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Soil-plant-atmosphere interactions: structure, function, and predictive scaling for climate change mitigation



It is well established that the functioning of terrestrial ecosystems depends on biophysical and biogeochemical feedbacks occurring at the soil-plant-atmosphere (SPA) interface. However, dynamic biophysical and biogeochemical processes that operate at local scales are seldom studied in conjunction with structural ecosystem properties that arise from broad environmental constraints. As a result, the effect of SPA interactions on how ecosystems respond to, and exert influence on, the global environment remains difficult to predict.


We review recent findings that link structural and functional SPA interactions and evaluate their potential for predicting ecosystem responses to chronic environmental pressures. Specifically, we propose a quantitative framework for the integrated analysis of three major plant functional groups (evergreen conifers, broadleaf deciduous, and understory shrubs) and their distinct mycorrhizal symbionts under rising levels of carbon dioxide, changing climate, and disturbance regime. First, we explain how symbiotic and competitive strategies involving plants and soil microorganisms influence scale-free patterns of carbon, nutrient, and water use from individual organisms to landscapes. We then focus on the relationship between those patterns and structural traits such as specific leaf area, leaf area index, and soil physical and chemical properties that constrain root connectivity and canopy gas exchange. Finally, we use those relationships to predict how changes in ecosystem structure may affect processes that are important for climate stability.


On the basis of emerging ecological theory and empirical biophysical and biogeochemical knowledge, we propose ten interpretive hypotheses that serve as a primary set of hierarchical relationships (or scaling rules), by which local SPA interactions can be spatially and temporally aggregated to inform broad climate change mitigation efforts. To this end, we provide a series of numerical formulations that simplify the net outcome of complex SPA interactions as a first step towards anticipating shifts in terrestrial carbon, water, and nutrient cycles.

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Fig. 1
Fig. 2
Fig. 3
Fig. 4







arbuscular mycorrhizae



Ca :

atmospheric CO2

Cbg :

total amount of carbon invested belowground

Ci :

intercellular CO2

Cresp :

heterotrophic respiration

Croot :

carbon allocated to root growth

Ctrans :

carbon transferred from roots to symbionts


solute dispersion coefficient


stable carbon isotope ratio


stable hydrogen isotope ratio 


stable oxygen isotope ratios






gross primary productivity

gs :

stomatal conductance

kw :

relative permeability of the soil

K :

hydraulic conductivity


leaf area intex






soil porosity




parent materials


pedogenic energy


connectivity of root-fungal networks

Rac :

resource acquisition

Rsp :

species-specific level of resource needed to ensure survival


soil saturation


specific leaf area






rate of resource uptake


water-use efficiency


nutrient-use efficiency


water-holding capacity


rate of water loss via ET

ψ :

water potential


return on carbon investment


  1. Almond P, Roering J, Hales TC (2007) Using soil residence time to delineate spatial and temporal patterns of transient landscape response. J Geophys Res 112:F03S17.

  2. Amundson R, Berhe AA, Hopmans JW et al (2015) Soil science. Soil and human security in the 21st century. Science 348:1261071.

  3. Asner GP, Brodrick PG, Anderson CB et al (2016a) Progressive forest canopy water loss during the 2012-2015 California drought. Proc Natl Acad Sci U S A 113:E249–E255.

  4. Asner GP, Knapp DE, Anderson CB et al (2016b) Large-scale climatic and geophysical controls on the leaf economics spectrum. Proc Natl Acad Sci 12:E4043–E4051.

  5. Averill C, Bhatnagar JM, Dietze MC et al (2019) Global imprint of mycorrhizal fungi on whole-plant nutrient economics. Proc Natl Acad Sci U S A.

  6. Baldocchi D (2008) “Breathing” of the terrestrial biosphere: lessons learned from a global network of carbon dioxide flux measurement systems. Aust J Bot 56:1–26

  7. Baldocchi D (2014) Biogeochemistry: managing land and climate. Nat Clim Chang 4:330–331.

  8. Baldocchi D, Peñuelas J (2019) The physics and ecology of mining carbon dioxide from the atmosphere by ecosystems. Glob Chang Biol 25:1191–1197.

  9. Baldocchi D, Chu H, Reichstein M (2018) Inter-annual variability of net and gross ecosystem carbon fluxes: a review. Agric For Meteorol 249:520–533.

  10. Baldocchi D, Dralle D, Jiang C, Ryu Y (2019) How much water is evaporated across California? A multiyear assessment using a biophysical model forced with satellite remote sensing data. Water Resour Res 55:2722–2741.

  11. Bauters M, Verbeeck H, Rütting T et al (2019) Contrasting nitrogen fluxes in African tropical forests of the Congo Basin. Ecol Monogr 89:e01342.

  12. Beer C, Reichstein M, Tomelleri E et al (2010) Terrestrial gross carbon dioxide uptake: global distribution and covariation with climate. Science 329:834–838.

  13. Berhe AA, Barnes RT, Six J, Marín-Spiotta E (2018) Role of soil erosion in biogeochemical cycling of essential elements: carbon, nitrogen, and phosphorus. Annu Rev Earth Planet Sci 46:521–548.

  14. Bingham MA, Simard S (2012) Ectomycorrhizal networks of seudotsuga menziesii var. glauca trees facilitate establishment of conspecific seedlings under drought. Ecosystems 15:188–199

  15. Bomfim B, Silva LCR, Doane TA, Horwath WR (2019) Interactive effects of land-use change and topography on asymbiotic nitrogen fixation in the Brazilian Atlantic Forest. Biogeochemistry 142:137–153.

  16. Bonan G (2015) Surface energy fluxes, third. Cambridge, UK

  17. Bonan GB, Williams M, Fisher RA, Oleson KW (2014) Modeling stomatal conductance in the earth system: linking leaf water-use efficiency and water transport along the soil–plant–atmosphere continuum. Geosci Model Dev 7:2193–2222.

  18. Boyce CK, Lee J-E (2010) An exceptional role for flowering plant physiology in the expansion of tropical rainforests and biodiversity

  19. Brantley SL, Eissenstat DM, Marshall JA et al (2017) Reviews and syntheses: on the roles trees play in building and plumbing the critical zone. Biogeosciences 145194:5115–5142.

  20. Brice M, Cazelles K, Legendre P, Fortin M (2019) Disturbances amplify tree community responses to climate change in the temperate–boreal ecotone. Glob Ecol Biogeogr Geb.12971. doi:

  21. Brown JH, Gillooly JF, Allen AP et al (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789.

  22. Bucher SF, Auerswald K, Tautenhahn S et al (2016) Inter- and intraspecific variation in stomatal pore area index along elevational gradients and its relation to leaf functional traits. Plant Ecol 217:229–240.

  23. Buzzard V, Michaletz ST, Deng Y et al (2019) Continental scale structuring of forest and soil diversity via functional traits. Nat Ecol Evol 3:1298–1308.

  24. Chen D-X, Coughenour MB (2004) Photosynthesis, transpiration, and primary productivity: scaling up from leaves to canopies and regions using process models and remotely sensed data. Global Biogeochem cycles 18:n/a-n/a. doi:

  25. Coenders-Gerrits AMJ, van der Ent RJ, Bogaard TA et al (2014) Uncertainties in transpiration estimates. Nature 506:E1–E2.

  26. Correa-Díaz A, Silva LCR, Horwath WR et al (2019) Linking remote sensing and dendrochronology to quantify climate-induced shifts in high-elevation forests over space and time. J Geophys Res Biogeosci 124:JG004687.

  27. Creed IF, Spargo AT, Jones JA et al (2014) Changing forest water yields in response to climate warming: results from long-term experimental watershed sites across North America. Glob Chang Biol 20:3191–3208.

  28. Crowther TW, Todd-Brown KEO, Rowe CW et al (2016) Quantifying global soil carbon losses in response to warming. Nature 540:104–108.

  29. Davis EL, Gedalof Z (2018) Limited prospects for future alpine treeline advance in the Canadian Rocky Mountains. Glob Chang Biol.

  30. Delgado-Baquerizo M, Oliverio AM, Brewer TE et al (2018) A global atlas of the dominant bacteria found in soil. Science 359:320–325.

  31. Dietrich R, Bell FW, Silva LCR et al (2016) Climatic sensitivity, water-use efficiency, and growth decline in boreal jack pine (Pinus banksiana) forests in northern Ontario. J Geophys Res Biogeosci 121:2761–2774.

  32. Doetterl S, Berhe AA, Arnold C et al (2018) Links among warming, carbon and microbial dynamics mediated by soil mineral weathering. Nat Geosci 11:589–593.

  33. Earles JM, Sperling O, Silva LCR et al (2016) Bark water uptake promotes localized hydraulic recovery in coastal redwood crown. Plant Cell Environ 39:320–328.

  34. Eller CB, Lima AL, Oliveira RS (2013) Foliar uptake of fog water and transport belowground alleviates drought effects in the cloud forest tree species, Drimys brasiliensis (Winteraceae). New Phytol 199:151–162.

  35. Elser JJ, Fagan WF, Kerkhoff AJ et al (2010) Biological stoichiometry of plant production: metabolism, scaling and ecological response to global change. New Phytol 186:593–608.

  36. Enquist BJ (2002) Universal scaling in tree and vascular plant allometry: toward a general quantitative theory linking plant form and function from cells to ecosystems. Tree Physiol 22:1045–1064.

  37. Enquist BJ, Norberg J, Bonser SP et al (2015) Scaling from traits to ecosystems: developing a general trait driver theory via integrating trait-based and metabolic scaling theories. Adv Ecol Res 52:249–318

  38. Enquist BJ, Bentley LP, Shenkin A et al (2017) Assessing trait-based scaling theory in tropical forests spanning a broad temperature gradient. Glob Ecol Biogeogr.

  39. Estes L, Elsen PR, Treuer T et al (2018) The spatial and temporal domains of modern ecology. Nat Ecol Evol 2:819–826.

  40. Evaristo J, Jasechko S, McDonnell JJ (2015) Global separation of plant transpiration from groundwater and streamflow. Nature 525:91–94.

  41. Farnsworth KD, Albantakis L, Caruso T (2017) Unifying concepts of biological function from molecules to ecosystems. Oikos 126:1367–1376.

  42. Farquhar G, Richards R (1984) Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Funct Plant Biol 11:539–552

  43. Fellbaum CR, Mensah JA, Cloos AJ et al (2014) Fungal nutrient allocation in common mycorrhizal networks is regulated by the carbon source strength of individual host plants. New Phytol 203:646–656.

  44. Ferlian O, Biere A, Bonfante P et al (2018) Growing research networks on mycorrhizae for mutual benefits. Trends Plant Sci 23:975–984.

  45. Fine PVA (2015) Ecological and evolutionary drivers of geographic variation in species diversity. Annu Rev Ecol Evol Syst 46:369–392.

  46. Folke C, Carpenter S, Walker B et al (2004) Regime shifts, resilience, and biodiversity in ecosystem management. Annu Rev Ecol Evol Syst 35:557–581.

  47. Franco AC, Rossatto DR, Silva LCR, Ferreira CS (2014) Cerrado vegetation and global change: the role of functional types, resource availability and disturbance in regulating plant community responses to rising CO2 levels and climate warming. Theor Exp Plant Physiol 26:19–38.

  48. Franklin JF, Norman Johnson K (2014) Lessons in policy implementation from experiences with the northwest Forest plan, USA. Biodivers Conserv 23:3607–3613.

  49. Giguère-Croteau C, Boucher É, Bergeron Y et al (2019) North America’s oldest boreal trees are more efficient water users due to increased [CO2], but do not grow faster. Proc Natl Acad Sci 116:2749–2754.

  50. Gilbert L, Johnson D (2017) Plant–plant communication through common Mycorrhizal networks. Adv Bot Res 82:83–97.

  51. Gorzelak MA, Asay AK, Pickles BJ, Simard SW (2015) Inter-plant communication through mycorrhizal networks mediates complex adaptive behaviour in plant communities. AoB Plants 7:2041–2851

  52. Gómez‐Guerrero A, Silva LCR, Barrera‐Reyes M, Kishchuk B (2013) Growth decline and divergent tree ring isotopic composition (δ13C and δ18O) contradict predictions of CO2 stimulation in high altitudinal forests. Global Change Biology 19(6):1748–1758

  53. Griscom BW, Adams J, Ellis PW et al (2017) Natural climate solutions. Proc Natl Acad Sci U S A 114:11645–11650.

  54. Gunderson LH, Holling CS (2002) Panarchy: understanding transformations in human and natural systems. Island Press

  55. Gunderson L, Cosens BA, Chaffin BC et al (2017) Regime shifts and panarchies in regional scale social-ecological water systems. Ecol Soc 22:art31.

  56. Hallema DW, Sun G, Caldwell PV et al (2018) Burned forests impact water supplies. Nat Commun 9:1307.

  57. Harrison S, Damschen E, Fernandez-Going B et al (2015) Plant communities on infertile soils are less sensitive to climate change. Ann Bot 116:1017–1022.

  58. Harrison SP, Bartlein PJ, Prentice IC (2016) What have we learnt from palaeoclimate simulations? J Quat Sci 31:363–385.

  59. Hastings A, Abbott KC, Cuddington K et al (2018) Transient phenomena in ecology. Science 361:eaat6412.

  60. Hayes JL, Riebe CS, Holbrook WS et al (2019) Porosity production in weathered rock: where volumetric strain dominates over chemical mass loss. Sci Adv 5:eaao0834.

  61. Hazard C, Johnson D (2018) Does genotypic and species diversity of mycorrhizal plants and fungi affect ecosystem function? New Phytol.

  62. Heaton LLM, López E, Maini PK et al (2010) Growth-induced mass flows in fungal networks. Proc R Soc Lond B Biol Sci 277:3265–3274

  63. Heaton LLM, López E, Maini PK et al (2012) Advection, diffusion, and delivery over a network. Phys Rev E Stat Nonlinear Soft Matter Phys 86:021905.

  64. Higgins SI (2017) Ecosystem assembly: a Mission for terrestrial earth system science. Ecosystems 20:69–77.

  65. Hinsinger P, Marschner P (2006) Rhizosphere—perspectives and challenges—a tribute to Lorenz Hiltner 12–17 September 2004—Munich, Germany. Plant Soil 283:vii–viii. doi:

  66. Hoffmann WA, Geiger EL, Gotsch SG et al (2012) Ecological thresholds at the savanna-forest boundary: how plant traits, resources and fire govern the distribution of tropical biomes. Ecol Lett 15:759–768.

  67. Jasechko S, Sharp ZD, Gibson JJ et al (2013) Terrestrial water fluxes dominated by transpiration. Nature 496:347–350.

  68. Jerszurki D, Couvreur V, Maxwell T et al (2017) Impact of root growth and hydraulic conductance on canopy carbon-water relations of young walnut trees (Juglans regia L.) under drought. Sci Hortic (Amsterdam) 226:342–352.

  69. Johnstone JA, Dawson TE (2010) Climatic context and ecological implications of summer fog decline in the coast redwood region. Proc Natl Acad Sci U S A 107:4533–4538.

  70. Johnstone JA, Roden JS, Dawson TE (2013) Oxygen and carbon stable isotopes in coast redwood tree rings respond to spring and summer climate signals. J Geophys Res Biogeosci 118:1438–1450.

  71. Joosten H (2015) Current soil carbon loss and land degradation globally: where are the hotspots and why there? Soil Carbon Sci Manag Policy Mult Benefits 71:224–234

  72. Kapoor V, Gelhar LW, Miralles-Wilhelm F (1997) Bimolecular second-order reactions in spatially varying flows: segregation induced scale-dependent transformation rates. Water Resour Res 33:527–536.

  73. Kempes CP, Koehl MAR, West GB (2019) The scales that limit: the physical boundaries of evolution. Front Ecol Evol.

  74. Kiers ET, Duhamel M, Beesetty Y, et al (2011) Reciprocal rewards stabilize cooperation in the Mycorrhizal Symbiosis. Science (80- ) 333:880–882

  75. Körner C (2012) Alpine Treelines. Springer, Basel

  76. Kröber W, Plath I, Heklau H, Bruelheide H (2015) Relating stomatal conductance to leaf functional traits. J Vis Exp.

  77. Ladd B, Peri PL, Pepper DA et al (2014) Carbon isotopic signatures of soil organic matter correlate with leaf area index across woody biomes. J Ecol 102:1606–1611.

  78. Lago ME, Miralles-Wilhelm F, Mahmoudi M, Engel V (2010) Numerical modeling of the effects of water flow, sediment transport and vegetation growth on the spatiotemporal patterning of the ridge and slough landscape of the Everglades wetland. Adv Water Resour 33:1268–1278.

  79. Lambers H, Bultynck L, Zhu Y-G (2007) Marschner reviews: a new initiative in delivering cutting-edge science in soil–plant interactions. Plant Soil 300:1–7.

  80. Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103.

  81. Lambers H, Martinoia E, Renton M (2015) Plant adaptations to severely phosphorus-impoverished soils. Curr Opin Plant Biol 25:23–31.

  82. Lambers H, Albornoz F, Kotula L et al (2018) How belowground interactions contribute to the coexistence of mycorrhizal and non-mycorrhizal species in severely phosphorus-impoverished hyperdiverse ecosystems. Plant Soil 424:11–33.

  83. Le Quéré C, Andrew RM, Friedlingstein P et al (2018) Global carbon budget 2018. Earth Syst Sci Data 10:2141–2194.

  84. Levin S (1992) The problem of pattern and scale in ecology. Ecology 73:1943–1967

  85. Liles GC, Maxwell TM, Silva LCR et al (2019) Two decades of experimental manipulation reveal potential for enhanced biomass accumulation and water use efficiency in ponderosa pine plantations across climate gradients. J Geophys Res Biogeosci 124:2321–2334.

  86. Lindeburg KS, Almond P, Roering JJ, Chadwick OA (2013) Pathways of soil genesis in the coast range of Oregon, USA. Plant Soil 367:57–75.

  87. Louca S, Polz MF, Mazel F et al (2018) Function and functional redundancy in microbial systems. Nat Ecol Evol 2:936–943.

  88. Lützow MV, Kögel-Knabner I, Ekschmitt K et al (2006) Stabilization of organic matter in temperate soils : mechanisms and their relevance under different soil conditions - a review. Eur J Soil Sci 57:426–445

  89. Mankin JS, Smerdon JE, Cook BI, et al (2017) The curious case of projected 21st-century drying but greening in the American West. J Clim JCLI-D-17-0213.1. doi:

  90. Marshall JD, Brooks JR, Lajtha K (2007) Sources of variation in stable isotopes of plants. In: Lajtha K, Michener R (eds) Stable isotopes in ecology and environmental science

  91. Maxwell TM, Silva LCR, Horwath WR (2014) Using multielement isotopic analysis to decipher drought impacts and adaptive management in ancient agricultural systems: fig. 1. Proc Natl Acad Sci 111:E4807–E4808.

  92. Maxwell TM, Silva LCR, Horwath WR (2018a) Integrating effects of species composition and soil properties to predict shifts in montane forest carbon–water relations. Proc Natl Acad Sci 115:201718864.

  93. Maxwell TM, Silva LCR, Horwath WR (2018b) Predictable oxygen isotope exchange between plant lipids and environmental water: implications for ecosystem water balance reconstruction. J Geophys Res Biogeosci 123:2941–2954.

  94. Medlyn BE, Zaehle S, De Kauwe MG, et al (2015) Using ecosystem experiments to improve vegetation models. 5:528–534. doi:

  95. Medlyn BE, De Kauwe MG, Lin Y-S et al (2017) How do leaf and ecosystem measures of water-use efficiency compare? New Phytol 216:758–770.

  96. Messier J, Violle C, Enquist BJ et al (2018) Similarities and differences in intrapopulation trait correlations of co-occurring tree species: consistent water-use relationships amid widely different correlation patterns. Am J Bot 105:1477–1490.

  97. Michaletz ST, Kerkhoff AJ, Enquist BJ (2018) Drivers of terrestrial plant production across broad geographical gradients. Glob Ecol Biogeogr 27:166–174.

  98. Mikutta R, Kleber M, Torn MS, Jahn R (2006) Stabilization of soil organic matter: association with minerals or chemical recalcitrance? Biogeochemistry 77:25–56.

  99. Miralles-Wilhelm F (2016) Development and application of integrative modeling tools in support of food-energy-water nexus planning—a research agenda. J Environ Stud Sci 6:3–10.

  100. Morford SL, Houlton BZ, Dahlgren RA (2016) Geochemical and tectonic uplift controls on rock nitrogen inputs across terrestrial ecosystems. Glob Biogeochem Cycles 30:333–349.

  101. Myers SS, Zanobetti A, Kloog I et al (2014) Increasing CO2 threatens human nutrition. Nature 510:139–142.

  102. Nolan C, Overpeck JT, Allen JRM et al (2018) Past and future global transformation of terrestrial ecosystems under climate change. Science 361:920–923.

  103. Novák V (2012) Movement of water in soil during evaporation. In: Evapotranspiration in the Soil-Plant-Atmosphere System. Springer, pp 59–83

  104. O’Geen AT, Safeeq M, Wagenbrenner J et al (2018) Southern sierra critical zone observatory and kings river experimental watersheds: a synthesis of measurements, new insights, and future directions. Vadose Zo J.

  105. Ogle K, Barber JJ, Barron-Gafford GA et al (2015) Quantifying ecological memory in plant and ecosystem processes. Ecol Lett 18:221–235.

  106. Oliveira RS, Dawson TE, Burgess SSO (2005) Evidence for direct water absorption by the shoot of the desiccation-tolerant plant Vellozia flavicans in the savannas of Central Brazil. J Trop Ecol 21:585–588.

  107. Or D, Wraith JM (2002) Soil water content and water potential relationships. In: Handbook of soil sciences: properties and processes. CRC Press, New York, pp 49–84

  108. Paiva AO, Silva LCR, Haridasan M (2016) Productivity-efficiency tradeoffs in tropical gallery forest-savanna transitions: linking plant and soil processes through litter input and composition. Plant Ecol 216:775–787.

  109. Pangala SR, Enrich-Prast A, Basso LS et al (2017) Large emissions from floodplain trees close the Amazon methane budget. Nature 14:230–234.

  110. Perry TD, Jones JA (2017) Summer streamflow deficits from regenerating Douglas-fir forest in the Pacific northwest, USA. Ecohydrology 10:e1790.

  111. Philip JR (1966) Plant water relations: some physical aspects. Annu Rev Plant Physiol 17:245–268.

  112. Pietsch KA, Ogle K, Cornelissen JHC et al (2014) Global relationship of wood and leaf litter decomposability: the role of functional traits within and across plant organs. Glob Ecol Biogeogr 23:1046–1057.

  113. Powell JR, Riley RC, Cornwell W (2017) Relationships between mycorrhizal type and leaf flammability in the Australian flora. Pedobiologia (Jena) 65:43–49.

  114. Qiao Y, Miao S, Silva LCR, Horwath WR (2014) Understory species regulate litter decomposition and accumulation of C and N in forest soils: a long-term dual-isotope experiment. For Ecol Manag 329:318–327.

  115. Rasmussen C, Tabor NJ (2007) Applying a quantitative Pedogenic energy model across a range of environmental gradients. Soil Sci Soc Am J 71:1719.

  116. Raven JA, Lambers H, Smith SE, Westoby M (2018) Costs of acquiring phosphorus by vascular land plants: patterns and implications for plant coexistence. New Phytol 217:1420–1427.

  117. Reich PB, Hobbie SE, Lee TD (2014) Plant growth enhancement by elevated CO2 eliminated by joint water and nitrogen limitation. Nat Geosci 7:920–924.

  118. Roering JJ, Perron JT, Kirchner JW (2007) Functional relationships between denudation and hillslope form and relief. Earth Planet Sci Lett 264:245–258.

  119. Rossatto DR, Silva LCR, Villalobos-Vega R et al (2012) Depth of water uptake in woody plants relates to groundwater level and vegetation structure along a topographic gradient in a neotropical savanna. Environ Exp Bot 77:259–266.

  120. Sachse D, Billault I, Bowen GJ et al (2012) Molecular Paleohydrology: interpreting the hydrogen-isotopic composition of lipid biomarkers from photosynthesizing organisms. Annu Rev Earth Planet Sci 40:221–249.

  121. Saha AK, Setegn SG (2015) Ecohydrology: understanding and maintaining ecosystem services for IWRM. In: Sustainability of integrated water resources management. Springer International Publishing, Cham, pp 121–145

  122. Saha AK, da Silveira O’Reilly Sternberg L, Ross MS, Miralles-Wilhelm F (2010) Water source utilization and foliar nutrient status differs between upland and flooded plant communities in wetland tree islands. Wetl Ecol Manag 18:343–355.

  123. Salzer MW, Hughes MK, Bunn AG, Kipfmueller KF (2009) Recent unprecedented tree-ring growth in bristlecone pine at the highest elevations and possible causes. Proc Natl Acad Sci U S A 106:20348–20353

  124. Schlesinger WH, Amundson R (2018) Managing for soil carbon sequestration: Let’s get realistic. Glob Chang Biol GCB.14478. doi:

  125. Schlesinger WH, Jasechko S (2014) Transpiration in the global water cycle. Agric For Meteorol 189–190:115–117.

  126. Schmidt M, Torn MS, Abiven S et al (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56.

  127. Seitz S, Goebes P, Puerta VL et al (2019) Conservation tillage and organic farming reduce soil erosion. Agron Sustain Dev 39:4.

  128. Shi C, Silva LCR, Zhang H et al (2015) Climate warming alters nitrogen dynamics and total non-structural carbohydrate accumulations of perennial herbs of distinctive functional groups during the plant senescence in autumn in an alpine meadow of the Tibetan plateau, China. Agric For Meteorol 200:21–29.

  129. Silva LCR, Anand M (2013) Historical links and new frontiers in the study of forest-atmosphere interactions. Community Ecol 14:208–218.

  130. Silva LCR, Lambers H (2018) Soil-plant-atmosphere interactions: ecological and biogeographical considerations for climate-change research. In: Horwath W, Kuzyakov Y (eds) Climate change impacts on soil processes and ecosystem properties. Elsevier Academic Press, p 625

  131. Silva LCR, Corrêa R, Doane TA et al (2013a) Unprecedented carbon accumulation in mined soils: the synergistic effect of resource input and plant species invasion. Ecol Appl 23:1345–1356.

  132. Silva LCR, Hoffmann WA, Rossatto DR et al (2013b) Can savannas become forests? A coupled analysis of nutrient stocks and fire thresholds in Central Brazil. Plant Soil 373:829–842.

  133. Silva LCR, Salamanca-Jimenez A, Doane TA, Horwath WR (2015a) Carbon dioxide level and form of soil nitrogen regulate assimilation of atmospheric ammonia in young trees. Sci Rep 5:13141.

  134. Silva LCR, Doane TA, Corrêa RS et al (2015b) Iron-mediated stabilization of soil carbon amplifies the benefits of ecological restoration in degraded lands. Ecol Appl 25:1226–1234.

  135. Silva LCR, Pedroso G, Doane TA et al (2015c) Beyond the cellulose: oxygen isotope composition of plant lipids as a proxy for terrestrial water balance. Geochemical Perspect Lett 1:33–42

  136. Silva LCR, Sun G, Zhu-Barker X et al (2016) Tree growth acceleration and expansion of alpine forests: the synergistic effect of atmospheric and edaphic change. Sci Adv 2:e1501302

  137. Simard SW (2009) The foundational role of mycorrhizal networks in self-organization of interior Douglas-fir forests. For Ecol Manag 258:S95–S107.

  138. Simard SW, Beiler KJ, Bingham MA et al (2012) Mycorrhizal networks: mechanisms, ecology and modelling. Fungal Biol Rev 26:39–60.

  139. Simard S, Asay A, Beiler K, et al (2015) Mycorrhizal networks: mechanisms, ecology and modelling. In: Mycorrhizal Networks. pp 133–176

  140. Song YY, Simard SW, Carroll A et al (2015) Defoliation of interior Douglas-fir elicits carbon transfer and stress signalling to ponderosa pine neighbors through ectomycorrhizal networks. Sci Rep 5:8495.

  141. Sperling O, Silva LCR, Tixier A et al (2017) Temperature gradients assist carbohydrate allocation within trees. Sci Rep 7:3265.

  142. Sprintsin M, Chen JM, Desai A, Gough CM (2012) Evaluation of leaf-to-canopy upscaling methodologies against carbon flux data in North America. J Geophys Res Biogeosci.

  143. Stevens JT, Safford HD, Harrison S, Latimer AM (2015) Forest disturbance accelerates thermophilization of understory plant communities. J Ecol 103:1253–1263.

  144. Taylor LL, Banwart SA, Valdes PJ et al (2012) Evaluating the effects of terrestrial ecosystems, climate and carbon dioxide on weathering over geological time: a global-scale process-based approach. Philos Trans R Soc Lond Ser B Biol Sci 367:565–582.

  145. Taylor TC, McMahon SM, Smith MN et al (2018) Isoprene emission structures tropical tree biogeography and community assembly responses to climate. New Phytol 220:435–446.

  146. Terrer C, Vicca S, Hungate BA et al (2016) Mycorrhizal association as a primary control of the CO2 fertilization effect. Science 353:72–74.

  147. Terrer C, Vicca S, Stocker BD et al (2018) Ecosystem responses to elevated CO2 governed by plant-soil interactions and the cost of nitrogen acquisition. New Phytol 217:507–522.

  148. Terrer C, Jackson RB, Prentice IC et al (2019) Nitrogen and phosphorus constrain the CO2 fertilization of global plant biomass. Nat Clim Chang:1–6.

  149. Teste FP, Simard SW, Durall DM et al (2010) Net carbon transfer between Pseudotsuga menziesii var. glauca seedlings in the field is influenced by soil disturbance. J Ecol 98:429–439.

  150. Tharammal T, Bala G, Narayanappa D, Nemani R (2019) A review of the major drivers of the terrestrial carbon uptake: model-based assessments, consensus, and uncertainties. Environ Res Lett.

  151. Tian F, Wigneron J-P, Ciais P et al (2018) Coupling of ecosystem-scale plant water storage and leaf phenology observed by satellite. Nat Ecol Evol.

  152. Tuthorn M, Zech M, Ruppenthal M et al (2014) Oxygen isotope ratios (18O/16O) of hemicellulose-derived sugar biomarkers in plants, soils and sediments as paleoclimate proxy II: insight from a climate transect study. Geochim Cosmochim Acta 126:624–634.

  153. Valentini R, Gamon JA, Field CB (1995) Ecosystem gas exchange in a California grassland: seasonal patterns and implications for scaling. Ecology 76:1940–1952.

  154. van der Heijden MGA, Martin FM, Selosse M-A, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423.

  155. Verhoeven E, Barthel M, Yu L et al (2019) Early season N2O emissions under variable water management in rice systems: source-partitioning emissions using isotope ratios along a depth profile. Biogeosciences 16:383–408.

  156. Vitousek PM, Chadwick OA (2013) Pedogenic thresholds and soil process domains in basalt-derived soils. Ecosystems 16:1379–1395.

  157. Ward BM, Wong CI, Novello VF et al (2019) Reconstruction of Holocene coupling between the South America monsoon system and local moisture variability from speleothem δ18O and 87Sr/86Sr records. Quat Sci Rev 210:51–63.

  158. Weil RR, Brady NC (2016) The nature and properties of soils. Soil Sci Soc Am J 80:1428.

  159. Weremijewicz J, da Sternberg LSLO, Janos DP (2016) Common mycorrhizal networks amplify competition by preferential mineral nutrient allocation to large host plants. New Phytol 212:461–471.

  160. West GB (2017) Scale : the universal laws of growth, innovation, sustainability, and the pace of life in organisms, cities, economies, and companies. New York, NY

  161. Winsome T, Silva LCR, Scow KM et al (2017) Plant-microbe interactions regulate carbon and nitrogen accumulation in forest soils. For Ecol Manag 384:415–423.

  162. Wortham BE, Wong CI, Silva LCR et al (2017) Assessing response of local moisture conditions in Central Brazil to variability in regional monsoon intensity using speleothem 87 Sr/ 86 Sr values. Earth Planet Sci Lett 463:310–322.

  163. Wright IJ, Reich PB, Westoby M et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827

  164. Zech M, Glaser B (2009) Compound-specific d18O analyses of neutral sugars in soils using gas chromatography–pyrolysis–isotope ratio mass spectrometry: problems, possible solutions and a first application. Rapid Commun Mass Spectrom 23:3522–3532

  165. Zech M, Werner RA, Juchelka D et al (2012) Absence of oxygen isotope fractionation/exchange of (hemi-) cellulose derived sugars during litter decomposition. Org Geochem 42:1470–1475

  166. Zech M, Mayr C, Tuthorn M et al (2014) Oxygen isotope ratios (18O/16O) of hemicellulose-derived sugar biomarkers in plants, soils and sediments as paleoclimate proxy I: insight from a climate chamber experiment. Geochim Cosmochim Acta 126:614–623.

  167. Zemunik G, Turner BL, Lambers H, Laliberté E (2015) Diversity of plant nutrient-acquisition strategies increases during long-term ecosystem development. Nat Plants 1:15050.

  168. Zemunik G, Turner BL, Lambers H, Laliberté E (2016) Increasing plant species diversity and extreme species turnover accompany declining soil fertility along a long-term chronosequence in a biodiversity hotspot. J Ecol 104:792–805.

  169. Zhai L, Jiang J, DeAngelis D, da Silveira Lobo Sternberg L (2016) Prediction of plant vulnerability to salinity increase in a coastal ecosystem by stable isotope composition (δ18O) of plant stem water: a model study. Ecosystems 19:32–49.

  170. Zhang K, Kimball JS, Nemani RR et al (2015) Vegetation greening and climate change promote multidecadal rises of global land evapotranspiration. Sci Rep 5:15956.

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Some of the data and ideas used in this synthesis were developed based on funding by the National Science Foundation Plant Biotic Interactions 1758947, Convergence Accelerator Pilot 1939511, and Atmospheric and Geospace Sciences 1602958 programs. We are thankful for comments provided by two anonymous reviewers and members of the Soil-Plant-Atmosphere Research Laboratory and Institute of Ecology & Evolution at the University of Oregon, which helped improve this review.

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Correspondence to Lucas C. R. Silva.

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Silva, L.C.R., Lambers, H. Soil-plant-atmosphere interactions: structure, function, and predictive scaling for climate change mitigation. Plant Soil (2020).

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  • Carbon-water relations
  • Emerging properties
  • Numerical modeling
  • Soil-plant-microbe feedbacks
  • Resource limitation
  • Symbiosis
  • Spatiotemporal scaling