1932

Abstract

Global change is pressing forest pathologists to solve increasingly complex problems. We argue that understanding interactive effects between forest pathogens and global warming, globalization, and land-use changes may benefit from a functional ecology mindset. Traits can be more informative about ecological functions than species inventories and may deliver a more mechanistic description of forest disease. Myriad microbes with pathogenic potential interact with forest ecosystems at different organizational levels. Elucidation of functional traits may enable the microbial complexity to be reduced into manageable categories with predictive power. In this review, we propose guidelines that allow the research community to develop a functional forest pathology approach. We suggest new angles by which functional questions can be used to resolve burning issues on tree disease. Building up functional databases for pathogenicity is key to implementing these approaches.

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2020-08-25
2024-12-12
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Literature Cited

  1. 1.
    Alexander HM. 2010. Disease in natural plant populations, communities, and ecosystems: insights into ecological and evolutionary processes. Plant Dis 94:492–503
    [Google Scholar]
  2. 2.
    Andrew M, Barua R, Short SM, Kohn LM 2012. Evidence for a common toolbox based on necrotrophy in a fungal lineage spanning necrotrophs, biotrophs, endophytes, host generalists and specialists. PLOS ONE 7:e29943
    [Google Scholar]
  3. 3.
    Bass D, Stentiford GD, Wang H-C, Koskella B, Tyler CR 2019. The pathobiome in animal and plant diseases. Trends Ecol. Evol. 34:996–1008
    [Google Scholar]
  4. 4.
    Bihon W, Slippers B, Burgess T, Wingfield MJ, Wingfield BD 2011. Sources of Diplodia pinea endophytic infections in Pinus patula and P. radiata seedlings in South Africa. For. Pathol. 41:370–75
    [Google Scholar]
  5. 5.
    Bjelke U, Boberg J, Oliva J, Tattersdill K, McKie BG 2016. Dieback of riparian alder caused by the Phytophthora alni complex: projected consequences for stream ecosystems. Freshw. Biol. 61:565–79
    [Google Scholar]
  6. 6.
    Blackburn TM, Pysek P, Bacher S, Carlton JT, Duncan RP et al. 2011. A proposed unified framework for biological invasions. Trends Ecol. Evol. 26:333–39
    [Google Scholar]
  7. 7.
    Boddy L. 2000. Interspecific combative interactions between wood-decaying basidiomycetes. FEMS Microbiol. Ecol. 31:185–94
    [Google Scholar]
  8. 8.
    Brasier C. 2000. The rise of the hybrid fungi. Nature 405:134–35
    [Google Scholar]
  9. 9.
    Cadotte MW, Tucker CM. 2017. Should environmental filtering be abandoned. Trends Ecol. Evol. 32:429–37
    [Google Scholar]
  10. 10.
    Connell JH. 1971. On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. Proceedings of the Advanced Study Institute on Dynamics of Numbers in Populations PJ Den Boer, GR Gradwell 298–312 Wageningen, Neth.: Cent. Agric. Publ. Doc.
    [Google Scholar]
  11. 11.
    Dalman K, Himmelstrand K, Olson Å, Lind M, Brandström-Durling M, Stenlid J 2013. A genome-wide association study identifies genomic regions for virulence in the non-model organism Heterobasidion annosum s.s. PLOS ONE 8:e53525
    [Google Scholar]
  12. 12.
    Dawson SK, Boddy L, Halbwachs H, Bässler C, Andrew C et al. 2019. Handbook for the measurement of macrofungal functional traits: a start with basidiomycete wood fungi. Funct. Ecol. 33:372–87
    [Google Scholar]
  13. 13.
    De Bie T, Cristianini N, Demuth JP, Hahn MW 2006. CAFE: a computational tool for the study of gene family evolution. Bioinformatics 22:1269–71
    [Google Scholar]
  14. 14.
    de Wit PJGM, van der Burgt A, Ökmen B, Stergiopoulos I, Abd-Elsalam KA et al. 2012. 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 8:e1003088
    [Google Scholar]
  15. 15.
    Dhillon B, Feau N, Aerts AL, Beauseigle S, Bernier L et al. 2015. Horizontal gene transfer and gene dosage drives adaptation to wood colonization in a tree pathogen. PNAS 112:3451–56
    [Google Scholar]
  16. 16.
    Dove NC, Hart SC. 2017. Fire reduces fungal species richness and in situ mycorrhizal colonization: a meta-analysis. Fire Ecol 13:37–65
    [Google Scholar]
  17. 17.
    Dubey M, Jensen DF, Karlsson M 2016. The ABC transporter ABCG29 is involved in H2O2 tolerance and biocontrol traits in the fungus Clonostachys rosea. Mol. Genet. . Genom 291:677–86
    [Google Scholar]
  18. 18.
    Duffy JE. 2002. Biodiversity and ecosystem function: the consumer connection. Oikos 99:201–19
    [Google Scholar]
  19. 19.
    Dunstan WA, Howard K, Hardy GES, Burgess TI 2016. An overview of Australia's Phytophthora species assemblage in natural ecosystems recovered from a survey in Victoria. IMA Fungus 7:47–58
    [Google Scholar]
  20. 20.
    Enderle R, Sander F, Metzler B 2017. Temporal development of collar necroses and butt rot in association with ash dieback. iForest Biogeosci. For. 10:529–36
    [Google Scholar]
  21. 21.
    Floudas D, Binder M, Riley R, Barry K, Blanchette RA et al. 2012. The paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336:1715–19
    [Google Scholar]
  22. 22.
    Gilbert GS. 2002. Evolutionary ecology of plant diseases in natural ecosystems. Annu. Rev. Phytopathol. 40:13–43
    [Google Scholar]
  23. 23.
    Gilbert GS, Webb CO. 2007. Phylogenetic signal in plant pathogen–host range. PNAS 104:4979–83
    [Google Scholar]
  24. 24.
    Giraud T, Lorys M, Villaréal MA, Austerlitz F, Gac ML, Lavigne C 2006. Importance of the life cycle in sympatric host race formation and speciation of pathogens. Phytopathology 96:280–87
    [Google Scholar]
  25. 25.
    Golan JJ, Pringle A. 2017. Long-distance dispersal of fungi. Microbiol. Spectr. 5: FUNK-0047-2016
    [Google Scholar]
  26. 26.
    Guidot A, Johannesson H, Dahlberg A, Stenlid J 2003. Parental tracking in the postfire wood decay ascomycete Daldinia loculata using highly variable nuclear gene loci. Mol. Ecol. 12:1717–30
    [Google Scholar]
  27. 27.
    Hallin S, Jones CM, Schloter M, Philippot L 2009. Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. ISME J 3:597–605
    [Google Scholar]
  28. 28.
    Hansen EM, Goheen EM. 2000. Phellinus weirii and other native root pathogens as determinants of forest structure and process in western North America. Annu. Rev. Phytopathol. 38:515–39
    [Google Scholar]
  29. 28a.
    Hansen EM, Stone JK, Capitano BR, Rosso P, Sutton Wet al 2000. Incidence and impact of Swiss needle cast in forest plantations of Douglas-fir in coastal Oregon. Plant Dis 84:77378
    [Google Scholar]
  30. 29.
    Hicke JA, Allen CD, Desai AR, Dietze MC, Hall RJ et al. 2012. Effects of biotic disturbances on forest carbon cycling in the United States and Canada. Glob. Change Biol. 18:7–34
    [Google Scholar]
  31. 30.
    Hill SB, Mallik AU, Chen HYH 2005. Canopy gap disturbance and succession in trembling aspen dominated boreal forests in northeastern Ontario. Can. J. For. Res. 35:1942–51
    [Google Scholar]
  32. 31.
    Hintikka V. 1970. Selective effect of terpenes on wood-decomposing Hymenomycetes. Karstenia 11:28–32
    [Google Scholar]
  33. 32.
    Holmer L, Stenlid J. 1997. Competitive hierarchies of wood decomposing basidiomycetes in artificial systems based on variable inoculum sizes. Oikos 79:77–84
    [Google Scholar]
  34. 33.
    Huot B, Yao J, Montgomery BL, He SY 2014. Growth-defense tradeoffs in plants: a balancing act to optimize fitness. Mol. Plant 7:1267–87
    [Google Scholar]
  35. 34.
    Ihrmark K, Asmail N, Ubhayasekera W, Melin P, Stenlid J, Karlsson M 2010. Comparative molecular evolution of Trichoderma chitinases in response to mycoparasitic interactions. Evol. Bioinform. Online 6:1–26
    [Google Scholar]
  36. 35.
    Janzen DH. 1970. Herbivores and the number of tree species in tropical forests. Am. Nat. 104:501–28
    [Google Scholar]
  37. 36.
    Jenkins MA, Jose S, White PS 2007. Impacts of an exotic disease and vegetation change on foliar calcium cycling in Appalachian forests. Ecol. Appl. 17:869–81
    [Google Scholar]
  38. 37.
    Jung T, Orlikowski L, Henricot B, Abad-Campos P, Aday AG et al. 2016. Widespread Phytophthora infestations in European nurseries put forest, semi-natural and horticultural ecosystems at high risk of Phytophthora diseases. For. Pathol. 43:134–63
    [Google Scholar]
  39. 38.
    Jönsson MT, Thor G. 2012. Estimating coextinction risks from epidemic tree death: affiliate lichen communities among diseased host tree populations of Fraxinus excelsior. . PLOS ONE 7:e45701
    [Google Scholar]
  40. 39.
    Karlsson M, Durling MB, Choi J, Kosawang C, Lackner G et al. 2015. Insights on the evolution of mycoparasitism from the genome of Clonostachys rosea. Genome Biol. Evol 7:465–80
    [Google Scholar]
  41. 40.
    Kempeneers P, Sedano F, Seebach L, Strobl P, San-Miguel-Ayanz J 2012. Data fusion of different spatial resolution remote sensing images applied to forest type mapping. IEEE Trans. Geosci. Remote Sens. 49:4977–86
    [Google Scholar]
  42. 41.
    Lamanna C, Blonder B, Violle C, Kraft NJB, Sandel B et al. 2014. Functional trait space and the latitudinal diversity gradient. PNAS 111:13745–50
    [Google Scholar]
  43. 42.
    Lavorel S, Garnier E. 2002. Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail. Funct. Ecol. 16:545–56
    [Google Scholar]
  44. 43.
    Loo JA. 2009. Ecological impacts of non-indigenous invasive fungi as forest pathogens. Biol. Invasions 11:81–96
    [Google Scholar]
  45. 44.
    Lovett GM, Arthur MA, Weathers KC, Griffin JM 2010. Long-term changes in forest carbon and nitrogen cycling caused by an introduced pest/pathogen complex. Ecosystems 13:1188–200
    [Google Scholar]
  46. 45.
    Lovett GM, Canham CD, Arthur MA, Weathers KC, Fitzhugh RD 2006. Forest ecosystem responses to exotic pests and pathogens in eastern North America. BioScience 56:395–405
    [Google Scholar]
  47. 46.
    Mangan SA, Schnitzer SA, Herre EA, Mack KML, Valencia MC et al. 2010. Negative plant–soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466:752–55
    [Google Scholar]
  48. 47.
    Manion PD. 1981. Tree Disease Concepts Englewood Cliffs, NJ: Prentice Hall
    [Google Scholar]
  49. 48.
    Marzluf GA. 1997. Genetic regulation of nitrogen metabolism in the fungi. Microbiol. Mol. Biol. Rev. 61:17–32
    [Google Scholar]
  50. 49.
    Mason NWH, Mouillot D, Lee WG, Wilson JB 2005. Functional richness, functional evenness and functional divergence: the primary components of functional diversity. Oikos 111:112–18
    [Google Scholar]
  51. 50.
    Matson PA, Boone RD. 1984. Natural disturbance and nitrogen mineralization: wave-form dieback of mountain hemlock in the Oregon Cascades. Ecology 65:1511–16
    [Google Scholar]
  52. 51.
    McGill BJ, Enquist BJ, Weiher E, Westoby M 2006. Rebuilding community ecology from functional traits. Trends Ecol. Evol. 21:178–85
    [Google Scholar]
  53. 52.
    Mitchell RJ, Beaton JK, Bellamy PE, Broome A, Chetcuti J et al. 2014. Ash dieback in the UK: a review of the ecological and conservation implications and potential management options. Biol. Conserv. 175:95–109
    [Google Scholar]
  54. 53.
    Mitchell RJ, Hewison RL, Hester AJ, Broome A, Kirby KJ 2016. Potential impacts of the loss of Fraxinus excelsior (Oleaceae) due to ash dieback on woodland vegetation in Great Britain. N. J. Bot. 6:2–15
    [Google Scholar]
  55. 54.
    Müller MM, Hamberg L, Kuskeri J, LaPorta N, Pavlov I, Korhonen K 2015. Respiration rate determinations suggest Heterobasidion parviporum subpopulations have potential to adapt to global warming. For. Pathol. 45:515–24
    [Google Scholar]
  56. 55.
    Munck IA, Smith DR, Sickley T, Stanosz GR 2009. Site-related influences on cone-borne inoculum and asymptomatic persistence of Diplodia shoot blight fungi on or in mature red pines. For. Ecol. Manag. 257:812–19
    [Google Scholar]
  57. 56.
    Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L et al. 2016. FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–48
    [Google Scholar]
  58. 57.
    Oliva J, Boberg JB, Hopkins AJ, Stenlid J 2013. Concepts of epidemiology of forest diseases. Infectious Forest Diseases P Gonthier, G Niccolotti 1–28 Wallingford, UK: CABI
    [Google Scholar]
  59. 58.
    Oliva J, Stenlid J, Martínez-Vilalta J 2014. The effect of fungal pathogens on the water and carbon economy of trees: implications for drought-induced mortality. New Phytol 203:1028–35
    [Google Scholar]
  60. 59.
    O'Malley MA. 2008. “Everything is everywhere: but the environment selects”: ubiquitous distribution and ecological determinism in microbial biogeography. Stud. Hist. Philos. Sci. Part C 39:314–25
    [Google Scholar]
  61. 60.
    Päivinen R, Lehikoinen M, Schuck A, Häme T, Väätäinen S et al. 2001. Combining Earth observation data and forest statistics EFI Res. Rep. 14, Eur. For. Inst Joensuu, Finl:.
    [Google Scholar]
  62. 61.
    Persson Y, Ihrmark K, Stenlid J 2011. Do bark beetles facilitate the establishment of rot fungi in Norway spruce. Fung. Ecol. 4:262–69
    [Google Scholar]
  63. 62.
    Philibert A, Desprez-Loustau M-L, Fabre B, Frey P, Halkett F et al. 2011. Predicting invasion success of forest pathogenic fungi from species traits. J. Appl. Ecol. 48:1381–90
    [Google Scholar]
  64. 63.
    Philippot L, Čuhel J, Saby NPA, Chèneby D, Chroňáková A et al. 2009. Mapping field-scale spatial patterns of size and activity of the denitrifier community. Environ. Microbiol. 11:1518–26
    [Google Scholar]
  65. 64.
    Rayner ADM, Boddy L. 1988. Decomposition of Wood: Its Biology and Ecology Chichester, UK: John Wiley
    [Google Scholar]
  66. 65.
    Redondo MA, Boberg J, Olsson CH, Oliva J 2015. Winter conditions correlate with Phytophthora alni subspecies distribution in Southern Sweden. Phytopathology 105:1191–97
    [Google Scholar]
  67. 66.
    Redondo MA, Boberg J, Stenlid J, Oliva J 2018. Contrasting distribution patterns between aquatic and terrestrial Phytophthora species along a climatic gradient are linked to functional traits. ISME J 12:2967–80
    [Google Scholar]
  68. 67.
    Redondo MA, Boberg J, Stenlid J, Oliva J 2018. Functional traits associated with the establishment of introduced Phytophthora spp. in Swedish forests. J. Appl. Ecol. 55:1538–52
    [Google Scholar]
  69. 68.
    Redondo MA, Stenlid J, Oliva J 2020. Genetic variation explains changes in susceptibility in a naïve host against an invasive forest pathogen: the case of alder and the Phytophthora alni complex. Phytopathology 110:2517–25
    [Google Scholar]
  70. 68a.
    Roll-Hansen F 1989. Phacidium infestans. A literature review. Eur. J. For. Pathol 19:23750
    [Google Scholar]
  71. 69.
    Schmera D, Heino J, Podani J, Erős T, Dolédec S 2017. Functional diversity: a review of methodology and current knowledge in freshwater macroinvertebrate research. Hydrobiologia 787:27–44
    [Google Scholar]
  72. 70.
    Schuck A, Van Brusselen J, Päivinen R, Häme T, Kennedy P, Folving S 2002. Compilation of a calibrated European forest map derived from NOAA-AVHRR data EFI Intern. Rep. 13 Eur. For. Inst., Joensuu, Finl.
    [Google Scholar]
  73. 71.
    Sherwood P, Villari C, Capretti P, Bonello P 2015. Mechanisms of induced susceptibility to Diplodia tip blight in drought-stressed Austrian pine. Tree Physiol 35:549–62
    [Google Scholar]
  74. 72.
    Slippers B, Burgess T, Pavlic D, Ahumada R, Maleme H et al. 2009. A diverse assemblage of Botryosphaeriaceae infect Eucalyptus in native and non-native environments. South. For. J. For. Sci. 71:101–10
    [Google Scholar]
  75. 73.
    Stenlid J, Oliva J. 2016. Phenotypic interactions between tree hosts and invasive forest pathogens in the light of globalization and climate change. Philos. Trans. R. Soc. B 371:20150455
    [Google Scholar]
  76. 74.
    Stukenbrock EH, McDonald BA. 2008. The origins of plant pathogens in agro-ecosystems. Annu. Rev. Phytopathol. 46:75–100
    [Google Scholar]
  77. 75.
    Terhonen E, Blumenstein K, Kovalchuk A, Asiegbu FO 2019. Forest tree microbiomes and associated fungal endophytes: functional roles and impact on forest health. Forests 10:42
    [Google Scholar]
  78. 76.
    Thrall PH, Barrett LG, Dodds PN, Burdon JJ 2016. Epidemiological and evolutionary outcomes in gene-for-gene and matching allele models. Front. Plant Sci. 6:1084
    [Google Scholar]
  79. 77.
    Tollenaere C, Susi H, Laine A-L 2016. Evolutionary and epidemiological implications of multiple infection in plants. Trends Plant Sci 21:80–90
    [Google Scholar]
  80. 78.
    Treseder KK, Lennon JT. 2015. Fungal traits that drive ecosystem dynamics on land. Microbiol. Mol. Biol. Rev. 79:243–62
    [Google Scholar]
  81. 79.
    Tzelepis G, Karlsson M. 2019. Killer toxin-like chitinases in filamentous fungi: structure, regulation and potential roles in fungal biology. Fungal Biol. Rev. 33:123–32
    [Google Scholar]
  82. 80.
    Van Der Heijden MGA, Scheublin TR 2007. Functional traits in mycorrhizal ecology: their use for predicting the impact of arbuscular mycorrhizal fungal communities on plant growth and ecosystem functioning. New Phytol 174:244–50
    [Google Scholar]
  83. 81.
    van der Linde S, Suz LM, Orme CDL, Cox F, Andreae H et al. 2018. Environment and host as large-scale controls of ectomycorrhizal fungi. Nature 558:243–48
    [Google Scholar]
  84. 82.
    van der Wal A, Ottosson E, de Boer W 2015. Neglected role of fungal community composition in explaining variation in wood decay rates. Ecology 96:124–33
    [Google Scholar]
  85. 83.
    Wapinski I, Pfeffer A, Friedman N, Regev A 2007. Natural history and evolutionary principles of gene duplication in fungi. Nature 449:54–61
    [Google Scholar]
  86. 84.
    Waring RH, Cromack K, Matson PA, Boone RD, Stafford SG 1987. Responses to pathogen-induced disturbance: decomposition, nutrient availability, and tree vigour. Forestry 60:219–27
    [Google Scholar]
  87. 85.
    van der Does HC, Rep M 2017. Adaptation to the host environment by plant-pathogenic fungi. Annu. Rev. Phytopathol. 55:427–50
    [Google Scholar]
  88. 86.
    Vasiliauskas R, Stenlid J. 2001. Homothallism in the postfire ascomycete Rhizina undulata. . Mycologia 93:447–52
    [Google Scholar]
  89. 87.
    Vaumourin E, Laine A-L. 2018. Role of temperature and coinfection in mediating pathogen life-history traits. Front. Plant Sci. 9:1670
    [Google Scholar]
  90. 88.
    Vetukuri RR, Tripathy S, Malar CM, Panda A, Kushwaha SK et al. 2018. Draft genome sequence for the tree pathogen Phytophthora plurivora. Genome Biol. Evol 10:2432–42
    [Google Scholar]
  91. 89.
    Violle C, Navas M-L, Vile D, Kazakou E, Fortunel C et al. 2007. Let the concept of trait be functional. ! Oikos 116:882–92
    [Google Scholar]
  92. 90.
    Zanne AE, Abarenkov K, Afkhami ME, Aguilar-Trigueros CA, Bates S et al. 2020. Fungal functional ecology: bringing a trait-based approach to plant-associated fungi. Biol. Rev. 95:2409–33
    [Google Scholar]
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