Current Forestry Reports

, Volume 4, Issue 2, pp 72–84 | Cite as

Molecular Genetic Approaches Toward Understanding Forest-Associated Fungi and Their Interactive Roles Within Forest Ecosystems

  • Jane E. Stewart
  • Mee-Sook Kim
  • Ned B. Klopfenstein
Forest Pathology (A Carnegie, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Forest Pathology

Abstract

Purpose of Review

The continued, rapid development of novel molecular genetic tools is contributing to a better understanding of forest-associated fungi and their interactive roles within diverse forest ecosystems. This paper focuses on recent developments of DNA-based diagnostics/detection, phylogenetics, population genetics, genomics, and metagenomics tools that have been applied to forest-associated fungi to better understand their roles in forest ecosystems and provide key insights for managing forest health.

Recent Findings

With the advent of new molecular technologies, we can better understand the biology of forest fungi by examining their genetic code. By utilizing genomics, fungal pathogens’ biological functions can be deduced from its genomic content. Further, high-resolution marker systems allow the determination of a pathogen’s population genetics and genomics, which provides important insights into its global movement and genetic shifts in local pathogen populations. Such genetic information has diverse applications for forest management to improve forest health. Lastly, new technologies in metagenomics will enhance the abilities to detect, describe, and utilize the complex interactions among fungal pathogens/symbionts, host trees, and associated microbial communities to develop novel management strategies for forest ecosystems.

Summary

Continued development and applications of molecular genetic and genomic tools provide insights into the diverse roles of forest-associated fungi in forest ecosystems, but long-term, wide-scale research is needed to determine how ecological functions are influenced by complex ecological interactions among microbial communities, other forest ecosystem components, and the environment. Such approaches may foster a paradigm shift away from single microbial pathogens, decomposers, or symbionts interacting with a single host or substrate, and provide more holistic approaches toward understanding interactions among microbial communities that drive forest health processes.

Keywords

Forest pathogens Genomics Transcriptomes Metagenomics 

Notes

Acknowledgments

The authors extend thanks to the researchers who facilitated the research described herein.

Funding information

Funding provided for this manuscript includes grants from the USDA Forest Service, Forest Health Protection, Special Technology Development Program, Evaluation Monitoring Program, the Western Wildland Environmental Threat Assessment Center, the Western Forest Conservation Association, and Colorado State University.

Compliance with Ethical Standards

Conflict of Interest

Dr. Stewart, Dr. Kim, and Dr. Klopfenstein have no conflicts of interests to declare.

Human and Animal Rights and Informed Consent

This article contains no studies with human and animal subjects performed by the authors.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Akiba M, Ota Y, Tsai IJ, Hattori T, Sahashi N, Kikuchi T. Genetic differentiation and spatial structure of Phellinus noxius, the causal agent of brown root rot of woody plants in Japan. PLoS One. 2015;10:e0141792.CrossRefGoogle Scholar
  2. 2.
    Alamouti SM, Wang V, DiGuistini S, Six DL, Bohlmann J, Hamelin RC, et al. Gene genealogies reveal cryptic species and host preferences for the pine fungal pathogen Grosmannia clavigera. Mol Ecol. 2011;20:2581–601.CrossRefGoogle Scholar
  3. 3.
    Aylward J, Steenkamp ET, Dreyer LL, Roets F, Wingfield BD, Wingfield MJ. A plant pathology perspective of fungal genome sequencing. IMA Fungus. 2017;8(1):1–15.  https://doi.org/10.5598/imafungus.2017.08.01.01.CrossRefGoogle Scholar
  4. 4.
    Baysal-Gurel F, Cinar A. First report of Armillaria root rot caused by Armillaria mellea infecting Carrizo citrange and sour orange rootstocks in Turkey. Plant Dis. 2014;98:1439.  https://doi.org/10.1094/PDIS-05-14-0463-PDN.CrossRefGoogle Scholar
  5. 5.
    Beenken L. Austropuccinia: a new genus name for the myrtle rust Puccinia psidii placed within the redefined family Sphaerophragmiaceae (Pucciniales). Phytotaxa. 2017;297(1):053–61.CrossRefGoogle Scholar
  6. 6.
    Bihon W, Wingfield MJ, Slippers B, Duong TA, Wingfield BD. MAT gene idiomorphs suggest a heterothallic sexual cycle in a predominantly asexual and important pine pathogen. Fungal Genet Biol. 2014;62:55–61.CrossRefGoogle Scholar
  7. 7.
    Bini AP, Quecine MC, da Silva TM, Silva LD, Labate CA. Development of a quantitative real-time PCR assay using SYBR Green for early detection and quantification of Austropuccinia psidii in Eucalyptus grandis. Eur J Plant Pathol. 2017;150:735–46.  https://doi.org/10.1007/s10658-017-1321-7.CrossRefGoogle Scholar
  8. 8.
    •• Bradshaw RE, Guo Y, Sim AD, Kabir MS, Chettri P, Ozturk IK, et al. Genome-wide gene expression dynamics of the fungal pathogen Dothistroma septosporum throughout its infection cycle of the gymnosperm host Pinus radiata. Mol Plant Pathol. 2016;17(2):210–24. Genome-wide expression patterns were characterized as a time series during the infection cycle of Dothistroma septosporum on Pinus radiata. The time series highlights the early biotrophic phase that is characterized by genes encoding fungal cell wall-modifying enzymes and signaling proteins to later necrotrophic stages that is characterized by genes for secondary metabolism, oxidoreductases, transporters, and starch degradation. CrossRefGoogle Scholar
  9. 9.
    • Brar S, Tsui CKM, Dhillon B, Bergeron M-J, Joly DL, Zambino PJ, et al. Colonization history, host distribution, anthropogenic influence and landscape features shape populations of white pine blister rust, an invasive alien tree pathogen. PLoS One. 2015;10(5):e0127916.  https://doi.org/10.1371/journal.pone.0127916. This study highlights the genetic diversity of Cronarium ribicola , the causal agent of white pine blister rust, 100 years after its introduction into North America. Using SNP analysis of 1292 samples from 66 locations, the authors found two distinct populations, western and eastern. The eastern population is 2 to 5 times more diverse than the western populations, indicating more introductions have occurred in eastern North America compared to the western region. CrossRefGoogle Scholar
  10. 10.
    Buée M, Reich M, Murat C, Morin E, Nilsson RH, Uroz S, et al. 454 pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol. 2009;184:449–56.CrossRefGoogle Scholar
  11. 11.
    Burns KS, Hanna JW, Klopfenstein NB, Kim M-S. First report of the Armillaria root disease pathogen, Armillaria sinapina, on subalpine fir (Abies lasiocarpa) and quaking aspen (Populus tremuloides) in Colorado. Plant Dis. 2016;100:217.CrossRefGoogle Scholar
  12. 12.
    • Burokiene D, Prospero S, Jung E, Marciulyniene D, Moosbrugger K, Norkute G, et al. Genetic population structure of the invasive ash dieback pathogen Hymenoscyphus fraxineus in its expanding range. Biol Invasions. 2015;17:2743–56.  https://doi.org/10.1007/s10530-015-0911-6. This research examined the genetic diversity of the exotic pathogen Hymenoscyphus fraxineus , causal agent of ash dieback at the epidemic disease front in Switzerland, compared to the post-epidemic phase in Lithuania. The authors found that diversity was comparable at both locations indicating weak founder effects and no reduction in diversity occurred at the epidemic disease phase, though more mating occurred at the post-epidemic phase. CrossRefGoogle Scholar
  13. 13.
    Cardenas E, Kranabetter JM, Hope G, Maas KR, Hallam S, Mohn WW. Forest harvesting reduces the soil metagenomic potential for biomass decomposition. ISME J. 2015;9:2465–76.CrossRefGoogle Scholar
  14. 14.
    Carnegie AJ, Lidbetter JR, Walker J, Horwood MA, Tesoriero L, Glen M, et al. Uredo rangelii, a taxon in the guava rust complex, newly recorded on Myrtaceae in Australia. Australas Plant Pathol. 2010;39:463–6.CrossRefGoogle Scholar
  15. 15.
    Chen C, Yao Y, Zhang L, Xu M, Jiang J, Dou T, et al. A comprehensive analysis of the transcriptomes of Marssonina brunnea and infected poplar leaves to capture vital events in host-pathogen interactions. PLoS One. 2015;10(7):e0134246.  https://doi.org/10.1371/journal.pone.0134246.CrossRefGoogle Scholar
  16. 16.
    Choi J, Lee G-W, Kim K-T, Jeon J, Détry N, Kuo H-C, et al. Comparative analysis of genome sequences of the conifer tree pathogen, Heterobasidion annosum s.s. Genomics Data. 2017;14:106–13.CrossRefGoogle Scholar
  17. 17.
    Chung C-L, Huang S-Y, Huang Y-C, Tzean S-S, Ann P-J, Tsai J-N, et al. The genetic structure of Phellinus noxius and dissemination pattern of brown root rot disease in Taiwan. PLoS One. 2015;10(10):e0139445.  https://doi.org/10.1371/journal.pone.0139445.CrossRefGoogle Scholar
  18. 18.
    • Chung C-L, Lee TJ, Akiba M, Lee H-H, Kuo T-H, Liu D, et al. Comparative and population genomics landscape of Phellinus noxius: a hypervariable fungus causing root rot in trees. Mol Ecol. 2017. early view.  https://doi.org/10.1111/mec.14359. The authors found an expanded 1,3-beta-glucan synthase gene family in Phellinus noxius and suggested that this may be linked to fast-growing abilities of P. noxius . Further, the authors found extreme genetic variability.
  19. 19.
    Coetzee MPA, Wingfield BD, Harrington TC, Steimel J, Coutinho TA, Wingfield MJ. The root rot fungus Armillaria mellea introduced into South Africa by early Dutch settlers. Mol Ecol. 2001;10:387–96.CrossRefGoogle Scholar
  20. 20.
    Coetzee MPA, Wingfield BD, Roux J, Crous PW, Denman S, Wingfield MJ. Discovery of two northern hemisphere Armillaria species on Proteaceae in South Africa. Plant Pathol. 2003;52:604–12.CrossRefGoogle Scholar
  21. 21.
    Collins C, Keane TM, Turner DJ, O’Keeffe G, Fitzpatrick DA, Doyle S. Genomic and proteomic dissection of the ubiquitous plant pathogen, Armillaria mellea: toward a new infection model system. J Proteome Res. 2013;12:2552−2570.CrossRefGoogle Scholar
  22. 22.
    Comeau AM, Dufour J, Bouvet GF, Jacobi V, Nigg M, Henrissat B, et al. Functional annotation of the Ophiostoma novo-ulmi genome: insights into the phytopathogenicity of the fungal agent of Dutch elm disease. Genome Biol Evol. 2014;7(2):410–30.CrossRefGoogle Scholar
  23. 23.
    • de Wit PJGM, van der Burgt A, Ökmen B, Stergiopoulos I, Abd-Elsalam KA, Aerts AL, et al. The genomes of the fungal plant pathogens Cladosporium fulvum and Dothistroma septosporum reveal adaptation to different hosts and lifestyles but also signatures of common ancestry. PLoS Genet. 2012;11(12):e1005775.  https://doi.org/10.1371/journal.pgen.1005775. This research compares and contrasts two phylogenetically related species that have different lifestyles and hosts. The authors found genes that were unique to Cladosporium fulvum for detoxification of tomatine. Each genome had genes involved in the production of the toxin dothistrormin; however, these genes were only expressed in Dothistroma septosporum , suggesting a recent adaption in their lifestyle. CrossRefGoogle Scholar
  24. 24.
    •• Dhillon B, Feau N, Aerts AL, Beauseigle S, Bernier L, Copeland A, et al. Horizontal gene transfer and gene dosage drives adaptation to wood colonization in a tree pathogen. PNAS. 2015;112:3451–6. A genomics approach was used to compare Mycosphaerella populorum (poplar canker pathogen) with M. populicola (poplar leaf pathogen) and found signatures of horizontal gene transfer for several carbohydrate degradation genes associated with wood decay suggesting that adaption in the canker pathogen was the result of these horizontally acquired genes. CrossRefGoogle Scholar
  25. 25.
    DiGuistini S, Liao NY, Platt D, Robertson G, Seidel M, Chan SK, et al. De novo genome sequence assembly of a filamentous fungus using Sanger, 454 and Illumina sequence data. Genome Biol. 2009;10:R94.  https://doi.org/10.1186/gb-2009-10-9-r94.CrossRefGoogle Scholar
  26. 26.
    DiGuistini S, Wang Y, Liao NY, Taylor G, Tanguay P, Feau N, et al. Genome and transcriptome analyses of the mountain pine beetle-fungal symbiont Grosmannia clavigera, a lodgepole pine pathogen. PNAS. 2011;108:2504–9.CrossRefGoogle Scholar
  27. 27.
    du Plessis E, McTaggart AR, Granados GM, Wingfield MJ, Roux J, Ali MIM, et al. First report of myrtle rust caused by Austropuccinia psidii on Rhodomyrtus tomentosa (Myrtaceae) from Singapore. Plant Dis. 2017;101:1676.CrossRefGoogle Scholar
  28. 28.
    Dumroese RK, Kim M-S, James RL. Fusarium oxysporum protects Douglas-fir (Pseudotsuga menziesii) seedlings from root disease caused by Fusarium commune. Plant Pathol J. 2012;28(3):311–6.CrossRefGoogle Scholar
  29. 29.
    Duplessis S, Cuomo CA, Lin YC, Aerts A, Tisserant E, Veneault-Fourrey C, et al. Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc Natl Acad Sci U S A. 2011;108(22):9166–71.  https://doi.org/10.1073/pnas.1019315108.CrossRefGoogle Scholar
  30. 30.
    • Eaton DAR, Ree RH. Inferring phylogeny and introgression using RADseq data: an example from flowering plants (Pedicularis: Orobanchaceae). Syst Biol. 2013;62:689–706.  https://doi.org/10.1093/sysbio/syt032. The authors were able to assess phylogeny and confirm introgression in broomrape plant family using 40,000 restriction-site associated DNA markers. The research highlights the importance of geographic isolation in the emergence of new species. CrossRefGoogle Scholar
  31. 31.
    Elías-Román RD, Guzmán-Plazola RA, Klopfenstein NB, Alvarado-Rosales D, Calderón-Zavala G, García-Espinosa R, et al. Incidence and phylogenetic analyses of Armillaria spp. associated with root disease in peach orchards in the State of Mexico, Mexico. For Pathol. 2013;43:390–401.Google Scholar
  32. 32.
    Elías-Román RD, Medel R, Klopfenstein NB, Hanna JW, Kim M-S, Alvarado D. Armillaria mexicana (Agaricales, Physalacriaceae), a newly described species from Mexico. Mycologia. 2018.  https://doi.org/10.1080/00275514.2017.1419031.
  33. 33.
    •• Fitz-Gibbon S, Hipp AL, Pham KK, Manos PS, Sork VL. Phylogenomic inferences from reference-mapped and de novo assembled short-read sequence data using RADseq sequencing of California white oaks (Quercus section Quercus). Genome. 2017;60:743–55.  https://doi.org/10.1139/gen-2016-0202. This research compares and contrasts bioinformatics pipelines, de novo assembly versus reference-mapped assemblies to produce phylogenies for California white oaks. The research shows that both methodologies yield similar phylogenies, but that downstream uses of RAD-seq data varied. CrossRefGoogle Scholar
  34. 34.
    Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, et al. The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science. 2012;336:1715–9.CrossRefGoogle Scholar
  35. 35.
    Garbelotto M, Guglielmo F, Mascheretti S, Croucher PJP, Gonthier P. Population genetic analyses provide insights on the introduction pathway and spread patterns of the North American forest pathogen Heterobasidion irregulare in Italy. Mol Ecol. 2013;22:4855–69.CrossRefGoogle Scholar
  36. 36.
    Gonthier P, Garbelotto M. Amplified fragment length polymorphism and sequence analyses reveal massive gene introgression from the European fungal pathogen Heterobasidion annosum into its introduced congener H. irregulare. Mol Ecol. 2011;20:2756–70.CrossRefGoogle Scholar
  37. 37.
    Gonthier P, Warner R, Nicolotti G, Mazzaglia A, Garbelotto M. Pathogen introduction as a collateral effect of military activity. Mycol Res. 2004;108:468–70.CrossRefGoogle Scholar
  38. 38.
    Graça RN, Ross-Davis AL, Klopfenstein NB, Kim M-S, Peever TL, Cannon PG, et al. Rust disease of eucalypts, caused by Puccinia psidii, did not originate via host jump from guava in Brazil. Mol Ecol. 2013;22(24):6033–47.CrossRefGoogle Scholar
  39. 39.
    Hacquard S, Joly DL, Lin Y-C, Tisserant E, Feau N, Delaruelle C, et al. A comprehensive analysis of genes encoding small secreted proteins identifies candidate effectors in Melampsora larici-populina (poplar leaf rust). MPMI. 2012;25:279–93.  https://doi.org/10.1094/MPMI-09-11-0238. CrossRefGoogle Scholar
  40. 40.
    Hamelin RC, Grigoriev IV, Szabo LJ, Martin F. Obligate biotrophy features unraveled by the genomic analysis of rust fungi. PNAS. 2011;108:9166–71.CrossRefGoogle Scholar
  41. 41.
    Hanna JW, Klopfenstein NB, Kim M-S. First report of the root-rot pathogen, Armillaria nabsnona, from Hawaii. Plant Dis. 2007;91:634.CrossRefGoogle Scholar
  42. 42.
    de Wit PJGM, van der Burgt A, Ökmen B, Stergiopoulos I, Abd-Elsalam K, et al. The genomes of the fungal plant pathogens Cladosporium fulvum and Dothistroma septosporum reveal adaptation to different hosts and lifestyles but also signatures of common ancestry. PLoS Genet. 2012;8(11):e1003088.  https://doi.org/10.1371/journal.pgen.1003088.
  43. 43.
    Hipp AL, Eaton DAR, Cavender-Bares J, Fitzek E, Nipper R, Manos PS, et al. A framework phylogeny of the American oak clade based on sequenced RAD data. PLoS One. 2014;9:e93975.  https://doi.org/10.1371/journal.pone.0093975.CrossRefGoogle Scholar
  44. 44.
    Hori C, Ishida T, Igarashi K, Samejima M, Suzuki H, Master E, et al. Analysis of the Phlebiopsis gigantea genome, transcriptome and secretome provides insight into its pioneer colonization strategies of wood. PLoS Genet. 2014;10(12):e1004759.  https://doi.org/10.1371/journal.pgen.1004759.CrossRefGoogle Scholar
  45. 45.
    Karlsson M, Olson A, Stenlid J. Expressed sequences from the basidiomycetous tree pathogen Heterobasidion annosum during early infection of Scots pine. Fungal Genet Biol. 2003;39:51–9.CrossRefGoogle Scholar
  46. 46.
    • Kaul S, Sharma T, Dhar MK. “Omics” tools for better understanding the plant–endophyte interactions. Front Plant Sci. 2016;7:955.  https://doi.org/10.3389/fpls.2016.00955. This review paper discusses methodologies and importance of understanding endophytic roles and complex interactions associated with plant systems. CrossRefGoogle Scholar
  47. 47.
    Kawanishi T, Uemastu S, Kakishima M, Kagiwada S, Hamamoto H, Horie H, et al. First report of rust disease on ohia and the causal fungus, Puccinia psidii, in Japan. J Gen Plant Pathol. 2009;75:428–31.CrossRefGoogle Scholar
  48. 48.
    Kim M-S, Hanna JW, Klopfenstein NB. First report of an Armillaria root disease pathogen, Armillaria gallica, associated with several new hosts in Hawaii. Plant Dis. 2010a;94:1510.  https://doi.org/10.1094/PDIS-04-10-0266.Google Scholar
  49. 49.
    Kim MS, Klopfenstein NB, Hanna JW, Cannon P, Medel R, López A. First report of Armillaria root disease caused by Armillaria tabescens on Araucaria araucana in Veracruz, Mexico. Plant Dis. 2010b;94(6):784.CrossRefGoogle Scholar
  50. 50.
    • Kim M-S, Hohenlohe P, Kim KH, Seo S-T, Klopfenstein NB. Genetic diversity and population structure of Raffaelea quercus-mongolicae, a fungus associated with oak mortality in South Korea. For Pathol. 2016;46:164–7. The authors used restriction-site-association DNA sequencing to highlight the low genetic diversity and no apparent population structure among populations of Raffaelea quercus-mongolicae , a fungus associated with oak mortality in South Korea. These results support the hypothesis that this pathogen was recently introduced to South Korea. CrossRefGoogle Scholar
  51. 51.
    Kim M-S, Fonseca NR, Hauff RD, Cannon PG, Hanna JW, Klopfenstein NB. First report of the root-rot pathogen, Armillaria gallica, on koa (Acacia koa) and ‘ōhi‘a lehua (Metrosideros polymorpha) on the island of Kaua‘i, Hawai‘i. Plant Dis. 2017;101:255.  https://doi.org/10.1094/PDIS-07-16-1043-PDN.CrossRefGoogle Scholar
  52. 52.
    Klopfenstein NB, Lundquist JE, Hanna JW, Kim M-S, McDonald GI. First report of Armillaria sinapina, a cause of Armillaria root disease, associated with a variety of tree hosts on sites with diverse climates in Alaska. Plant Dis. 2009;93:111.CrossRefGoogle Scholar
  53. 53.
    Klopfenstein NB, Hanna JW, Cannon PG, Medel-Ortiz R, Alvarado-Rosales D, Lorea-Hernández F, et al. First report of the Armillaria root-disease pathogen, Armillaria gallica, associated with several woody hosts in three states of Mexico. Plant Dis. 2014;98:1280.CrossRefGoogle Scholar
  54. 54.
    • Klopfenstein NB, Stewart JE, Ota Y, Hanna JW, Richardson BA, Ross-Davis AL, et al. Insights into the phylogeny of Northern Hemisphere Armillaria: neighbor-net and Bayesian analyses of translation elongation factor 1-α gene sequences. Mycologia. 2017;109:75–91. This research highlights the existence of four superclades within the genus of Armillaria and the utility of using the translation elongation factor 1-alpha as a species barcode for this genus. CrossRefGoogle Scholar
  55. 55.
    •• Koch RA, Wilson AW, Séné O, Henkel TW, Aime MC. Resolved phylogeny and biogeography of the root pathogen Armillaria and its gasteroid relative, Guyanagaster. BMC Evol Biol. 2017;17:33.  https://doi.org/10.1186/s12862-017-0877-3. This research used morphological and genetic data to determine the evolution of armillarioid fungi. Results suggest that the armillarioid lineage evolved in Eurasia around 51 million years ago and Armillaria species evolved in association with climate shift from warm/tropical to cool/arid during the late Eocene. Melanized rhizomorphs, which are unique to Armillaria species, could represent an adaption to harsh environments. CrossRefGoogle Scholar
  56. 56.
    Kubartová A, Ottosson E, Dahlberg A, Stenlid J. Patterns of fungal communities among and within decaying logs, revealed by 454 sequencing. Mol Ecol. 2012;21:4514–32.CrossRefGoogle Scholar
  57. 57.
    • Lamarche J, Potvin A, Pelletier G, Stewart D, Feau N, Alayon DIO, et al. Molecular detection of 10 of the most unwanted alien Forest pathogens in Canada using real-time PCR. PLoS One. 2015;10(8):e0134265.  https://doi.org/10.1371/journal.pone.0134265. This research developed molecular detection tools for 10 of the most unwanted forest pathogens in Canada. These tools could help detection/eradication of unwanted pathogens before they get established. CrossRefGoogle Scholar
  58. 58.
    Lee SK, Seo S-T. First report of Armillaria root disease caused by Armillaria tabescens on Carpinus tschonoskii in South Korea. Plant Dis. 2016;100:213.  https://doi.org/10.1094/PDIS-06-15-0651-PDN.CrossRefGoogle Scholar
  59. 59.
    Lee SK, Seo S-T, Park J-H, Lee SK. First report of Armillaria root disease caused by Armillaria ostoyae on Japanese larch (Larix kaempferi) and eastern white pine (Pinus strobus) in South Korea. Plant Dis. 2016;100:528.  https://doi.org/10.1094/PDIS-07-15-0744-PDN.CrossRefGoogle Scholar
  60. 60.
    •• Lindahl BD, Nilsson RH, Tedersoo L, Abarenkov K, Carlsen T, Kjøller R, et al. Fungal community analysis by high-throughput sequencing of amplified markers – a user’s guide. New Phytol. 2013;199:288–99. The article discusses methodologies for conducting metagenomics for fungal community analyses. CrossRefGoogle Scholar
  61. 61.
    Liu J-J, Sturrock RN, Sniezko RA, Williams H, Benton R, Zamany A. Transcriptome analysis of the white pine blister rust pathogen Cronartium ribicola: de novo assembly, expression profiling, and identification of candidate effectors. BMC Genomics. 2015;16:678.  https://doi.org/10.1186/s12864-015-1861-1.CrossRefGoogle Scholar
  62. 62.
    • Lundén K, Danielsson M, Durling MB, Ihrmark K, Gorriz MN, Stenlid J, et al. Transcriptional responses associated with virulence and defense in the interaction between Heterobasidion annosum s.s. and Norway spruce. PLoS One. 2015;10(7):e0131182.  https://doi.org/10.1371/journal.pone.0131182. This research highlights the transcriptional responses in a Heterobasidion -Norway spruce as a time series analysis. This research identified novel transcripts with expression patterns that suggest roles in defense. CrossRefGoogle Scholar
  63. 63.
    Machado PS, Alfenas AC, Alfenas RF, Mohammed CL, Glen M. Microsatellite analysis indicates that Puccinia psidii in Australia is mutating but not recombining. Australas Plant Pathol. 2015;44:455–62.CrossRefGoogle Scholar
  64. 64.
    Martin F, Aerts A, Ahrén D, Brun A, Danchin EGJ, Duchaussoy F, et al. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature. 2008;452:88–92.CrossRefGoogle Scholar
  65. 65.
    Martinez D, Larrondo LF, Putnam N, Gelpke MDS, Huang K, Chapman J, et al. Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nat Biotechnol. 2004;22:695–700.CrossRefGoogle Scholar
  66. 66.
    McDonald GI, Richardson BA, Zambino PJ, Klopfenstein NB, Kim M-S. Pedicularis and Castilleja are natural hosts of Cronartium ribicola in North America: a first report. For Pathol. 2006;36:73–82.CrossRefGoogle Scholar
  67. 67.
    McTaggart AR, Roux J, Granados GM, Gafur A, Tarrigan M, Santhakumar P, et al. Rust (Puccinia psidii) recorded in Indonesia poses a threat to forests and forestry in South-East Asia. Australasian Plant Pathol. 2016;45:83–9.CrossRefGoogle Scholar
  68. 68.
    Mmbaga MT, Klopfenstein NB, Kim M-S, Mmbaga NC. PCR-based identification of Erysiphe pulchra and Phyllactinia guttata from Cornus florida using ITS-specific primers. For Pathol. 2004;34:321–8.CrossRefGoogle Scholar
  69. 69.
    Nelson EV, Fairweather ML, Ashiglar SM, Hanna JW, Klopfenstein NB. First report of the Armillaria root disease pathogen, Armillaria gallica, on Douglas-fir (Pseudotsuga menziesii) in Arizona. Plant Dis. 2013;97:1658.CrossRefGoogle Scholar
  70. 70.
    Ohm RA, Riley R, Salamov A, Min B, Choi I-G, Grigoriev IV. Genomics of wood-degrading fungi. Fungal Genet Biol. 2014;72:82–90.CrossRefGoogle Scholar
  71. 71.
    Olson A, Aerts A, Asiegbu F, Belbahri L, Bouzid O, Broberg A, et al. Insight into trade-off between wood decay and parasitism from the genome of a fungal forest pathogen. New Phytol. 2012;194:1001–13.CrossRefGoogle Scholar
  72. 72.
    Ota Y, Tokuda S, Buchanan PK, Hattori T. Phylogenetic relationships of Japanese species of HeterobasidionH. annosum sensu lato and an undetermined Heterobasidion sp. Mycologia. 2006;98:717–25.Google Scholar
  73. 73.
    Richardson BA, Klopfenstein NB, Zambino PJ, McDonald GI, Geils BW, Carris LM. The influence of host resistance on the genetic structure of the white pine blister rust fungus, Cronartium ribicola, in western North America. Phytopathology. 2008;98:413–20.CrossRefGoogle Scholar
  74. 74.
    Ross-Davis AL, Stewart JE, Hanna JW, Kim M-S, Knaus B, Cronn R, et al. Transcriptome of an Armillaria root disease pathogen reveals candidate genes involved in substrate utilization at the host-pathogen interface. For Pathol. 2013;43:468–77.CrossRefGoogle Scholar
  75. 75.
    Roux J, Greyling I, Coutinho TA, Verleur M, Wingfield MJ. The Myrtle rust pathogen, Puccinia psidii, discovered in Africa. IMA Fungus. 2013;4:155–9.CrossRefGoogle Scholar
  76. 76.
    Roux J, Granados GM, Shuey L, Barnes I, Wingfield MJ, McTaggart AR. A unique genotype of the rust pathogen, Puccinia psidii, on Myrtaceae in South Africa. Australas Plant Pathol. 2016;45:645–52.  https://doi.org/10.1007/s13313-016-0447-y.CrossRefGoogle Scholar
  77. 77.
    Sandhu KS, Karaoglu H, Zhang P, Park RF. Simple sequence repeat markers support the presence of a single genotype of Puccinia psidii in Australia. Plant Pathol. 2016;65:1084–94.CrossRefGoogle Scholar
  78. 78.
    Schnabel G, Bryson PK, Williamson MA. First report of Armillaria tabescens causing Armillaria root rot of pindo palm in South Carolina. Plant Dis. 2006;90:1106.CrossRefGoogle Scholar
  79. 79.
    Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Leveseque CA, et al. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. PNAS. 2012;109:6241–6.CrossRefGoogle Scholar
  80. 80.
    Sipos G, Prasanna AN, Walter MC, O’Connor E, Bálint B, Krizsán K, et al. Genome expansion and lineage-specific genetic innovations in the forest pathogenic fungi Armillaria. Nat Ecol Evol. 2017;1:1931–41.CrossRefGoogle Scholar
  81. 81.
    Skovgaard K, Rosendahl S, Nirenberg HI. Fusarium commune is a new species identified by morphological and molecular phylogenetic data. Mycologia. 2003;95:630–6.CrossRefGoogle Scholar
  82. 82.
    Stewart JE, Kim M-S, James RL, Dumroese RK, Klopfenstein NB. Molecular characterization of Fusarium oxysporum and Fusarium commune isolates from a conifer nursery. Phytopathology. 2006;96:1124–33.CrossRefGoogle Scholar
  83. 83.
    Stewart JE, Abdo Z, Dumroese RK, Klopfenstein NB, Kim M-S. Virulence of Fusarium oxysporum and F. commune to Douglas-fir (Pseudotsuga menziesii) seedlings. For Pathol. 2012;42:220–8.CrossRefGoogle Scholar
  84. 84.
    • Stewart JE, Ross-Davis AL, Graҫa RN, Alfenas AC, Peever TL, Hanna JW, et al. Insights into the genetic diversity of the myrtle rust pathogen (Austropuccinia psidii) in the Americas and Hawaii: global implications for invasive threat assessments. For Pathol. 2018;48:e12378.  https://doi.org/10.1111/efp.12378/epdf. This research identifies three distinct lineages of the myrtle rust pathogen, Austropuccinia psidii, with different suitable climatic conditions. This research suggests that each lineage may behave differently as introduced pathogens. CrossRefGoogle Scholar
  85. 85.
    •• Štursová M, Šnajdr J, Cajthaml T, Bárta J, Šantrůčková H, Baldrian P. When the forest dies: the response of forest soil fungi to a bark beetle-induced tree dieback. The ISME Journal. 2014;8:1920–31. This article highlights the drastic changes in fungal communities and their functions in response to bark beetle-induced decline in spruce forests. The overall fungal biomass was reduced two-fold with a concomitant decrease in mycorrhizal fungi and slight increase in saprotrophic taxa. CrossRefGoogle Scholar
  86. 86.
    Tan M-K, Collins D, Chen Z, Englezou A, Wilkins MR. A brief overview of the size and composition of the myrtle rust genome and its taxonomic status. Mycology. 2014;5:52–63.  https://doi.org/10.1080/21501203.2014.919967.CrossRefGoogle Scholar
  87. 87.
    Tokuda S, Hattori T, Dai Y-C, Ota Y, Buchanan PK. Three species of Heterobasidion (Basidiomycota, Hericiales), H. parviporum, H. orientale sp. nov. and H. ecrustosum sp. nov. from East Asia. Mycoscience. 2009;50:190–202.CrossRefGoogle Scholar
  88. 88.
    Tzean Y, Shu P-Y, Liou R-F, Tzean S-S. Development of oligonucleotide microarrays for simultaneous multi-species identification of Phellinus tree-pathogenic fungi. Microb Biotechnol. 2016;9:235–44.CrossRefGoogle Scholar
  89. 89.
    Uchida J, Zhong S, Kilgore E. First report of a rust disease on 'ōhi'a caused by Puccinia psidii in Hawaii. Plant Dis. 2006;90:524.CrossRefGoogle Scholar
  90. 90.
    •• Uroz S, Buée M, Deveau A, Mieszkin S, Martin F. Ecology of the forest microbiome: Highlights of temperate and boreal ecosystems. Soil Biol Biochem. 2016;103:471–88. This study highlights differences in microbial communities associated with tree species, soil types and properties, seasons, and forestry practices. CrossRefGoogle Scholar
  91. 91.
    • Vaz ABM, Fonseca PLC, Leite LR, Badotti F, Salim ACM, Araujo FMG, et al. Using Next-Generation Sequencing (NGS) to uncover diversity of wood-decaying fungi in neotropical Atlantic forests. Phytotaxa. 2017;295(1):001–21. This study utilizes ITS1 and ITS2 amplified metagenomic sequencing methodologies to characterize the diversity of fungi associated with wood decay in neotropical forests of Brazil. CrossRefGoogle Scholar
  92. 92.
    Williams HL, Sturrock RN, Islam MA, Hammett C, Ekramoddoullah AKM, Leal I. Gene expression profiling of candidate virulence factors in the laminated root rot pathogen Phellinus sulphurascens. BMC Genomics. 2014;15:603. http://www.biomedcentral.com/1471-2164/15/603 CrossRefGoogle Scholar
  93. 93.
    Yakovlev IA, Hietala AM, Courty P-E, Lundell T, Solheim H, Fossdal CG. Genes associated with lignin degradation in the polyphagous white-rot pathogen Heterobasidion irregulare show substrate-specific regulation. Fungal Genet Biol. 2013;56:17–24.CrossRefGoogle Scholar
  94. 94.
    Zhu S, Cao Y-Z, Jiang C, Tan B-Y, Wang Z, Feng S, et al. Sequencing the genome of Marssonina brunnea reveals fungus-poplar co-evolution. BMC Genomics. 2012;13:382. http://www.biomedcentral.com/1471-2164/13/382 CrossRefGoogle Scholar
  95. 95.
    Žifčáková L, Větrovský T, Howe A, Baldrian P. Microbial activity in forest soil reflects the changes in ecosystem properties between summer and winter. Environ Microbiol. 2016;18(1):288–301.CrossRefGoogle Scholar
  96. 96.
    Otrosina WJ, Garbelotto M. Heterobasidion occidentale sp. nov. and Heterobasidion irregulare nom. nov.: A disposition of north American Heterobasidion biological species. Fungal Biol. 2010;114:16–25.CrossRefGoogle Scholar

Copyright information

© This is a U.S. government work and its text is not subject to copyright protection in the United States; however, its text may be subject to foreign copyright protection 2018

Authors and Affiliations

  • Jane E. Stewart
    • 1
  • Mee-Sook Kim
    • 2
  • Ned B. Klopfenstein
    • 3
  1. 1.Department of Bioagricultural Sciences and Pest ManagementColorado State UniversityFort CollinsUSA
  2. 2.Pacific Northwest Research StationUnited States Department of Agriculture, Forest ServiceCorvallisUSA
  3. 3.Rocky Mountain Research StationUnited States Department of Agriculture, Forest ServiceMoscowUSA

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