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Interactive effects of elevated carbon dioxide and environmental stresses on root mass fraction in plants: a meta-analytical synthesis using pairwise techniques

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Abstract

Rising atmospheric CO2 greatly enhances plant production, but its effect on biomass allocation, particularly in the presence of environmental stresses, is not well understood. Here, we used meta-analysis combined with pairwise techniques to examine root mass fraction (RMF; i.e., the fraction of root to total biomass) as affected by elevated CO2 and environmental stresses. Our results showed that lower soil fertility increased RMF and the magnitude was similar for ambient and elevated CO2-grown plants. Lower soil water also increased RMF, but to a greater extent at elevated than at ambient CO2. While CO2 enrichment had little effect on the magnitude of O3-caused reduction in RMF in herbaceous species, it alleviated the adverse effect of higher O3 on root production in woody species. These results demonstrate that CO2 has less pronounced effects on RMF than other environmental factors. Under abiotic stresses, e.g., drought and higher O3, elevated CO2-grown plants will likely increase biomass allocation below-ground. Because of the non-uniform changes in drought and O3 projected for different parts of the world, we conclude that elevated CO2 will have regional, but not global, effects on biomass allocation under various global change scenarios.

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References

  • Aerts R (1997) Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship. Oikos 79:439–449

    Article  Google Scholar 

  • Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 165:351–372

    Article  PubMed  Google Scholar 

  • Ainsworth EA, Rosenberg MS, Wang XZ (2007) Meta-analysis: the past, present and future. New Phytol 176:742–745

    Article  PubMed  Google Scholar 

  • Andersen CP (2003) Source-sink balance and carbon allocation below ground in plants exposed to ozone. New Phytol 157:213–228

    Article  CAS  Google Scholar 

  • BassiriRad H, Gutschick VP, Lussenhop J (2001) Root system adjustments: regulation of plant nutrient uptake and growth responses to elevated CO2. Oecologia 126:305–320

    Article  Google Scholar 

  • Bazzaz FA (1990) The response of natural ecosystems to the rising global CO2 levels. Annu Rev Ecol Syst 21:167–196

    Article  Google Scholar 

  • Benfey PN (1999) Is the shoot a root with a view? Curr Opin Plant Biol 2:39–43

    Article  CAS  PubMed  Google Scholar 

  • Bernacchi CJ, Coleman JS, Bazzaz FA, McConnaughay KDM (2000) Biomass allocation in old-field annual species grown in elevated CO2 environments: no evidence for optimal partitioning. Global Change Biol 6:855–863

    Article  Google Scholar 

  • Billings WD, Peterson KM, Luken JO, Mortenson DA (1984) Interaction of increasing atmospheric carbon dioxide and soil nitrogen on the carbon balance of tundra microcosms. Oecologia 65:26–29

    Article  Google Scholar 

  • Brouwer R (1962) Distribution of dry matter in the plant. Neth J Agric Sci 10:361–376

    Google Scholar 

  • Brouwer R (1983) Functional equilibrium: sense or nonsense? Neth J Agric Sci 31:335–348

    Google Scholar 

  • Cairns MA, Brown S, Helmer EH, Baumgardner GA (1997) Root biomass allocation in the world’s upland forests. Oecologia 111:1–11

    Article  Google Scholar 

  • Crist JW, Stout GJ (1929) Relation between top and root size in herbaceous plants. Plant Physiol 4:63–85

    Article  CAS  PubMed  Google Scholar 

  • Cure JD (1986) Crop responses to carbon dioxide doubling: a literature survey. Agric For Meteorol 38:127–145

    Article  Google Scholar 

  • Curtis PS, Wang XZ (1998) A meta-analysis of elevated CO2 effects on woody plant growth, form, and physiology. Oecologia 113:299–313

    Article  Google Scholar 

  • de Graaff MA, Van Groenigen KJ, Six J, Hungate B, Van Kessel C (2006) Interactions between plant growth and soil nutrient cycling under elevated CO2: a meta-analysis. Glob Change Biol 12:2077–2091

    Article  Google Scholar 

  • DeLucia EH et al (1999) Net primary production of a forest ecosystem with experimental CO2 enrichment. Science 284:1177–1179

    Article  CAS  PubMed  Google Scholar 

  • Drake BG, Gonzalez-Meler MA, Long SP (1997) More efficient plants: a consequence of rising atmospheric CO2? Annu Rev Plant Phys Plant Mol Biol 48:609–639

    Article  CAS  Google Scholar 

  • Eamus D, Jarvis PG (1989) The direct effects of increase in the global atmospheric CO2 concentration on natural and commercial temperate trees and forests. In: Begon M, Fitter AH, Ford ED, Macfadyen A (eds) Adv Ecol Res, vol 19. Academic Press, New York, pp 1–55

    Chapter  Google Scholar 

  • Ericsson T (1995) Growth and shoot:root ratio of seedlings in relation to nutrient availability. Plant Soil 168–169:205–214

    Article  Google Scholar 

  • Farrar JF (1992) The whole plant:carbon partitioning during development. In: Pollock CJ, Farrar JF, Gordon AJ (eds) Carbon partitioning within and between organisms. BIOS, Oxford, pp 163–179

    Google Scholar 

  • Farrar JF, Gunn S (1998) Allocation: allometry, acclimation—and alchemy? In: Lambers H, Poorter H, Van Vuren MMI (eds) Inherent variation in plant growth. Backhuys, Leiden, pp 183–198

    Google Scholar 

  • Gartner TB, Cardon ZG (2004) Decomposition dynamics in mixed-species leaf litter. Oikos 104:230–246

    Article  Google Scholar 

  • Giardina CP, Binkley D, Ryan MG, Fownes JH, Senock RS (2004) Belowground carbon cycling in a humid tropical forest decreases with fertilization. Oecologia 139:545–550

    Article  PubMed  Google Scholar 

  • Giardina CP et al (2005) The response of belowground carbon allocation in forests to global change. In: Binkley D, Menyailo O et al (eds) Tree species effects on soils: implications for global change. Springer, The Netherlands, pp 119–154

    Chapter  Google Scholar 

  • Gifford RM, Evans LT (1981) Photosynthesis, carbon partitioning, and yield. Annu Rev Plant Phys 32:485–509

    Article  CAS  Google Scholar 

  • Grantz DA, Gunn S, Vu H-B (2006) O3 impacts on plant development: a meta-analysis of root/shoot allocation and growth. Plant Cell Environ 29:1193–1209

    Article  CAS  PubMed  Google Scholar 

  • Gurevitch J, Curtis PS, Jones MH (2001) Meta-analysis in ecology. Adv Ecol Res 32:199–247

    Article  CAS  Google Scholar 

  • Gutschick VP (2007) Plant acclimation to elevated CO2: from simple regularities to biogeographic chaos. Ecol Modell 200:433–451

    Article  Google Scholar 

  • Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156

    Article  Google Scholar 

  • Hoosbeek MR, Vos JM, Meinders MBJ, Velthorst EJ, Scarascia-Mugnozza GE (2007) Free atmospheric CO2 enrichment (FACE) increased respiration and humification in the mineral soil of a popular plantation. Geoderma 138:204–212

    Article  CAS  Google Scholar 

  • Huang JG, Bergeron Y, Denneler B, Berninger F, Tardif J (2007) Response of forest trees to increased atmospheric CO2. Crit Rev Plant Sci 26:265–283

    Article  CAS  Google Scholar 

  • Hunt R, Lloyd PS (1987) Growth and partitioning. New Phytol 106(Suppl):235–249

    Google Scholar 

  • Hunt R, Nicholls AO (1986) Stress and the coarse control of growth and root–shoot partitioning in herbaceous plants. Oikos 47:149–158

    Article  Google Scholar 

  • Hunt R, Nicholls AO, Fathy SA (1987) Growth and root–shoot partitioning in eighteen British grasses. Oikos 50:53–59

    Article  Google Scholar 

  • Hyvonen R et al (2007) The likely impact of elevated [CO2], nitrogen deposition, increased temperature and management on carbon sequestration in temperature and boreal forest ecosystems: a literature review. New Phytol 173:463–480

    Article  PubMed  Google Scholar 

  • IPCC (2007) Intergovernmental Panel on Climate Change. Synthesis report: summary for policy makers. In: Climate change 2007. Geneva

  • Jasienski M, Bazzaz FA (1999) The fallacy of ratios and the testability of models in biology. Oikos 84:321–326

    Article  Google Scholar 

  • Keeling CD, Whorf TP, Wahlen M, Van Der Plicht J (1995) Interannual extremes in the rate of rise of atmospheric carbon dioxide since 1980. Nature 375:666–670

    Article  CAS  Google Scholar 

  • Kimball BA et al (1995) Productivity and water use of wheat under free-air CO2 enrichment. Global Change Biol 1:429–442

    Article  Google Scholar 

  • Körner C (1994) Biomass fraction in plants: a reconsideration of the definition based on plant functions. In: Roy J, Garnier E (eds) A whole plant perspective on carbon–nitrogen interactions. Academic Publishing, The Hague, pp 173–185

    Google Scholar 

  • Körner C (2000) Biosphere responses to CO2 enrichment. Ecol Appl 10:1590–1619

    Google Scholar 

  • Körner C (2006) Plant CO2 responses: an issue of definition, time and resource supply. New Phytol 172:393–411

    Article  PubMed  Google Scholar 

  • Litton CM, Raich JW, Ryan MG (2007) Carbon allocation in forest ecosystems. Global Change Biol 13:2089–2109

    Article  Google Scholar 

  • Loehle C (1995) Anomalous responses of plants to CO2 enrichment. Oikos 73:181–187

    Article  Google Scholar 

  • Luo Y, Field CB, Mooney HA (1994) Predicting response of photosynthesis and root fraction to elevated [CO2]a: interactions among carbon, nitrogen, and growth. Plant Cell Environ 17:1195–1204

    Article  Google Scholar 

  • Luo Y et al (2004) Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54:731–739

    Article  Google Scholar 

  • Luo Y, Hui D, Zhang DQ (2006) Elevated CO2 stimulates net accumulations of carbon and nitrogen in land ecosystems: a meta-analysis. Ecology 87:53–63

    Article  PubMed  Google Scholar 

  • Maestre FT, Reynolds JF (2006) Spatial heterogeneity in soil nutrient supply modulates nutrient and biomass responses to multiple global change drivers in model grassland communities. Global Change Biol 12:2431–2441

    Article  Google Scholar 

  • McGuire AD, Melillo JM, Joyce LA (1995) The role of nitrogen in the response of forest net primary production to elevated atmospheric carbon dioxide. Annu Rev Ecol Syst 26:473–503

    Article  Google Scholar 

  • Melillo JM, Mcguire AD, Kicklighter DW, Moore B III, Vorosmarty CJ, Schloss AL (1993) Global climate change and terrestrial net primary production. Nature 363:234–240

    Article  CAS  Google Scholar 

  • Meyer WB, Turner BLI (1992) Human population growth and global land-use/cover change. Annu Rev Ecol Syst 23:39–61

    Article  Google Scholar 

  • Mokany K, Raison JR, Prokushkin AS (2006) Critical analysis of root: shoot ratios in terrestrial biomes. Global Change Biol 12:84–96

    Article  Google Scholar 

  • Morgan PB, Ainsworth EA, Long SP (2003) How does elevated ozone impact soybean? A meta-analysis of photosynthesis, growth and yield. Plant Cell Environ 26:1317–1328

    Article  CAS  Google Scholar 

  • Morgan JA et al (2004) Water relations in grassland and desert ecosystems exposed to elevated atmospheric CO2. Oecologia 140:11–25

    Article  CAS  PubMed  Google Scholar 

  • Norby RJ (1994) Issues and perspectives for investigation root responses to elevated atmospheric carbon dioxide. Plant Soil 165:9–20

    Article  CAS  Google Scholar 

  • Norby RJ, Wullschleger SD, Gunderson CA, Johnson DW, Ceulemans R (1999) Tree responses to rising CO2 in field experiment: implications for the future forest. Plant Cell Environ 22:683–714

    Article  CAS  Google Scholar 

  • Norby RJ et al (2005) Forest response to elevated CO2 is conserved across a broad range of productivity. Proc Natl Acad Sci USA 102:18052–18056

    Article  CAS  PubMed  Google Scholar 

  • Nowak RS, Ellsworth DS, Smith SD (2004) Functional responses of plants to elevated atmospheric CO2: do photosynthetic and productivity data from FACE experiments support early predictions? New Phytol 162:253–280

    Article  Google Scholar 

  • Palmroth S et al (2006) Aboveground sink strength in forests controls the allocation of carbon below ground and its [CO2]-induced enhancement. Proc Natl Acad Sci USA 103:19362–19367

    Article  CAS  PubMed  Google Scholar 

  • Poorter H, Nagel O (2000) The role of biomass allocation in the growth response of plants to different levels of light, CO2, nutrients and water: a quantitative review. Aust J Plant Physiol 27:595–607

    Article  CAS  Google Scholar 

  • Raich JW, Russell AE, Kitayama K, Parton WJ, Vitousek PM (2006) Temperature influences carbon accumulation in moist tropical forests. Ecology 87:76–87

    Article  PubMed  Google Scholar 

  • Reynolds HL, D’Antonio C (1996) The ecological significance of plasticity in root weight ratio in response to nitrogen: opinion. Plant Soil 185:75–97

    Article  CAS  Google Scholar 

  • Reynolds JF, Thornley JHM (1982) A shoot:root partitioning model. Ann Bot 49:585–597

    Google Scholar 

  • Rogers HH, Prior SA, Runion GB, Mitchell RJ (1996) Root to shoot ratio of crops as influenced by CO2. Plant Soil 187:229–248

    Article  CAS  Google Scholar 

  • Rosenberg NJ, Adams DC, Gurevitch J (2000) MetaWin: Statistical software for meta-analysis. In: MetaWin: statistical software for meta-analysis, version 2.0 (edn). Sinauer, Sunderland

  • Schimel DS (1995) Terrestrial ecosystems and the carbon cycle. Global Change Biol 1:77–91

    Article  Google Scholar 

  • Schlesinger WH (1977) Carbon balance in terrestrial detritus. Annu Rev Ecol Syst 8:51–81

    Article  CAS  Google Scholar 

  • Shipley B, Meziane D (2002) The balanced-growth hypothesis and the allometry of leaf and root biomass allocation. Funct Ecol 16:326–331

    Article  Google Scholar 

  • Stulen I, den Hertog J (1993) Root growth and functioning under atmospheric CO2 enrichment. Vegetation 104(105):99–115

    Article  Google Scholar 

  • Tang JJ, Chen J, Chen X (2006) Response of 12 weedy species to elevated CO2 in low-phosphorus-availability soil. Ecol Res 21:664–670

    Article  CAS  Google Scholar 

  • Thornley JHM (1972) A balanced quantitative model for root:shoot ratios in vegetative plants. Ann Bot 36:431–441

    Google Scholar 

  • Tubiello FN et al (2007) Crop response to elevated CO2 and world food supply: a comment on “Food for Thought…” by Long et al, Science 312: 1918–1921, 2006. Eur J Agron 26:215–223

    Article  CAS  Google Scholar 

  • Wang XZ (2007) Effects of species richness and elevated carbon dioxide on biomass accumulation: a synthesis using meta-analysis. Oecologia 152:595–605

    Article  PubMed  Google Scholar 

  • Wilson JB (1988) A review of evidence on the control of shoot:root ratio, in relation to models. Ann Bot 61:433–449

    Google Scholar 

  • Wilson SD, Tilman D (1995) Competitive responses of eight old-field plant species in four environments. Ecology 76:1169–1180

    Article  Google Scholar 

  • Wullschleger SD, Post WM, King AW (1995) On the potential for a CO2 fertilization effects in forests: estimates of the biotic growth factor based on 58 controlled-exposure studies. In: Woodwell GM, Mackenzie FT (eds) Biotic feedbacks in the global climatic system: will the warming feed the warming? Oxford University Press, New York, pp 85–107

    Google Scholar 

  • Wullschleger SD, Tschaplinski TJ, Norby RJ (2002) Plant water relations at elevated CO2: implications for water-limited environments. Plant Cell Environ 25:319–331

    Article  PubMed  Google Scholar 

  • Zak DR, Pregitzer KS, Curtis PS, Teeri JA, Fogel R, Randlett DL (1993) Elevated atmospheric CO2 and feedback between carbon and nitrogen cycles. Plant Soil 151:105–117

    Article  CAS  Google Scholar 

  • Zak DR, Holmes WE, Pregitzer KS, King JS, Ellsworth DS, Kubiske ME (2007) Belowground competition and the response of developing forest communities to atmospheric CO2 and O3. Global Change Biol 13:2230–2238

    Article  Google Scholar 

  • Ziska LH, Bunce JA (2007) Predicting the impact of changing CO2 on crop yields: some thoughts on food. New Phytol 175:607–618

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Financial support for this project was provided in part by Indiana University-Purdue University Indianapolis (IUPUI) Office of Professional Development. We thank anonymous reviewers for constructive comments on an earlier version of this manuscript. We also thank the Interlibrary loan team at the IUPUI University Library for obtaining publications for this project and Dr Xin Chen of Zhejiang University, China, for providing unpublished root results to complement the shoot biomass reported for 12 weedy species in Tang et al. (2006).

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  1. Department of Biology, Indiana University-Purdue University Indianapolis, 723 W. Michigan Street, Indianapolis, IN, 46202, USA

    Xianzhong Wang

  2. Biology Department, Southwestern University, 1001 East University Avenue, Georgetown, TX, 78626, USA

    Daniel R. Taub

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  1. Xianzhong Wang
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Correspondence to Xianzhong Wang.

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Wang, X., Taub, D.R. Interactive effects of elevated carbon dioxide and environmental stresses on root mass fraction in plants: a meta-analytical synthesis using pairwise techniques. Oecologia 163, 1–11 (2010). https://doi.org/10.1007/s00442-010-1572-x

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