Phylogenetic and population genetic analyses reveal three distinct lineages of the invasive brown root-rot pathogen, Phellinus noxius, and bioclimatic modeling predicts differences in associated climate niches

Stewart, Jane E.; Kim, M. S.; Ota, Yuko; Sahashi, Norio; Hanna, John W.; Akiba, Mitsuteru; Ata, Jessa P.; Atibalentja, N.; Brooks, Fred E.; Chung, Chi-Ming; Dann, E. K.; Farid, A. Mohd; Hattori, Tsutomu; Lee, S. S.; Otto, Kristen; Pegg, Geoff S.; Schlub, Robert L.; Shuey, Louise S.; Tang, Alvin M. C.; Tsai, Jyh-Nong; Cannon, Philip; Klopfenstein, Ned B.

doi:10.1007/s10658-019-01926-5

Cited by 10 publications

(41 citation statements)

References 42 publications

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“…noxius were identified using Bayesian population structure analyses, PCA and phylogenetic analyses (Figure 1). Interestingly, populations from American Samoa and Malaysia showed almost no admixture with other genetic groups, suggesting limited or absent ongoing gene flow, and isolates from American Samoa formed the most genetically distinct clade in the phylogenetic tree (Figure 1a) and treemix graph (Figure 4a), concurring with previous phylogenetic analyses with protein‐coding loci (Stewart et al, 2020) and reflecting its isolation from other populations.…”

Section: Discussionsupporting

confidence: 87%

“…For example, the genetic groups of P . noxius determined in Stewart et al (2020) have different suitable climate space, and potential hybridization among these groups may favour their adaptation to wider range of climatic/environmental conditions. Also, Ibarra Caballero et al (2020) showed that the P .…”

Section: Discussionmentioning

confidence: 98%

“…These findings suggest a complex evolutionary history of P. noxius that has yet to be determined. Additionally, the results of bioclimatic modelling revealed that P. noxius represents a threat to many tropical/subtropical regions worldwide, including the Hawaiian Islands, southeastern USA, eastern Mexico, eastern Central America, parts of Africa and Madagascar, with different genetic lineages representing distinct threats (Stewart et al, 2020). Herein, using restriction siteassociated DNA sequencing (RADseq) data on 107 P. noxius isolates from 15 locations, we address four questions: (i) What is the genetic structure of P. noxius populations in regions of eastern Asia, Australia and the Pacific Islands?…”

Section: Introductionmentioning

confidence: 99%

“…Such movement can have a direct effect on pathogen and disease emergence. For example, the genetic groups of P. noxius determined inStewart et al (2020) have different suitable climate space, and potential hybridization among these groups may favour their adaptation to wider range of climatic/environmental conditions. Also, IbarraCaballero et al (2020) showed that the P. noxius genome encodes a large arsenal of wood-degrading enzymes, and exchange and accumulation of such genetic regions among different genetic groups could contribute to its virulence and wide host range.…”

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confidence: 99%

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Long evolutionary history of an emerging fungal pathogen of diverse tree species in eastern Asia, Australia and the Pacific Islands

et al. 2022

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Emerging plant pathogens have been increasing exponentially over the last century. To address this issue, it is critical to determine whether these pathogens are native to ecosystems or have been recently introduced. Understanding the ecological and evolutionary processes fostering emergence can help to manage their spread and predict epidemics/epiphytotics. Using restriction site‐associated DNA sequencing data, we studied genetic relationships, pathways of spread and the evolutionary history of Phellinus noxius, an emerging root‐rotting fungus of unknown origin, in eastern Asia, Australia and the Pacific Islands. We analysed patterns of genetic variation using Bayesian inference, maximum‐likelihood phylogeny, population splits and mixtures measuring correlations in allele frequencies and genetic drift, and finally applied coalescent‐based theory using Approximate Bayesian computation (ABC) with supervised machine learning. Population structure analyses revealed five genetic groups with signatures of complex recent and ancient migration histories. The most probable scenario of ancient pathogen spread is movement from an unsampled population to Malaysia and the Pacific Islands, with subsequent spread to Taiwan and Australia. Furthermore, ABC analyses indicate P. noxius spread occurred thousands of generations ago, contradicting previous assumptions that this pathogen was recently introduced to multiple geographical regions. Our results suggest that recent emergence of P. noxius in eastern Asia, Australia and the Pacific Islands has probably been driven by anthropogenic and natural disturbances, such as deforestation, land‐use change, severe weather events and/or introduction of exotic plants. This study provides a novel example of applying genome‐wide allele frequency data to unravel the dynamics of pathogen emergence under changing ecosystem conditions.

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Section: Discussionsupporting

confidence: 87%

Section: Discussionmentioning

confidence: 98%

Section: Introductionmentioning

confidence: 99%

mentioning

confidence: 99%

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Long evolutionary history of an emerging fungal pathogen of diverse tree species in eastern Asia, Australia and the Pacific Islands

et al. 2022

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“…Overall, under the contemporary climate, the predicted potential distribution of P. menziesii using the MaxEnt is generally congruent with the established range map of P. menziesii within the continental United States (Little, 1971). Recently, MaxEnt bioclimatic models have been widely used to investigate the suitable climate space of other plants and plant pathogens, with high predictive performance (e.g., Kumar and Stohlgren, 2009;Khanum et al, 2013;Remya et al, 2015;Stewart et al, 2018Stewart et al, , 2020Tang et al, 2021).…”

Section: Discussionmentioning

confidence: 53%

Predicting Present and Future Suitable Climate Spaces (Potential Distributions) for an Armillaria Root Disease Pathogen (Armillaria solidipes) and Its Host, Douglas-fir (Pseudotsuga menziesii), Under Changing Climates

Kim

Hanna

Stewart

et al. 2021

Front. For. Glob. Change

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Climate change and associated disturbances are expected to exacerbate forest root diseases because of altered distributions of existing and emerging forest pathogens and predisposition of trees due to climatic maladaptation and other disturbances. Predictions of suitable climate space (potential geographic distribution) for forest pathogens and host trees under contemporary and future climate scenarios will guide the selection of appropriate management practices by forest managers to minimize adverse impacts of forest disease within forest ecosystems. A native pathogen (Armillaria solidipes) that causes Armillaria root disease of conifers in North America is used to demonstrate bioclimatic models (maps) that predict suitable climate space for both pathogen and a primary host (Pseudotsuga menziesii, Douglas-fir) under contemporary and future climate scenarios. Armillaria root disease caused by A. solidipes is a primary cause of lost productivity and reduced carbon sequestration in coniferous forests of North America, and its impact is expected to increase under climate change due to tree maladaptation. Contemporary prediction models of suitable climate space were produced using Maximum Entropy algorithms that integrate climatic data with 382 georeferenced occurrence locations for DNA sequence-confirmed A. solidipes. A similar approach was used for visually identified P. menziesii from 11,826 georeferenced locations to predict its climatic requirements. From the contemporary models, data were extrapolated through future climate scenarios to forecast changes in geographic areas where native A. solidipes and P. menziesii will be climatically adapted. Armillaria root disease is expected to increase in geographic areas where predictions suggest A. solidipes is well adapted and P. menziesii is maladapted within its current range. By predicting areas at risk for Armillaria root disease, forest managers can deploy suitable strategies to reduce damage from the disease.

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Physiological responses of seedlings to the invasion of brown root rot hyphae differ between semi-deciduous Bischofia javanica Blume and evergreen Rhaphiolepis umbellata (Thunb.) Makino

Yazaki,

Kimura,

Zhang

et al. 2023

Eur J Plant Pathol

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Phylogenetic and population genetic analyses reveal three distinct lineages of the invasive brown root-rot pathogen, Phellinus noxius, and bioclimatic modeling predicts differences in associated climate niches

Cited by 10 publications

References 42 publications

Long evolutionary history of an emerging fungal pathogen of diverse tree species in eastern Asia, Australia and the Pacific Islands

Long evolutionary history of an emerging fungal pathogen of diverse tree species in eastern Asia, Australia and the Pacific Islands

Predicting Present and Future Suitable Climate Spaces (Potential Distributions) for an Armillaria Root Disease Pathogen (Armillaria solidipes) and Its Host, Douglas-fir (Pseudotsuga menziesii), Under Changing Climates

Physiological responses of seedlings to the invasion of brown root rot hyphae differ between semi-deciduous Bischofia javanica Blume and evergreen Rhaphiolepis umbellata (Thunb.) Makino

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