. A recently described species, Armillaria altimontana, formerly North American biological species (NABS) X, is also usually considered as a weak pathogen [17], but evidence for pathogenicity is not well documented [18]. Armillaria solidipes (as A. ostoyae) and A. altimontana have been documented to co-occur within forest stands in the inland northwestern USA [18][19][20]. A previous study in northern Idaho, USA provided evidence that A. altimontana can provide natural biological control of Armillaria root disease of western white pine (Pinus monticola) caused by A. solidipes. In this study, A. solidipes was uncommon in areas dominated by A. altimontana, and trees colonized by A. solidipes were associated with a lower growth and survival than trees colonized only by A. altimontana. The results demonstrated that A. altimontana was not harmful to western white pine within the northern Idaho planting site, and further suggest that A. altimontana behaves as a long-term, in situ biological control agent against A. solidipes [20]. Recognizing the genetic or underlying soil factors that drive host-fungal interactions may provide approaches for enhancing the management of Armillaria root disease.The distribution, life cycle, pathogenicity, and evolutionary relationships have been studied for several Armillaria species [10, 12,14, 16,[21][22][23][24][25]. Collins et al. [26] studied the genome and proteome of A. mellea, identifying carbohydrate degrading enzymes, laccases, and lignin peroxidases among other geneencoded proteins. characterized the transcriptome of an A. solidipe...

IMA genome‑F17

“…Various groups have conducted omics-based research on Armillaria species (Akulova et al 2020 ; Anderson et al 2018 ; Caballero et al 2022 ; Collins et al 2017 ; Collins et al 2013 ; Heinzelmann et al 2020 ; Kolesnikova et al 2019 ; Linnakoski et al 2021 ; Misiek et al 2011 ; Misiek and Hoffmeister 2012 ; Sipos et al 2017 ; Sonnenbichler et al 1997 ; Sun et al 2020 ; Wingfield et al 2016a , b ; Zhan et al 2020 ). These genomics, proteomics and metabolomics studies were done to gain insight into the molecular mechanisms and biochemical properties that drive the pathogenicity and virulence of Armillaria spp.…”

Genomic innovation and horizontal gene transfer shaped plant colonization and biomass degradation strategies of a globally prevalent fungal pathogen

“…To analyze the genomic innovations associated with the rise of Armillaria , we used genomes of 15 Armillaria species and 5 outgroups from the Physalacriaceae, which increased sampling density nearly four-fold compared to previous comparative studies 17, 25 . We combined these with those of other Agaricales exhibiting a range of lifestyles, resulting in a dataset of 66 species (Table S1).…”

“…Despite a well-documented epidemiology and etiology 2, 19, 21–24 , molecular aspects of the infection process are poorly known. Recent studies and genome sequencing efforts highlighted certain secondary metabolites, plant cell wall degrading enzymes (PCWDEs), chitin-binding proteins and expanded protein-coding repertoires enriched in putative pathogenicity-related genes, among others 1, 17, 18, 25–30 . It is likely that these previous findings only cover a fraction of the virulence genes of Armillaria , leaving much of its pathogenic arsenal yet to be characterized.…”

Fungal communities associated with early immature tubers of wild Gastrodia elata

“…Some Armillaria species were considered harmless (Przemieniecki et al., 2021 ) or not causing lethal diseases (Guo et al., 2016 ). A. altimontana was further shown to form a mutualistic symbiosis with western white pine ( Pinus monticola ) in northern Idaho, USA (Caballero et al., 2023 ), and A. luteo‐virens was considered an ectomycorrhizal symbiont in Qinghai‐Tibet Plateau, China (Xing et al., 2014 ). The third aspect was that Armillaria species suitable for symbiosis with G. elata were considered to be low pathogenic and similar in genetic and morphological characteristics, such as A. cepistipes and A. nabsnona , while A. mellea does not fit these characteristics (Guo et al., 2016 ), which was also supported by some of our unpublished results on rhizomorphs from the mature G. elata tubers.…”