1932

Abstract

Interactions between plants and microbes have important influences on evolutionary processes, population dynamics, community structure, and ecosystem function. We review the literature to document how climate change may disrupt these ecological interactions and develop a conceptual framework to integrate the pathways of plant-microbe responses to climate over different scales in space and time. We then create a blueprint to aid generalization that categorizes climate effects into changes in the context dependency of plant-microbe pairs, temporal mismatches and altered feedbacks over time, or spatial mismatches that accompany species range shifts. We pair a new graphical model of how plant-microbe interactions influence resistance to climate change with a statistical approach to predictthe consequences of increasing variability in climate. Finally, we suggest pathways through which plant-microbe interactions can affect resilience during recovery from climate disruption. Throughout, we take a forward-looking perspective, highlighting knowledge gaps and directions for future research.

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2020-11-02
2024-04-20
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Literature Cited

  1. Afkhami ME, McIntyre PJ, Strauss SY 2014. Mutualist-mediated effects on species’ range limits across large geographic scales. Ecol. Lett. 17:1265–73
    [Google Scholar]
  2. Alexander JM, Diez JM, Levine JM 2015. Novel competitors shape species’ responses to climate change. Nature 525:515–18
    [Google Scholar]
  3. Araújo MB, Ferri-Yáñez F, Bozinovic F, Marquet PA, Valladares F, Chown SL 2013. Heat freezes niche evolution. Ecol. Lett. 16:1206–19
    [Google Scholar]
  4. Arora P, Riyaz-Ul-Hassan S. 2019. Endohyphal bacteria; the prokaryotic modulators of host fungal biology. Fungal Biol. Rev. 33:72–81
    [Google Scholar]
  5. Bardgett RD, Manning P, Morriën E, De Vries FT 2013. Hierarchical responses of plant-soil interactions to climate change: consequences for the global carbon cycle. J. Ecol. 101:334–43
    [Google Scholar]
  6. Barrett G, Campbell CD, Hodge A 2014. The direct response of the external mycelium of arbuscular mycorrhizal fungi to temperature and the implications for nutrient transfer. Soil Biol. Biochem. 78:109–17
    [Google Scholar]
  7. Beals KK, Moore JA, Kivlin SN, Bayliss SL, Lumibao CY et al. 2020. Predicting plant-soil feedback in the field: competitive interactions may reduce plant growth more than stress or disturbance. Front. Ecol. Evol. 8:191
    [Google Scholar]
  8. Bell-Dereske L, Gao XD, Masiello CA, Sinsabaugh RL, Emery SM, Rudgers JA 2017a. Plant-fungal symbiosis affects litter decomposition during primary succession. Oikos 126:801–11
    [Google Scholar]
  9. Bell-Dereske L, Takacs-Vesbach C, Kivlin SN, Emery SM, Rudgers JA 2017b. Leaf endophytic fungus interacts with precipitation to alter belowground microbial communities in primary successional dunes. FEMS Microbiol. Ecol. 93:fix036
    [Google Scholar]
  10. Bennett JA, Maherali H, Reinhart KO, Lekberg Y, Hart MM, Klironomos J 2017. Plant-soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Science 355:181–84
    [Google Scholar]
  11. Berger S, Sinha AK, Roitsch T 2007. Plant physiology meets phytopathology: plant primary metabolism and plant-pathogen interactions. J. Exp. Bot. 58:4019–26
    [Google Scholar]
  12. Bever JD, Westover KM, Antonovics J 1997. Incorporating the soil community into plant population dynamics: the utility of the feedback approach. J. Ecol. 85:561–73
    [Google Scholar]
  13. Birnbaum C, Bissett A, Thrall PH, Leishman MR 2016. Nitrogen‐fixing bacterial communities in invasive legume nodules and associated soils are similar across introduced and native range populations in Australia. J. Biogeogr. 43:1631–44
    [Google Scholar]
  14. Branco S. 2019. Fungal diversity from communities to genes. Fungal Biol. Rev. 33:225–37
    [Google Scholar]
  15. Busby PE, Ridout M, Newcombe G 2016. Fungal endophytes: modifiers of plant disease. Plant Mol. Biol. 90:645–55
    [Google Scholar]
  16. Cavicchioli R, Ripple WJ, Timmis KN, Azam F, Bakken LR et al. 2019. Scientists’ warning to humanity: microorganisms and climate change. Nat. Rev. Microbiol. 17:569–86
    [Google Scholar]
  17. Che R, Wang S, Wang Y, Xu Z, Wang W et al. 2019. Total and active soil fungal community profiles were significantly altered by six years of warming but not by grazing. Soil Biol. Biochem. 139:107611
    [Google Scholar]
  18. 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 284:20170641
    [Google Scholar]
  19. Classen AT, Sundqvist MK, Henning JA, Newman GS, Moore JAM et al. 2015. Direct and indirect effects of climate change on soil microbial and soil microbial-plant interactions: What lies ahead. ? Ecosphere 6:130
    [Google Scholar]
  20. Connor EW, Sandy M, Hawkes CV 2017. Microbial tools in agriculture require an ecological context: stress-dependent non-additive symbiont interactions. Agron. J. 109:917–26
    [Google Scholar]
  21. 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. 22:1274–84
    [Google Scholar]
  22. Daru BH, Bowman EA, Pfister DH, Arnold AE 2019. A novel proof of concept for capturing the diversity of endophytic fungi preserved in herbarium specimens. Philos. Trans. R. Soc. B 374:20170395
    [Google Scholar]
  23. Datlof EM, Amend AS, Earl K, Hayward J, Morden CW et al. 2017. Uncovering unseen fungal diversity from plant DNA banks. PeerJ 5:e3730
    [Google Scholar]
  24. Davis TS, Bosque-Pérez NA, Foote NE, Magney T, Eigenbrode SD 2015. Environmentally dependent host–pathogen and vector–pathogen interactions in the Barley yellow dwarf virus pathosystem. J. Appl. Ecol. 52:1392–401
    [Google Scholar]
  25. de Nijs EA, Hicks LC, Leizeaga A, Tietema A, Rousk J 2019. Soil microbial moisture dependences and responses to drying-rewetting: the legacy of 18 years drought. Glob. Change Biol. 25:1005–15
    [Google Scholar]
  26. de Vries FT, Griffiths RI, Bailey M, Craig H, Girlanda M et al. 2018. Soil bacterial networks are less stable under drought than fungal networks. Nat. Commun. 9:3033
    [Google Scholar]
  27. Dickie IA, Bufford JL, Cobb RC, Desprez‐Loustau M, Grelet G et al. 2017. The emerging science of linked plant-fungal invasions. New Phytol 215:1314–32
    [Google Scholar]
  28. Diez JM, James TY, McMunn M, Ibáñez I 2013. Predicting species-specific responses of fungi to climatic variation using historical records. Glob. Change Biol. 19:3145–54
    [Google Scholar]
  29. Emery SM, Bell-Dereske L, Rudgers JA 2015. Fungal symbiosis and precipitation alter traits and dune building by the ecosystem engineer. Ammophila breviligulata. Ecology 96:927–35
    [Google Scholar]
  30. Fitzpatrick CR, Copeland J, Wang PW, Guttman DS, Kotanen PM, Johnson MTJ 2018. Assembly and ecological function of the root microbiome across angiosperm plant species. PNAS 115:E1157–65
    [Google Scholar]
  31. Frank AC, Guzman JPS, Shay JE 2017. Transmission of bacterial endophytes. Microorganisms 5:70
    [Google Scholar]
  32. Frantzeskakis L, Pietro AD, Rep M, Schirawski J, Wu C-H, Panstruga R 2020. Rapid evolution in plant–microbe interactions – a molecular genomics perspective. New Phytol 225:1134–42
    [Google Scholar]
  33. Fry EL, Johnson GN, Hall AL, Pritchard WJ, Bullock JM, Bardgett RD 2018. Drought neutralises plant-soil feedback of two mesic grassland forbs. Oecologia 186:1113–25
    [Google Scholar]
  34. Gehring CA, Sthultz CM, Flores-Renteria L, Whipple AV, Whitham TG 2017. Tree genetics defines fungal partner communities that may confer drought tolerance. PNAS 114:11169–74
    [Google Scholar]
  35. Gherardi LA, Sala OE. 2015. Enhanced precipitation variability decreases grass- and increases shrub-productivity. PNAS 112:12735–40
    [Google Scholar]
  36. Gómez MR, Ashman T. 2019. Floral organs act as environmental filters and interact with pollinators to structure the yellow monkeyflower (Mimulus guttatus) floral microbiome. Mol. Ecol. 28:5155–71
    [Google Scholar]
  37. Griffin-Nolan RJ, Blumenthal DM, Collins SL, Farkas TE, Hoffman AM et al. 2019. Shifts in plant functional composition following long-term drought in grasslands. J. Ecol. 107:2133–48
    [Google Scholar]
  38. Groffman PM, Rustad LE, Templer PH, Campbell JL, Christenson LM et al. 2012. Long-term integrated studies show complex and surprising effects of climate change in the northern hardwood forest. BioScience 62:1056–66
    [Google Scholar]
  39. Guo X, Feng J, Shi Z, Zhou X, Yuan M et al. 2018. Climate warming leads to divergent succession of grassland microbial communities. Nat. Clim. Change 8:813–18
    [Google Scholar]
  40. Hall EK, Bernhardt ES, Bier RL, Bradford MA, Boot CM et al. 2018. Understanding how microbiomes influence the systems they inhabit. Nat. Microbiol. 3:977–82
    [Google Scholar]
  41. Hardoim PR, van Overbeek LS, Berg G, Pirttila AM, Compant S et al. 2015. The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol. Mol. Biol. Rev. 79:293–320
    [Google Scholar]
  42. Harrison JG, Griffin EA. 2020. The diversity and distribution of endophytes across biomes, plant phylogeny and host tissues: How far have we come and where do we go from here. ? Environ. Microbiol. 22:2107–123
    [Google Scholar]
  43. Hawkes CV, Waring BG, Rocca JD, Kivlin SN 2017. Historical climate controls soil respiration responses to current soil moisture. PNAS 114:6322–27
    [Google Scholar]
  44. Hawkins AP, Crawford KM. 2018. Interactions between plants and soil microbes may alter the relative importance of intraspecific and interspecific plant competition in a changing climate. AoB PLANTS 10:ply039
    [Google Scholar]
  45. Hayward J, Horton TR, Nuñez MA 2015a. Ectomycorrhizal fungal communities coinvading with Pinaceae host plants in Argentina: Gringos bajo el bosque. New Phytol 208:497–506
    [Google Scholar]
  46. Hayward J, Horton TR, Pauchard A, Nuñez MA 2015b. A single ectomycorrhizal fungal species can enable a Pinus invasion. Ecology 96:1438–44
    [Google Scholar]
  47. Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J et al. 2010. A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol. Lett. 13:394–407
    [Google Scholar]
  48. Homet P, González M, Matías L, Godoy O, Pérez-Ramos IM et al. 2019. Exploring interactive effects of climate change and exotic pathogens on Quercus suber performance: Damage caused by Phytophthora cinnamomi varies across contrasting scenarios of soil moisture. Agric. For. Meteorol. 276–277:107605
    [Google Scholar]
  49. IPCC. 2013. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change TF Stocker, D Qin, G-K Plattner, M Tignor, SK Allen et al. Cambridge, UK/New York: Cambridge
  50. Johnson NC, Angelard C, Sanders IR, Kiers ET 2013. Predicting community and ecosystem outcomes of mycorrhizal responses to global change. Ecol. Lett. 16:140–53
    [Google Scholar]
  51. Jumpponen A, Herrera J, Porras-Alfaro A, Rudgers JA 2017. Biogeography of root-associated fungal endophytes. Biogeography of Mycorrhizal Symbiosis L Tedersoo 195–222 Cham, Switz.: Springer
    [Google Scholar]
  52. Kaisermann A, de Vries FT, Griffiths RI, Bardgett RD 2017. Legacy effects of drought on plant–soil feedbacks and plant–plant interactions. New Phytol 215:1413–24
    [Google Scholar]
  53. Kariman K, Barker SJ, Tibbett M 2018. Structural plasticity in root-fungal symbioses: Diverse interactions lead to improved plant fitness. PeerJ 6:e6030
    [Google Scholar]
  54. Keane RM, Crawley MJ. 2002. Exotic plant invasions and the enemy release hypothesis. Trends Ecol. Evol. 17:164–70
    [Google Scholar]
  55. Keitt TH, Addis C, Mitchell D, Salas A, Hawkes CV 2016. Climate change, microbes, and soil carbon cycling. Climate Change and Microbial Ecology: Current Research and Future Trends J Marxsen 97–112 Norfolk, UK: Caister Acad.
    [Google Scholar]
  56. Kivlin SN, Emery SM, Rudgers JA 2013. Fungal symbionts alter plant responses to global change. Am. J. Bot. 100:1445–57
    [Google Scholar]
  57. Kivlin SN, Winston GC, Goulden ML, Treseder KK 2014. Environmental filtering affects soil fungal community composition more than dispersal limitation at regional scales. Fungal Ecol 12:14–25
    [Google Scholar]
  58. Körner C, Basler D. 2010. Phenology under global warming. Science 327:1461–62
    [Google Scholar]
  59. Kou L, Li S, Wang H, Fu X, Dai X 2019. Unaltered phenology but increased production of ectomycorrhizal roots of Pinus elliottii under 4 years of nitrogen addition. New Phytol 221:2228–38
    [Google Scholar]
  60. Lau JA, Lennon JT. 2012. Rapid responses of soil microorganisms improve plant fitness in novel environments. PNAS 109:14058–62
    [Google Scholar]
  61. Lau JA, terHorst CP. 2020. Evolutionary responses to global change in species-rich communities. Ann. N.Y. Acad. Sci. In press. https://doi.org/10.1111/nyas.14221
    [Crossref] [Google Scholar]
  62. Marino D, Frendo P, Ladrera R, Zabalza A, Puppo A et al. 2007. Nitrogen fixation control under drought stress. Localized or systemic. ? Plant Physiol 143:1968–74 2007. Plant. Physiol.1233
    [Google Scholar]
  63. Márquez LM, Redman RS, Rodriguez RJ, Roossinck MJ 2007. A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science 315:513–15
    [Google Scholar]
  64. Martiny JBH, Jones SE, Lennon JT, Martiny AC 2015. Microbiomes in light of traits: a phylogenetic perspective. Science 350:aac9323
    [Google Scholar]
  65. Menge DNL, Chisholm RA, Davies SJ, Abu Salim K, Allen D et al. 2019. Patterns of nitrogen-fixing tree abundance in forests across Asia and America. J. Ecol. 107:2598–610
    [Google Scholar]
  66. Merckx V, Bidartondo MI, Hynson NA 2009. Myco-heterotrophy: when fungi host plants. Ann. Bot. 104:1255–61
    [Google Scholar]
  67. Morrissey EM, Mau RL, Hayer M, Liu X-JA, Schwartz E et al. 2019. Evolutionary history constrains microbial traits across environmental variation. Nat. Ecol. Evol. 3:1064–69
    [Google Scholar]
  68. Mougi A, Kondoh M. 2012. Diversity of interaction types and ecological community stability. Science 337:349–51
    [Google Scholar]
  69. Moyano J, Dickie I, Rodriguez-Cabal MA, Núñez MA 2020. Patterns of plant naturalization show that facultative mycorrhizal plants are more likely to succeed outside their native Eurasian ranges. Ecography 43:648–59
    [Google Scholar]
  70. Mueller EA, Wisnoski NI, Peralta AL, Lennon JT 2020. Microbial rescue effects: how microbiomes can save hosts from extinction. Funct. Ecol. In press. https://doi.org/10.1111/1365-2435.13493
    [Crossref] [Google Scholar]
  71. Nguyen NH, Song ZW, 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]
  72. Northfield TD, Ives AR. 2013. Coevolution and the effects of climate change on interacting species. PLOS Biol 11:e1001685
    [Google Scholar]
  73. Núñez MA, Chiuffo MC, Torres A, Paul T, Dimarco RD et al. 2017. Ecology and management of invasive Pinaceae around the world: progress and challenges. Biol. Invasions 19:3099–120
    [Google Scholar]
  74. Núñez MA, Dickie IA. 2014. Invasive belowground mutualists of woody plants. Biol. Invasions 16:645–61
    [Google Scholar]
  75. Olofsson J, Ericson L, Torp M, Stark S, Baxter R 2011. Carbon balance of Arctic tundra under increased snow cover mediated by a plant pathogen. Nat. Clim. Change 1:220–23
    [Google Scholar]
  76. 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. 52:701–16
    [Google Scholar]
  77. Panaccione DG, Beaulieu WT, Cook D 2014. Bioactive alkaloids in vertically transmitted fungal endophytes. Funct. Ecol. 28:299–314
    [Google Scholar]
  78. Parmesan C. 2006. Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Syst. 37:637–69
    [Google Scholar]
  79. Pickles BJ, Twieg BD, O'Neill GA, Mohn WW, Simard SW 2015. Local adaptation in migrated interior Douglas-fir seedlings is mediated by ectomycorrhizas and other soil factors. New Phytol 207:858–71
    [Google Scholar]
  80. Ploughe LW, Jacobs EM, Frank GS, Greenler SM, Smith MD, Dukes JS 2019. Community Response to Extreme Drought (CRED): a framework for drought‐induced shifts in plant–plant interactions. New Phytol 222:52–69
    [Google Scholar]
  81. Porras-Alfaro A, Bayman P. 2011. Hidden fungi, emergent properties: endophytes and microbiomes. Annu. Rev. Phytopathol. 49:291–315
    [Google Scholar]
  82. Pugnaire FI, Morillo JA, Peñuelas J, Reich PB, Bardgett RD et al. 2019. Climate change effects on plant-soil feedbacks and consequences for biodiversity and functioning of terrestrial ecosystems. Sci. Adv. 5:eaaz1834
    [Google Scholar]
  83. Radville L, McCormack ML, Post E, Eissenstat DM 2016. Root phenology in a changing climate. J. Exp. Bot. 67:3617–28
    [Google Scholar]
  84. Rana KL, Kour D, Sheikh I, Dhiman A, Yadav N et al. 2019. Endophytic fungi: biodiversity, ecological significance, and potential industrial applications. Recent Advancement in White Biotechnology Through Fungi, Vol. 1: Diversity and Enzymes Perspectives AN Yadav, S Mishra, S Singh, A Gupta 1–62 Cham, Switz: Springer
    [Google Scholar]
  85. Requena N, Perez-Solis E, Azcon-Aguilar C, Jeffries P, Barea JM 2001. Management of indigenous plant-microbe symbioses aids restoration of desertified ecosystems. Appl. Environ. Microbiol. 67:495–98
    [Google Scholar]
  86. Rillig MC, Ryo M, Lehmann A, Aguilar-Trigueros CA, Buchert S et al. 2019. The role of multiple global change factors in driving soil functions and microbial biodiversity. Science 366:886–90
    [Google Scholar]
  87. Rineau F, Malina R, Beenaerts N, Arnauts N, Bardgett RD et al. 2019. Towards more predictive and interdisciplinary climate change ecosystem experiments. Nat. Clim. Change 9:809–16
    [Google Scholar]
  88. Rodriguez RJ, White JF, Arnold AE, Redman RS 2009. Fungal endophytes: diversity and functional roles. New Phytol 182:314–30
    [Google Scholar]
  89. Rúa MA, Antoninka A, Antunes PM, Chaudhary VB, Gehring C et al. 2016. Home-field advantage? Evidence of local adaptation among plants, soil, and arbuscular mycorrhizal fungi through meta-analysis. BMC Evol. Biol. 16:122
    [Google Scholar]
  90. Rudgers JA, Bell-Dereske L, Crawford KM, Emery SM 2015. Fungal symbiont effects on dune plant diversity depend on precipitation. J. Ecol. 103:219–30
    [Google Scholar]
  91. Rudgers JA, Chung YA, Maurer GE, Litvak ME, Moore DI et al. 2018a. Climate sensitivity functions and net primary production: a framework for incorporating climate mean and variability. Ecology 99:576–82
    [Google Scholar]
  92. Rudgers JA, Dettweiler-Robinson E, Belnap J, Green LE, Sinsabaugh RL et al. 2018b. Are fungal networks key to dryland primary production. ? Am. J. Bot. 105:1783–87
    [Google Scholar]
  93. Sardans J, Grau O, Chen HYH, Janssens IA, Ciais P et al. 2017. Changes in nutrient concentrations of leaves and roots in response to global change factors. Glob. Change Biol. 23:3849–56
    [Google Scholar]
  94. Schnitzer SA, Klironomos JN, HilleRisLambers J, Kinkel LL, Reich PB et al. 2011. Soil microbes drive the classic plant diversity–productivity pattern. Ecology 92:296–303
    [Google Scholar]
  95. Shade A, Jacques M-A, Barret M 2017. Ecological patterns of seed microbiome diversity, transmission, and assembly. Curr. Opin. Microbiol. 37:15–22
    [Google Scholar]
  96. Shemesh H, Boaz BE, Millar CI, Bruns TD 2019. Symbiotic interactions above treeline of long‐lived pines: mycorrhizal advantage of limber pine (Pinus flexilis) over Great Basin bristlecone pine (Pinus longaeva) at the seedling stage. J. Ecol. 108:908–16
    [Google Scholar]
  97. Smith MD, Knapp AK, Collins SL 2009. A framework for assessing ecosystem dynamics in response to chronic resource alterations induced by global change. Ecology 90:3279–89
    [Google Scholar]
  98. Smith SE, Read DJ. 2008. Mycorrhizal Symbiosis New York: Academic, 3rd ed..
  99. Snyder AE, Harmon-Threatt AN. 2019. Reduced water-availability lowers the strength of negative plant-soil feedbacks of two Asclepias species. Oecologia 190:425–32
    [Google Scholar]
  100. Song J, Wan S, Piao S, Knapp AK, Classen AT et al. 2019. A meta-analysis of 1,119 manipulative experiments on terrestrial carbon-cycling responses to global change. Nat. Ecol. Evol. 3:1309–20
    [Google Scholar]
  101. Soudzilovskaia NA, van Bodegom PM, Terrer C, van't Zelfde M, McCallum I et al. 2019. Global mycorrhizal plant distribution linked to terrestrial carbon stocks. Nat. Commun. 10:5077
    [Google Scholar]
  102. Steidinger BS, Bhatnagar JM, Vilgalys R, Taylor JW, Qin C et al. 2020. Ectomycorrhizal fungal diversity predicted to substantially decline due to climate changes in North American Pinaceae forests. J. Biogeogr. 47:772–82
    [Google Scholar]
  103. 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 569:404–8
    [Google Scholar]
  104. Sulman BN, Shevliakova E, Brzostek ER, Kivlin SN, Malyshev S et al. 2019. Diverse mycorrhizal associations enhance terrestrial C storage in a global model. Glob. Biogeochem. Cycles 33:501–23
    [Google Scholar]
  105. Terrer C, Vicca S, Hungate BA, Phillips RP, Prentice IC 2016. Mycorrhizal association as a primary control of the CO2 fertilization effect. Science 353:72–74
    [Google Scholar]
  106. Vacher C, Hampe A, Porté AJ, Sauer U, Compant S, Morris CE 2016. The phyllosphere: microbial jungle at the plant-climate interface. Annu. Rev. Ecol. Evol. Syst. 47:1–24
    [Google Scholar]
  107. van der Heijden MGA, Bardgett RD, van Straalen NM 2008. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol. Lett. 11:296–310
    [Google Scholar]
  108. van Grunsven RHA, van der Putten WH, Bezemer TM, Berendse F, Veenendaal EM 2010. Plant-soil interactions in the expansion and native range of a poleward shifting plant species. Glob. Change Biol. 16:380–85
    [Google Scholar]
  109. Vandegrift R, Blaser W, Campos-Cerda F, Heneghan AF, Carroll GC, Roy BA 2015. Mixed fitness effects of grass endophytes modulate impact of enemy release and rapid evolution in an invasive grass. Biol. Invasions 17:1239–51
    [Google Scholar]
  110. Varoquaux N, Cole B, Gao C, Pierroz G, Baker CR et al. 2019. Transcriptomic analysis of field-droughted sorghum from seedling to maturity reveals biotic and metabolic responses. PNAS 116:27124–32
    [Google Scholar]
  111. Vazquez DP, Gianoli E, Morris WF, Bozinovic F 2017. Ecological and evolutionary impacts of changing climatic variability. Biol. Rev. 92:22–42
    [Google Scholar]
  112. Velasquez AC, Castroverde CDM, He SY 2018. Plant-pathogen warfare under changing climate conditions. Curr. Biol. 28:R619–34
    [Google Scholar]
  113. Wagner MR, Lundberg DS, del Rio TG, Tringe SG, Dangl JL, Mitchell-Olds T 2016. Host genotype and age shape the leaf and root microbiomes of a wild perennial plant. Nat. Commun. 7:12151
    [Google Scholar]
  114. Waring B, Hawkes CV. 2018. Ecological mechanisms underlying soil bacterial responses to rainfall along a steep natural precipitation gradient. FEMS Microbiol. Ecol. 94:fiy001
    [Google Scholar]
  115. Werner GDA, Cornelissen JHC, Cornwell WK, Soudzilovskaia NA, Kattge J et al. 2018. Symbiont switching and alternative resource acquisition strategies drive mutualism breakdown. PNAS 115:5229–34
    [Google Scholar]
  116. 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. 20:1064–73
    [Google Scholar]
  117. Whitney KD, Mudge J, Natvig DO, Sundararajan A, Pockman WT et al. 2019. Experimental drought reduces genetic diversity in the grassland foundation species Bouteloua eriopoda. . Oecologia 189:1107–20
    [Google Scholar]
  118. Wilcox KR, Shi Z, Gherardi LA, Lemoine NP, Koerner SE et al. 2017a. Asymmetric responses of primary productivity to precipitation extremes: a synthesis of grassland precipitation manipulation experiments. Glob. Change Biol. 23:4376–85
    [Google Scholar]
  119. Wilcox KR, Tredennick AT, Koerner SE, Grman E, Hallett LM et al. 2017b. Asynchrony among local communities stabilises ecosystem function of metacommunities. Ecol. Lett. 20:1534–45
    [Google Scholar]
  120. Woodward C, Hansen L, Beckwith F, Redman RS, Rodriguez RJ 2012. Symbiogenics: an epigenetic approach to mitigating impacts of climate change on plants. Hortscience 47:699–703
    [Google Scholar]
  121. Wu Z, Dijkstra P, Koch GW, Penuelas J, Hungate BA 2011. Responses of terrestrial ecosystems to temperature and precipitation change: a meta-analysis of experimental manipulation. Glob. Change Biol. 17:927–42
    [Google Scholar]
  122. Wubs ERJ, van der Putten WH, Bosch M, Bezemer TM 2016. Soil inoculation steers restoration of terrestrial ecosystems. Nat. Plants 2:16107
    [Google Scholar]
  123. 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. 95:409–33
    [Google Scholar]
  124. Zhou Z, Wang C, Luo Y 2018. Response of soil microbial communities to altered precipitation: a global synthesis. Glob. Ecol. Biogeogr. 27:1121–36
    [Google Scholar]
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