1932

Abstract

Tree planting and natural regeneration contribute to the ongoing effort to restore Earth's forests. Our review addresses how the plant microbiome can enhance the survival of planted and naturally regenerating seedlings and serve in long-term forest carbon capture and the conservation of biodiversity. We focus on fungal leaf endophytes, ubiquitous defensive symbionts that protect against pathogens. We first show that fungal and oomycetous pathogen richness varies greatly for tree species native to the United States ( = 0–876 known pathogens per US tree species), with nearly half of tree species either without pathogens in these major groups or with unknown pathogens. Endophytes are insurance against the poorly known and changing threat of tree pathogens. Next, we review studies of plant phyllosphere feedback, but knowledge gaps prevent us from evaluating whether adding conspecific leaf litter to planted seedlings promotes defensive symbiosis, analogous to adding soil to promote positive feedback. Finally, we discuss research priorities for integrating the plant microbiome into efforts to expand Earth's forests.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-021320-010717
2022-08-26
2024-12-11
Loading full text...

Full text loading...

/deliver/fulltext/phyto/60/1/annurev-phyto-021320-010717.html?itemId=/content/journals/10.1146/annurev-phyto-021320-010717&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Adame-Álvarez R-M, Mendiola-Soto J, Heil M 2014. Order of arrival shifts endophyte-pathogen interactions in bean from resistance induction to disease facilitation. FEMS Microbiol. Lett. 355:2100–7
    [Google Scholar]
  2. 2.
    Aerts R, Honnay O. 2011. Forest restoration, biodiversity and ecosystem functioning. BMC Ecol 11:129
    [Google Scholar]
  3. 3.
    Agrios GN. 2005. Plant Pathology Cambridge, MA: Acad. Press. , 5th ed..
    [Google Scholar]
  4. 4.
    Arnold AE, Lutzoni F. 2007. Diversity and host range of foliar fungal endophytes: Are tropical leaves biodiversity hotspots?. Ecology 88:3541–49
    [Google Scholar]
  5. 5.
    Arnold AE, Mejía LC, Kyllo D, Rojas EI, Maynard Z et al. 2003. Fungal endophytes limit pathogen damage in a tropical tree. PNAS 100:2615649–54
    [Google Scholar]
  6. 6.
    Asplund J, Hustoft E, Nybakken L, Ohlson M, Lie MH. 2018. Litter impair spruce seedling emergence in beech forests: a litter manipulation experiment. Scand. J. For. Res. 33:4332–37
    [Google Scholar]
  7. 7.
    Averill C, Turner BL, Finzi AC. 2014. Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505:7484543–45
    [Google Scholar]
  8. 8.
    Baldrian P. 2016. Forest microbiome: diversity, complexity and dynamics. FEMS Microbiol. Rev. 41:2109–30
    [Google Scholar]
  9. 9.
    Barge EG, Leopold DR, Peay KG, Newcombe G, Busby PE. 2019. Differentiating spatial from environmental effects on foliar fungal communities of Populus trichocarpa. J. Biogeogr. 46:92001–11
    [Google Scholar]
  10. 10.
    Barge EG, Leopold DR, Rojas A, Vilgalys R, Busby PE. 2022. Phylogenetic conservatism of mycoparasitism and its contribution to pathogen antagonism. Mol. Ecol. 31:103018–30
    [Google Scholar]
  11. 11.
    Barnes I, Fourie A, Wingfield MJ, Harrington TC, McNew DL et al. 2018. New Ceratocystis species associated with rapid death of Metrosideros polymorpha in Hawai'i. Persoonia 40:1154–81
    [Google Scholar]
  12. 12.
    Baskin CC, Baskin JM. 1998. Seeds: Ecology, Biogeography, and Evolution of Dormancy and Germination San Diego: Academic
    [Google Scholar]
  13. 13.
    Bebber DP, Gurr SJ. 2015. Crop-destroying fungal and oomycete pathogens challenge food security. Fungal Genet. Biol. 74:62–64
    [Google Scholar]
  14. 14.
    Beech E, Rivers M, Oldfield S, Smith PP. 2017. GlobalTreeSearch: the first complete global database of tree species and country distributions. J. Sustain. For. 36:5454–89
    [Google Scholar]
  15. 15.
    Benítez M-S, Hersh MH, Vilgalys R, Clark JS. 2013. Pathogen regulation of plant diversity via effective specialization. Trends Ecol. Evol. 28:12705–11
    [Google Scholar]
  16. 16.
    Bever JD, Mangan SA, Alexander HM. 2015. Maintenance of plant species diversity by pathogens. Annu. Rev. Ecol. Evol. Syst. 46:305–25
    [Google Scholar]
  17. 17.
    Bever JD, Schultz PA, Miller RM, Gades L, Jastrow JD. 2003. Prairie mycorrhizal fungi inoculant may increase native plant diversity on restored sites (Illinois). Ecol. Restor. 21:311–12
    [Google Scholar]
  18. 18.
    Bever JD, Westover KM, Antonovics J. 1997. Incorporating the soil community into plant population dynamics: the utility of the feedback approach. J. Ecol. 85:5561–73
    [Google Scholar]
  19. 19.
    Blanco-García A, Sáenz-Romero C, Martorell C, Alvarado-Sosa P, Lindig-Cisneros R. 2011. Nurse-plant and mulching effects on three conifer species in a Mexican temperate forest. Ecol. Eng. 37:6994–98
    [Google Scholar]
  20. 20.
    Bogdanski BEC, Cruickshank M, Mario Di Lucca C, Becker E 2018. Stumping out tree root disease: an economic analysis of controlling root disease, including its effects on carbon storage in southern British Columbia. For. Ecol. Manag. 409:129–47
    [Google Scholar]
  21. 21.
    Brasier CM. 2008. The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathol 57:5792–808
    [Google Scholar]
  22. 22.
    Bremer LL, Farley KA. 2010. Does plantation forestry restore biodiversity or create green deserts? A synthesis of the effects of land-use transitions on plant species richness. Biodivers. Conserv. 19:143893–915
    [Google Scholar]
  23. 23.
    Brinck K, Fischer R, Groeneveld J, Lehmann S, Dantas De Paula M et al. 2017. High resolution analysis of tropical forest fragmentation and its impact on the global carbon cycle. Nat. Commun. 8:114855
    [Google Scholar]
  24. 24.
    Brown PE. 1918. Soil inoculation Rep. 43 Agric. Exp. Stn. Iowa State Coll. Agric. Mech. Arts Ames, IA:
    [Google Scholar]
  25. 25.
    Brown SP, Leopold DR, Busby PE. 2018. Protocols for investigating the leaf mycobiome using high-throughput DNA sequencing. Methods Mol. Biol. 1848:39–51
    [Google Scholar]
  26. 26.
    Brunner K, Zeilinger S, Ciliento R, Woo SL, Lorito M et al. 2005. Improvement of the fungal biocontrol agent Trichoderma atroviride to enhance both antagonism and induction of plant systemic disease resistance. Appl. Environ. Microbiol. 71:73959–65
    [Google Scholar]
  27. 27.
    Busby PE, Aime MC, Newcombe G 2012. Foliar pathogens of Populus angustifolia are consistent with a hypothesis of Beringian migration into North America. Fungal Biol 116:7792–801
    [Google Scholar]
  28. 28.
    Busby PE, Peay KG, Newcombe G. 2016. Common foliar fungi of Populus trichocarpa modify Melampsora rust disease severity. New Phytol 209:41681–92
    [Google Scholar]
  29. 29.
    Busby PE, Ridout M, Newcombe G. 2016. Fungal endophytes: modifiers of plant disease. Plant Mol. Biol. 90:6645–55
    [Google Scholar]
  30. 30.
    Cervantes D, Ridout M, Nischwitz C, Newcombe G. 2021. Adult plant resistance to white rust in Lunaria annua. Phytopathol. Mediterr. 60:2381–85
    [Google Scholar]
  31. 31.
    Chen T, Nomura K, Wang X, Sohrabi R, Xu J et al. 2020. A plant genetic network for preventing dysbiosis in the phyllosphere. Nature 580:7805653–57
    [Google Scholar]
  32. 32.
    Chock MK, Hoyt BK, Amend AS. 2021. Mycobiome transplant increases resistance to Austropuccinia psidii in an endangered Hawaiian plant. Phytobiomes J 5:3326–34
    [Google Scholar]
  33. 33.
    Christian N, Herre EA, Mejia LC, Clay K. 2017. Exposure to the leaf litter microbiome of healthy adults protects seedlings from pathogen damage. Proc. R. Soc. B 284:185820170641
    [Google Scholar]
  34. 34.
    Compant S, Duffy B, Nowak J, Clément C, Barka EA. 2005. Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl. Environ. Microbiol. 71:94951–59
    [Google Scholar]
  35. 35.
    Crawford KM, Bauer JT, Comita LS, Eppinga MB, Johnson DJ et al. 2019. When and where plant-soil feedback may promote plant coexistence: a meta-analysis. Ecol. Lett. 22:81274–84
    [Google Scholar]
  36. 36.
    Crowther TW, Glick HB, Covey KR, Bettigole C, Maynard DS et al. 2015. Mapping tree density at a global scale. Nature 525:7568201–5
    [Google Scholar]
  37. 37.
    Darwin C. 2008. On the Origin of Species New York: Oxford Univ. Press
    [Google Scholar]
  38. 38.
    Dastogeer KMG, Tumpa FH, Sultana A, Akter MA, Chakraborty A. 2020. Plant microbiome: an account of the factors that shape community composition and diversity. Curr. Plant Biol. 23:100161
    [Google Scholar]
  39. 39.
    DeLong RL, Lewis KJ, Simard SW, Gibson S. 2002. Fluorescent pseudomonad population sizes baited from soils under pure birch, pure Douglas-fir, and mixed forest stands and their antagonism toward Armillaria ostoyae in vitro. Can. J. For. Res. 32:122146–59
    [Google Scholar]
  40. 40.
    DeWoody J, Rowe CA, Hipkins VD, Mock KE. 2008.. “ Pando” lives: molecular genetic evidence of a giant aspen clone in central Utah. West. N. Am. Nat. 68:4493–97
    [Google Scholar]
  41. 41.
    Egan CP, Koko JH, Muir CD, Zahn G, Swift SOI et al. 2021. Restoration of the mycobiome of the endangered Hawaiian mint Phyllostegia kaalaensis increases its resistance to a common powdery mildew. Fungal Ecol 52:101070
    [Google Scholar]
  42. 42.
    Eitzen K, Sengupta P, Kroll S, Kemen E, Doehlemann G 2021. A fungal member of the Arabidopsis thaliana phyllosphere antagonizes Albugo laibachii via a GH25 lysozyme. eLife 10:e65306
    [Google Scholar]
  43. 43.
    Enebak SA, Carey WA. 2000. Evidence for induced systemic protection to fusiform rust in loblolly pine by plant growth-promoting rhizobacteria. Plant Dis 84:3306–8
    [Google Scholar]
  44. 44.
    Ernfors M, Rütting T, Klemedtsson L. 2011. Increased nitrous oxide emissions from a drained organic forest soil after exclusion of ectomycorrhizal mycelia. Plant Soil 343:1–2161–70
    [Google Scholar]
  45. 45.
    Feng X, Chen L, Zhou J, Yang Z-P, Dong X-F, Zhang H-B. 2019. Plant–soil–foliage feedbacks on seed germination and seedling growth of the invasive plant Ageratina adenophora. Proc. R. Soc. B. 286:1917
    [Google Scholar]
  46. 46.
    Fenner M, Thompson K. 2005. The Ecology of Seeds New York: Cambridge Univ. Press
    [Google Scholar]
  47. 47.
    Flor HH. 1971. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9:275–96
    [Google Scholar]
  48. 48.
    Fonseca JP, Mysore KS. 2019. Genes involved in nonhost disease resistance as a key to engineer durable resistance in crops. Plant Sci 279:108–16
    [Google Scholar]
  49. 49.
    Franklin JF, Donato DC. 2020. Variable retention harvesting in the Douglas-fir region. Ecol. Process. 9:18
    [Google Scholar]
  50. 50.
    Ganley RJ, Brunsfeld SJ, Newcombe G. 2004. A community of unknown, endophytic fungi in western white pine. PNAS 101:2710107–12
    [Google Scholar]
  51. 51.
    Ganley RJ, Newcombe G. 2006. Fungal endophytes in seeds and needles of Pinus monticola. Mycol. Res. 110:3318–27
    [Google Scholar]
  52. 52.
    Ganley RJ, Sniezko RA, Newcombe G. 2008. Endophyte-mediated resistance against white pine blister rust in Pinus monticola. For. Ecol. Manag. 255:72751–60
    [Google Scholar]
  53. 53.
    Gatti LV, Basso LS, Miller JB, Gloor M, Gatti Domingues L et al. 2021. Amazonia as a carbon source linked to deforestation and climate change. Nature 595:7867388–93
    [Google Scholar]
  54. 54.
    Gautam H, Sharma I, Kumar R. 2014. Jadav Molai Payeng: the “Forest Man of India. .” Curr. Sci. 106:4499
    [Google Scholar]
  55. 55.
    Gomes T, Pereira JA, Benhadi J, Lino-Neto T, Baptista P 2018. Endophytic and epiphytic phyllosphere fungal communities are shaped by different environmental factors in a Mediterranean ecosystem. Microb. Ecol. 76:3668–79
    [Google Scholar]
  56. 56.
    Griffin EA, Carson WP. 2018. Tree endophytes: cryptic drivers of tropical forest diversity. Endophytes of Forest Trees AM Pirttilä, AC Frank 63–103 Cham, Switz: Springer
    [Google Scholar]
  57. 57.
    Hansen AJ, Burns P, Ervin J, Goetz SJ, Hansen M et al. 2020. A policy-driven framework for conserving the best of Earth's remaining moist tropical forests. Nat. Ecol. Evol. 4:101377–84
    [Google Scholar]
  58. 58.
    Hansen AJ, Noble BP, Veneros J, East A, Goetz SJ et al. 2021. Toward monitoring forest ecosystem integrity within the post-2020 Global Biodiversity Framework. Conserv. Lett. 14:4e12822
    [Google Scholar]
  59. 59.
    Harper JL. 2010. Population Biology of Plants London: Acad. Press
    [Google Scholar]
  60. 60.
    Harrison JG, Forister ML, Parchman TL, Koch GW. 2016. Vertical stratification of the foliar fungal community in the world's tallest trees. Am. J. Bot. 103:122087–95
    [Google Scholar]
  61. 61.
    Hassani MA, Durán P, Hacquard S 2018. Microbial interactions within the plant holobiont. Microbiome 6:158
    [Google Scholar]
  62. 62.
    Hatch AB. 1936. The role of mycorrhizae in afforestation. J. For. 34:122–29
    [Google Scholar]
  63. 63.
    Heijden MGA, Martin FM, Selosse M, Sanders IR. 2015. Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:41406–23
    [Google Scholar]
  64. 64.
    Helgason T, Daniell TJ, Husband R, Fitter AH, Young JPW. 1998. Ploughing up the wood-wide web?. Nature 394:6692431
    [Google Scholar]
  65. 65.
    Hermann RK, Lavender DP. 1990. Pseudotsuga menziesii (Mirb.) Franco, Douglas-fir. Silv. N. Am. 1:527–40
    [Google Scholar]
  66. 66.
    Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ. 2012. Mycorrhiza-induced resistance and priming of plant defenses. J. Chem. Ecol. 38:6651–64
    [Google Scholar]
  67. 67.
    Keith LM, Hughes RF, Sugiyama LS, Heller WP, Bushe BC, Friday JB 2015. First report of Ceratocystis wilt on ˋŌhiˋa (Metrosideros polymorpha). Plant Dis. 99:91276
    [Google Scholar]
  68. 68.
    Klironomos JN. 2002. Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:688467–70
    [Google Scholar]
  69. 69.
    Kolbert E. 2014. The Sixth Extinction: An Unnatural History New York: Henry Holt
    [Google Scholar]
  70. 70.
    Kosaka H, Aikawa T, Ogura N, Tabata K, Kiyohara T. 2001. Pine wilt disease caused by the pine wood nematode: induced resistance of pine trees by the avirulent isolates of nematode. Eur. J. Plant Pathol. 107:7667–75
    [Google Scholar]
  71. 71.
    Koziol L, Bauer JT, Duell EB, Hickman K, House GL et al. 2021. Manipulating plant microbiomes in the field: Native mycorrhizae advance plant succession and improve native plant restoration. J. Appl. Ecol. In press
    [Google Scholar]
  72. 72.
    Laforest-Lapointe I, Paquette A, Messier C, Kembel SW. 2017. Leaf bacterial diversity mediates plant diversity and ecosystem function relationships. Nature 546:7656145–47
    [Google Scholar]
  73. 73.
    Lajoie G, Kembel SW. 2019. Making the most of trait-based approaches for microbial ecology. Trends Microbiol 27:10814–23
    [Google Scholar]
  74. 74.
    LaManna JA, Mangan SA, Alonso A, Bourg NA, Brockelman WY et al. 2017. Plant diversity increases with the strength of negative density dependence at the global scale. Science 356:63451389–92
    [Google Scholar]
  75. 75.
    Leopold A 1972. A Sand County Almanac and Sketches Here and There New York: Oxford Univ. Press
    [Google Scholar]
  76. 76.
    Leopold DR, Busby PE. 2020. Host genotype and colonist arrival order jointly govern plant microbiome composition and function. Curr. Biol. 30:163260–66.e5
    [Google Scholar]
  77. 77.
    Liu H, Shen G, Ma Z, Yang Q, Xia J et al. 2016. Conspecific leaf litter-mediated effect of conspecific adult neighborhood on early-stage seedling survival in a subtropical forest. Sci. Rep. 6:137830
    [Google Scholar]
  78. 78.
    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 466:7307752–55
    [Google Scholar]
  79. 79.
    Martinez-Vilalta J. 2014. Carbon storage in trees: pathogens have their say. Tree Physiol 34:3215–17
    [Google Scholar]
  80. 80.
    Marx DH. 1969. The influence of ectotrophic mycorrhizal fungi on the resistance of pine roots to pathogenic infections. II. Production, identification, and biological activity of antibiotics produced by Leucopaxillus cerealis var. piceina. . Phytopathology 59:4411–17
    [Google Scholar]
  81. 81.
    Marx DH. 1991. The practical significance of ectomycorrhizae in forest establishment. Marcus Wallenberg Found. Symp. Proc 7:54–90
    [Google Scholar]
  82. 82.
    McLaren MR, Callahan BJ. 2020. Pathogen resistance may be the principal evolutionary advantage provided by the microbiome. Philos. Trans. R. Soc. B 375:180820190592
    [Google Scholar]
  83. 83.
    Mejía LC, Herre EA, Sparks JP, Winter K, García MN et al. 2014. Pervasive effects of a dominant foliar endophytic fungus on host genetic and phenotypic expression in a tropical tree. Front. Microbiol. 5:479
    [Google Scholar]
  84. 84.
    Middleton EL, Bever JD. 2012. Inoculation with a native soil community advances succession in a grassland restoration. Restor. Ecol. 20:2218–26
    [Google Scholar]
  85. 85.
    Middleton EL, Richardson S, Koziol L, Palmer CE, Yermakov Z et al. 2015. Locally adapted arbuscular mycorrhizal fungi improve vigor and resistance to herbivory of native prairie plant species. Ecosphere 6:12art276
    [Google Scholar]
  86. 86.
    Mishra S, Hättenschwiler S, Yang X 2020. The plant microbiome: a missing link for the understanding of community dynamics and multifunctionality in forest ecosystems. Appl. Soil Ecol. 145:103345
    [Google Scholar]
  87. 87.
    Mitchard ETA. 2018. The tropical forest carbon cycle and climate change. Nature 559:7715527–34
    [Google Scholar]
  88. 88.
    Mitchell CE, Power AG. 2003. Release of invasive plants from fungal and viral pathogens. Nature 421:6923625–27
    [Google Scholar]
  89. 89.
    Miyawaki A, Box EO. 2006. The Healing Power of Forests: The Philosophy Behind Restoring Earth's Balance with Native Trees Tokyo: Kosei Publ.
    [Google Scholar]
  90. 90.
    Möhler H, Diekötter T, Bauer GM, Donath TW. 2021. Conspecific and heterospecific grass litter effects on seedling emergence and growth in ragwort (Jacobaea vulgaris). PLOS ONE 16:2e0246459
    [Google Scholar]
  91. 91.
    Mora C, Dousset B, Caldwell IR, Powell FE, Geronimo RC et al. 2017. Global risk of deadly heat. Nat. Clim. Change 7:7501–6
    [Google Scholar]
  92. 92.
    Newcombe G, Fraser SJ, Ridout M, Busby PE. 2020. Leaf endophytes of Populus trichocarpa act as pathogens of neighboring plant species. Front. Microbiol. 11:573056
    [Google Scholar]
  93. 93.
    Newton P, Kinzer AT, Miller DC, Oldekop JA, Agrawal A. 2020. The number and spatial distribution of forest-proximate people globally. One Earth 3:3363–70
    [Google Scholar]
  94. 94.
    Nguyen NH, Hynson NA, Bruns TD. 2012. Stayin’ alive: survival of mycorrhizal fungal propagules from 6-yr-old forest soil. Fungal Ecol 5:6741–46
    [Google Scholar]
  95. 95.
    Nischwitz C, Newcombe G, Anderson CL. 2005. Host specialization of the mycoparasite Eudarluca caricis and its evolutionary relationship to Ampelomyces. Mycol. Res. 109:4421–28
    [Google Scholar]
  96. 96.
    O'Connor B, Bojinski S, Röösli C, Schaepman ME. 2020. Monitoring global changes in biodiversity and climate essential as ecological crisis intensifies. Ecol. Inform. 55:101033
    [Google Scholar]
  97. 97.
    Osono T. 2006. Role of phyllosphere fungi of forest trees in the development of decomposer fungal communities and decomposition processes of leaf litter. Can. J. Microbiol. 52:8701–16
    [Google Scholar]
  98. 98.
    Percy DM, Garver AM, Wagner WL, James HF, Cunningham CW et al. 2008. Progressive island colonization and ancient origin of Hawaiian Metrosideros (Myrtaceae). Proc. R. Soc. B 275:16421479–90
    [Google Scholar]
  99. 99.
    Petrini O. 1991. Fungal endophytes of tree leaves. Microbial Ecology of Leaves JH Andrews, SS Hirano 179–97 New York: Springer
    [Google Scholar]
  100. 100.
    Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM. 2014. Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol. 52:347–75
    [Google Scholar]
  101. 101.
    Piovesan G, Biondi F. 2021. On tree longevity. New Phytol 231:41318–37
    [Google Scholar]
  102. 102.
    Porras-Alfaro A, Bayman P 2011. Hidden fungi, emergent properties: endophytes and microbiomes. Annu. Rev. Phytopathol. 49:291–315
    [Google Scholar]
  103. 103.
    Price JP, Wagner WL. 2018. Origins of the Hawaiian flora: Phylogenies and biogeography reveal patterns of long-distance dispersal. J. Syst. Evol. 56:6600–20
    [Google Scholar]
  104. 104.
    Prigge BA. 2002. A new species of Prunus (Rosaceae) from the Mojave Desert of California. Madroño 49:4285–88
    [Google Scholar]
  105. 105.
    Putkinen A, Siljanen HMP, Laihonen A, Paasisalo I, Porkka K et al. 2021. New insight to the role of microbes in the methane exchange in trees: evidence from metagenomic sequencing. New Phytol 231:2524–36
    [Google Scholar]
  106. 106.
    Raaijmakers JM, Vlami M, de Souza JT. 2002. Antibiotic production by bacterial bioconrol agenets. Antonie Van Leeuwenhoek 81:1–4537–47
    [Google Scholar]
  107. 107.
    Rabiey M, Hailey LE, Roy SR, Grenz K, Al-Zadjali MAS et al. 2019. Endophytes versus tree pathogens and pests: Can they be used as biological control agents to improve tree health?. Eur. J. Plant Pathol. 155:3711–29
    [Google Scholar]
  108. 108.
    Raghavendra AKH, Newcombe G. 2013. The contribution of foliar endophytes to quantitative resistance to Melampsora rust. New Phytol 197:3909–18
    [Google Scholar]
  109. 109.
    Rehfeldt GE. 1989. Ecological adaptations in Douglas-Fir (Pseudotsuga menziesii var. glauca): a synthesis. For. Ecol. Manag. 28:3–4203–15
    [Google Scholar]
  110. 110.
    Ridout M, Newcombe G. 2016. Disease suppression in winter wheat from novel symbiosis with forest fungi. Fungal Ecol 20:40–48
    [Google Scholar]
  111. 111.
    Roberts M, Gilligan CA, Kleczkowski A, Hanley N, Whalley AE, Healey JR. 2020. The effect of forest management options on forest resilience to pathogens. Front. For. Glob. Change 3:7
    [Google Scholar]
  112. 112.
    Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L et al. 2008. Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2:4404–16
    [Google Scholar]
  113. 113.
    Rodriguez RJ, White JF Jr., Arnold AE, Redman RS. 2009. Fungal endophytes: diversity and functional roles. New Phytol 182:2314–30
    [Google Scholar]
  114. 114.
    Rønsted N, Wood KR. 2020. Cyanea kuhihewa: rediscovering one of Hawai'i’s rarest trees. Plants People Planet 2:2107–10
    [Google Scholar]
  115. 115.
    Ross AF. 1961. Systemic acquired resistance induced by localized virus infections in plants. Virology 14:3340–58
    [Google Scholar]
  116. 116.
    Schnitzer SA, Klironomos JN, HilleRisLambers J, Kinkel LL, Reich PB et al. 2011. Soil microbes drive the classic plant diversity-productivity pattern. Ecology 92:2296–303
    [Google Scholar]
  117. 117.
    Simard S. 2021. Finding the Mother Tree: Discovering the Wisdom of the Forest New York: Knopf
    [Google Scholar]
  118. 118.
    Simard SW, Perry DA, Jones MD, Myrold DD, Durall DM, Molina R. 1997. Net transfer of carbon between ectomycorrhizal tree species in the field. Nature 388:6642579–82
    [Google Scholar]
  119. 119.
    Song XP, Richards D, Edwards P, Tan PY. 2017. Benefits of trees in tropical cities. Science 356:63441241
    [Google Scholar]
  120. 120.
    Song YY, Simard SW, Carroll A, Mohn WW, Zeng RS. 2015. Defoliation of interior Douglas-fir elicits carbon transfer and stress signalling to ponderosa pine neighbors through ectomycorrhizal networks. Sci. Rep. 5:18495
    [Google Scholar]
  121. 121.
    Stanke H, Finley AO, Domke GM, Weed AS, MacFarlane DW. 2021. Over half of western United States’ most abundant tree species in decline. Nat. Commun. 12:1451
    [Google Scholar]
  122. 122.
    Steidinger BS, Crowther TW, Liang J, Van Nuland ME, Werner GDA et al. 2019. Climatic controls of decomposition drive the global biogeography of forest-tree symbioses. Nature 569:7756404–8
    [Google Scholar]
  123. 123.
    Sturrock RN, Frankel SJ, Brown AV, Hennon PE, Kliejunas JT et al. 2011. Climate change and forest diseases: climate change and forest diseases. Plant Pathol 60:1133–49
    [Google Scholar]
  124. 124.
    Talbot JM, Bruns TD, Taylor JW, Smith DP, Branco S et al. 2014. Endemism and functional convergence across the North American soil mycobiome. PNAS 111:176341–46
    [Google Scholar]
  125. 125.
    Thomas E, Jalonen R, Loo J, Boshier D, Gallo L et al. 2014. Genetic considerations in ecosystem restoration using native tree species. For. Ecol. Manag. 333:66–75
    [Google Scholar]
  126. 126.
    Thomsen MS, Wernberg T. 2014. On the generality of cascading habitat-formation. Proc. R. Soc. B 281:177720131994
    [Google Scholar]
  127. 127.
    Tilman D, Lehman CL, Thomson KT. 1997. Plant diversity and ecosystem productivity: theoretical considerations. PNAS 94:51857–61
    [Google Scholar]
  128. 128.
    Tilman D, Wedin D, Knops J. 1996. Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature 379:6567718–20
    [Google Scholar]
  129. 129.
    Tinya F, Kovács B, Bidló A, Dima B, Király I et al. 2021. Environmental drivers of forest biodiversity in temperate mixed forests: a multi-taxon approach. Sci. Total Environ. 795:148720
    [Google Scholar]
  130. 130.
    Trivedi P, Leach JE, Tringe SG, Sa T, Singh BK. 2020. Plant-microbiome interactions: from community assembly to plant health. Nat. Rev. Microbiol. 18:11607–21
    [Google Scholar]
  131. 131.
    U'Ren JM, Arnold AE. 2016. Diversity, taxonomic composition, and functional aspects of fungal communities in living, senesced, and fallen leaves at five sites across North America. PeerJ 4:e2768
    [Google Scholar]
  132. 132.
    U'Ren JM, Lutzoni F, Miadlikowska J, Laetsch AD, Arnold AE. 2012. Host and geographic structure of endophytic and endolichenic fungi at a continental scale. Am. J. Bot. 99:5898–914
    [Google Scholar]
  133. 133.
    Vahter T, Bueno CG, Davison J, Herodes K, Hiiesalu I et al. 2020. Co-introduction of native mycorrhizal fungi and plant seeds accelerates restoration of post-mining landscapes. J. Appl. Ecol. 57:91741–51
    [Google Scholar]
  134. 134.
    Van Bael SA, Estrada C, Arnold AE 2017. Foliar endophyte communities and leaf traits in tropical trees. The Fungal Community: Its Organization and Role in the Ecosystem J Dighton, JF White, pp. 79–94 Boca Raton, FL: CRC Press. , 4th ed..
    [Google Scholar]
  135. 135.
    Vannier N, Agler M, Hacquard S. 2019. Microbiota-mediated disease resistance in plants. PLOS Pathog 15:6e1007740
    [Google Scholar]
  136. 136.
    Vazquez-Yanes C, Orozco-Segovia A. 1992. Effects of litter from a tropical rainforest on tree seed germination and establishment under controlled conditions. Tree Physiol 11:4391–400
    [Google Scholar]
  137. 137.
    Veen GF, Fry EL, ten Hooven FC, Kardol P, Morriën E, De Long JR. 2019. The role of plant litter in driving plant-soil feedbacks. Front. Environ. Sci. 7:168
    [Google Scholar]
  138. 138.
    Weller DM. 1988. Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Annu. Rev. Phytopathol. 26:379–407
    [Google Scholar]
  139. 139.
    Werner D. 1992. Symbiosis of Plants and Microbes New York: Chapman & Hall
    [Google Scholar]
  140. 140.
    Whitaker BK, Bauer JT, Bever JD, Clay K. 2017. Negative plant-phyllosphere feedbacks in native Asteraceae hosts: a novel extension of the plant-soil feedback framework. Ecol. Lett. 20:81064–73
    [Google Scholar]
  141. 141.
    Woodcock P, Cottrell JE, Buggs RJA, Quine CP. 2018. Mitigating pest and pathogen impacts using resistant trees: a framework and overview to inform development and deployment in Europe and North America. For. Int. J. For. Res. 91:11–16
    [Google Scholar]
  142. 142.
    Wubs ERJ, Putten WH, Mortimer SR, Korthals GW, Duyts H et al. 2019. Single introductions of soil biota and plants generate long-term legacies in soil and plant community assembly. Ecol. Lett. 22:71145–51
    [Google Scholar]
  143. 143.
    Zahawi RA, Reid JL, Holl KD. 2014. Hidden costs of passive restoration: passive restoration. Restor. Ecol. 22:3284–87
    [Google Scholar]
  144. 144.
    Zahn G, Amend AS. 2017. Foliar microbiome transplants confer disease resistance in a critically-endangered plant. PeerJ 5:e4020
    [Google Scholar]
  145. 145.
    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]
  146. 146.
    Zaret MM, Bauer JT, Clay K, Whitaker BK 2021. Conspecific leaf litter induces negative feedbacks in Asteraceae seedlings. Ecology 102:12e03557
    [Google Scholar]
  147. 147.
    Zilber-Rosenberg I, Rosenberg E. 2008. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol. Rev. 32:5723–35
    [Google Scholar]
  148. 148.
    Zimmerman NB, Vitousek PM. 2012. Fungal endophyte communities reflect environmental structuring across a Hawaiian landscape. PNAS 109:3213022–27
    [Google Scholar]
/content/journals/10.1146/annurev-phyto-021320-010717
Loading
/content/journals/10.1146/annurev-phyto-021320-010717
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error