Abstract:The mutualism between siricid woodwasps and Amylostereum fungal symbionts has long been considered to be species-specific. Recent studies from North America have challenged this assumption, where native siricids and the introduced Sirex noctilio are clearly swapping symbionts. Whether this pattern is a consequence of invasion or an underappreciated property of siricid biology is unknown. Here we show that the native Japanese siricid, Sirex nitobei, carries both Amylostereum areolatum and Amylostereum chailleti… Show more
“…Here, we describe trends in genomic architecture and gene content in twenty representative species of Russulales. Our dataset contains fourteen previously unanalyzed genomes, including 11 species of ECM Russulaceae and their saprotrophic sister group ( Gloeopeniophorella convolvens ), and Amylostereum chailletii , a white-rot wood-decomposer that is associated with siricid woodwasps in a timber pathogenic symbiosis (Fitza et al 2016). Our analysis elucidates patterns of functional diversity that have evolved within the ECM symbiotrophs, including evolution of PCWDEs, retention of genes to scavenge nitrogen compounds in soil organic matter, secondary metabolism, and TE invasion favoring duplication of species-specific genes.…”
The ectomycorrhizal symbiosis is an essential guild of many forested ecosystems and has a dynamic evolutionary history across kingdom Fungi, having independently evolved from diverse types of saprotrophic ancestors. In this study, we seek to identify genomic features of the transition to the ectomycorrhizal habit within the Russulaceae, one of the most diverse lineages of ectomycorrhizal fungi. We present comparative analyses of the pangenome and gene repertoires of 21 species across the order Russulales, including a closely related saprotrophic member of Russulaceae. The ectomycorrhizal Russulaceae is inferred to have originated around the Cretaceous-Paleogene extinction event (73.6-60.1 million years ago (MY)). The genomes of the ectomycorrhizal Russulaceae are characterized by a loss of genes for plant cell-wall degrading enzymes (PCWDEs), an expansion of genome size through increased transposable element (TE) content, a reduction in secondary metabolism clusters, and an association of genes coding for certain secreted proteins with TE "nests". The saprotrophic sister group of the ectomycorrhizal Russulaceae, Gloeopeniophorella convolvens, possesses some of these aspects (e.g., loss of PCWDE and protease orthologs, TE expansion, reduction in secondary metabolism clusters), resulting from an accelerated rate of gene evolution in the shared ancestor of Russulaceae that predates the evolution of the ectomycorrhizal habit. Genomes of Russulaceae possess a high degree of synteny, including a conserved set of terpene secondary metabolite gene clusters. We hypothesize that the evolution of the ectomycorrhizal habit requires premodification of the genome for plant root association followed by an accelerated rate of gene evolution within the secretome for host-defense circumvention and symbiosis establishment.
“…Here, we describe trends in genomic architecture and gene content in twenty representative species of Russulales. Our dataset contains fourteen previously unanalyzed genomes, including 11 species of ECM Russulaceae and their saprotrophic sister group ( Gloeopeniophorella convolvens ), and Amylostereum chailletii , a white-rot wood-decomposer that is associated with siricid woodwasps in a timber pathogenic symbiosis (Fitza et al 2016). Our analysis elucidates patterns of functional diversity that have evolved within the ECM symbiotrophs, including evolution of PCWDEs, retention of genes to scavenge nitrogen compounds in soil organic matter, secondary metabolism, and TE invasion favoring duplication of species-specific genes.…”
The ectomycorrhizal symbiosis is an essential guild of many forested ecosystems and has a dynamic evolutionary history across kingdom Fungi, having independently evolved from diverse types of saprotrophic ancestors. In this study, we seek to identify genomic features of the transition to the ectomycorrhizal habit within the Russulaceae, one of the most diverse lineages of ectomycorrhizal fungi. We present comparative analyses of the pangenome and gene repertoires of 21 species across the order Russulales, including a closely related saprotrophic member of Russulaceae. The ectomycorrhizal Russulaceae is inferred to have originated around the Cretaceous-Paleogene extinction event (73.6-60.1 million years ago (MY)). The genomes of the ectomycorrhizal Russulaceae are characterized by a loss of genes for plant cell-wall degrading enzymes (PCWDEs), an expansion of genome size through increased transposable element (TE) content, a reduction in secondary metabolism clusters, and an association of genes coding for certain secreted proteins with TE "nests". The saprotrophic sister group of the ectomycorrhizal Russulaceae, Gloeopeniophorella convolvens, possesses some of these aspects (e.g., loss of PCWDE and protease orthologs, TE expansion, reduction in secondary metabolism clusters), resulting from an accelerated rate of gene evolution in the shared ancestor of Russulaceae that predates the evolution of the ectomycorrhizal habit. Genomes of Russulaceae possess a high degree of synteny, including a conserved set of terpene secondary metabolite gene clusters. We hypothesize that the evolution of the ectomycorrhizal habit requires premodification of the genome for plant root association followed by an accelerated rate of gene evolution within the secretome for host-defense circumvention and symbiosis establishment.
“…Preference for this fungal strain by S. nigricornis in the present study is consistent with the fact that larvae of this native Sirex are known to develop in the same trees as S. noctilio (Long et al ., ; Ryan et al ., ; Hajek et al ., ) and horizontal transmission of Amylostereum between Sirex species appears to occur within trees (Hajek et al ., ; Wooding et al ., ). Sirex species were previously considered specific to single Amylostereum species (Talbot, ; Gilbertson, ), although studies of Sirex and Urocerus have demonstrated flexibility in the Amylostereum species being carried (Wooding et al ., ; Fitza et al ., ; Hajek et al ., ), in particular by two Sirex native to North America, including S. nigricornis (Hajek et al ., ; Olatinwo et al ., ). Although relatively little is understood about the biology and behaviour of S. nigricornis , flexibility in symbiont use could be advantageous now that the competitive S. noctilio is present.…”
1 Globalization leads to the introduction of invasive species that are often accompanied by associated microorganisms, and this can lead to homogenization of both introduced hosts and microbes with the native biota. One such example is the invasive Eurasian woodwasp Sirex noctilio, which inoculates pines with an obligate nutritional mutualist, the white rot fungus Amylostereum areolatum. 2 Although S. noctilio has been previously introduced outside of its native range, its arrival in North America was the first time that it was introduced to communities hosting native Sirex species and Amylostereum strains. 3 We conducted experiments aiming to investigate acceptance versus avoidance of native and non-native Amylostereum strains and species during ovipositor drilling by females of S. noctilio and a native congener, Sirex nigricornis. 4 Sirex noctilio preferred wood without prior fungal emplacement, whereas S. nigricornis preferred wood inoculated with one of the strains of Amylostereum that putatively invaded with S. noctilio. 5 Drilling and presumed oviposition by both woodwasp species were highly aggregated. 6 Based on the responses of these two Sirex species to the fungal strains and species included in the present study, the invasive S. noctilio would continue its present symbiont associations, whereas the native S. nigricornis would partly use the strain of fungal symbiont putatively introduced with S. noctilio.
“…The fungus vectored by S. nitobei is either Amylostereum areolatum (Chaillet ex Fries) Boidin (in most cases) or A. chailletii (Pers.) Boidin (Kobayashi et al., 1978 ; Fitza et al., 2016 ; Wang et al., 2021 ). There are no records of both fungi being found together in any individual wasp.…”
Section: Pest Categorisationmentioning
confidence: 99%
“…No intraspecific diversity is reported for S. nitobei . However, the symbiotic fungus species has been observed to vary between individuals, with associations with either Amylostereum areolatum or A. chailletii (Fitza et al., 2016 ). Intraspecific variation within A. areolatum has also been observed.…”
The EFSA Panel on Plant Health performed a pest categorisation of Sirex nitobei (Hymenoptera: Siricidae), the nitobe horntail, for the territory of the EU. S. nitobei is not listed in Annex II of Commission Implementing Regulation (EU) 2019/2072 but was identified as a potential regulated pest in a commodity risk assessment of Pinus thunbergii artificially dwarfed plants from Japan. This species is present in Japan (except Hokkaid o), the Republic of Korea and 13 Chinese provinces. S. nitobei attacks several Pinus species and has been reported less frequently on Abies firma and Larix spp., including L. leptolepis. The females oviposit into the sapwood. Eggs are deposited together with a phytotoxic mucus and a symbiotic fungus, Amylostereum areolatum or A. chailletii. The combined action of the venom and the fungus results in the death of the host trees. The fungus degrades the lignocellulosic components of the wood, and the larvae feed on the liquid fraction of the digested residues left by the fungus. All immature stages live in the hosts sapwood. The lifecycle of the pest lasts 1 year. S. nitobei can travel with conifer wood, wood packaging material or plants for planting, but these pathways from third countries are closed by prohibition. However, a derogation exists for artificially dwarfed Japanese black pine (Pinus thunbergii) from Japan, which therefore provides a potential pathway. Climatic conditions in several EU member states and host plant availability in those areas are conducive for establishment. The introduction of S. nitobei is potentially damaging for pines. Phytosanitary measures are available to reduce the likelihood of entry and further spread, and there is a potential for biological control. S. nitobei satisfies all the criteria that are within the remit of EFSA to assess for it to be regarded as a potential Union quarantine pest.
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