, 167:339 | Cite as

Maintenance of C sinks sustains enhanced C assimilation during long-term exposure to elevated [CO2] in Mojave Desert shrubs

  • Iker Aranjuelo
  • Allison L. Ebbets
  • R. Dave Evans
  • David T. Tissue
  • Salvador Nogués
  • Natasja van Gestel
  • Paxton Payton
  • Volker Ebbert
  • Williams W. Adams III
  • Robert S. Nowak
  • Stanley D. Smith
Physiological ecology - Original Paper


During the first few years of elevated atmospheric [CO2] treatment at the Nevada Desert FACE Facility, photosynthetic downregulation was observed in desert shrubs grown under elevated [CO2], especially under relatively wet environmental conditions. Nonetheless, those plants maintained increased A sat (photosynthetic performance at saturating light and treatment [CO2]) under wet conditions, but to a much lesser extent under dry conditions. To determine if plants continued to downregulate during long-term exposure to elevated [CO2], responses of photosynthesis to elevated [CO2] were examined in two dominant Mojave Desert shrubs, the evergreen Larrea tridentata and the drought-deciduous Ambrosia dumosa, during the eighth full growing season of elevated [CO2] treatment at the NDFF. A comprehensive suite of physiological processes were collected. Furthermore, we used C labeling of air to assess carbon allocation and partitioning as measures of C sink activity. Results show that elevated [CO2] enhanced photosynthetic performance and plant water status in Larrea, especially during periods of environmental stress, but not in Ambrosia. δ13C analyses indicate that Larrea under elevated [CO2] allocated a greater proportion of newly assimilated C to C sinks than Ambrosia. Maintenance by Larrea of C sinks during the dry season partially explained the reduced [CO2] effect on leaf carbohydrate content during summer, which in turn lessened carbohydrate build-up and feedback inhibition of photosynthesis. δ13C results also showed that in a year when plant growth reached the highest rates in 5 years, 4% (Larrea) and 7% (Ambrosia) of C in newly emerging organs were remobilized from C that was assimilated and stored for at least 2 years prior to the current study. Thus, after 8 years of continuous exposure to elevated [CO2], both desert perennials maintained their photosynthetic capacities under elevated [CO2]. We conclude that C storage, remobilization, and partitioning influence the responsiveness of these desert shrubs during long-term exposure to elevated [CO2].


Ambrosia dumosa C allocation/partitioning Free-air CO2 enrichment (FACE) Larrea tridentata Photosynthetic downregulation 



Special thanks to Dene Charlet for substantial logistical and data management support. The authors gratefully acknowledge grant support from the Department of Energy’s Terrestrial Carbon Processes Program (DE-FG02-03ER63650, DE-FG02-03ER63651), the NSF Ecosystem Studies Program (DEB-0212812), the Nevada Agricultural Experiment Station, and the Spanish Education and Science Ministry (BFI-2003-09680, PR2008-0247, CGL2009-13079-CO2-02) and Generalitat de Catalunya (BE-11007). Iker Aranjuelo was the recipient of a Juan de la Cierva Research Grant from the Spanish Education and Science Ministry. We also thank the DOE-NTS Operations Office and Bechtel Nevada for site support. Naomi Clark, David Barker, Beth Newingham, and Amrita de Soyza provided assistance with data collection, Lynn Fenstermaker and Eric Knight with site logistical support, and Jim Raymond with sample preparation and processing. Natasja van Gestel acknowledges a scholarship from the Achievement Rewards for College Scientists (ARCS) Foundation, Lubbock Chapter.


  1. Ackerman TL, Romney EM, Wallace A, Kinnear JE (1980) Phenology of desert shrubs in southern Nye County, Nevada. Great Basin Nat Memoirs 4:4–23Google Scholar
  2. Adams WW III, Demmig-Adams B (1992) Operation of the xanthophyll cycle in higher plants in response to diurnal changes in incident sunlight. Planta 186:390–398CrossRefGoogle Scholar
  3. Adams WW III, Zarter CR, Mueh KE, Amiard V, Demmig-Adams B (2006) Energy dissipation and photoinhibition: a continuum of photoprotection. In: Demmig-Adams B, Adams WW III, Matoo AK (eds) Photoprotection, photoinhibition, gene regulation, and environment (Advances in Photosynthesis and Respiration, vol 21). Springer, Dordrecht, pp 49–64Google Scholar
  4. Ainsworth EA, Long SP (2005) Tansley review: 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 165:351–372PubMedCrossRefGoogle Scholar
  5. Ainsworth EA, Rogers A, Nelson R, Long SP (2004) Testing the “source-sink” hypothesis of down-regulation of photosynthesis in elevated [CO2] in the field with single gene substitution in Glycine max. Agr. Forest Meteorol 122:85–94CrossRefGoogle Scholar
  6. Aranjuelo I, Irigoyen JJ, Sánchez-Díaz M, Nogués S (2008a) Carbon partitioning in N2 fixing Medicago sativa plants exposed to different CO2 and temperature conditions. Funct Plant Biol 35:306–317CrossRefGoogle Scholar
  7. Aranjuelo I, Erice G, Nogués S, Morales F, Irigoyen JJ, Sánchez-Díaz M (2008b) The mechanism(s) involved in the photoprotection of PSII at elevated CO2 in nodulated alfalfa plants. Env Exp Bot 64:295–296CrossRefGoogle Scholar
  8. Aranjuelo I, Pardo T, Biel C, Savé R, Azcón-Bieto J, Nogués S (2009) Leaf carbon management in slow-growing plants exposed to elevated CO2. Global Change Biol 15:97–109CrossRefGoogle Scholar
  9. Bernacchi CJ, Singsaas EL, Pimentel C, Portis AR Jr, Long SP (2001) Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant Cell Environ 24:253–259CrossRefGoogle Scholar
  10. Billings SA, Schaeffer SM, Zitzer S, Charlet T, Smith SD, Evans RD (2002) Alterations of nitrogen dynamics under elevated carbon dioxide in an intact Mojave Desert ecosystem: evidence from nitrogen-15 natural abundance. Oecol 131:463–467CrossRefGoogle Scholar
  11. Billings SA, Schaeffer SM, Evans RD (2004) Soil microbial activity and N availability with elevated CO2 in Mojave Desert soils. Glob Biogeo Cycl 18:1011–1022Google Scholar
  12. Ceulemans R (1997) Direct impacts of CO2 and temperature on physiological processes in trees. In: Mohren GMJ, Kramer K, Sabaté S (eds) Impacts of global change on tree physiology and forest ecosystems. Kluwer, Dordrecht, pp 3–14Google Scholar
  13. Chaves MM, Pereira JS, Cerasoli S, Clifton-Brown J, Miglietta F, Raschi A (1995) Leaf metabolism during summer drought in Quercus ilex trees with lifetime exposure to elevated CO2. J Biogeogr 22:255–259CrossRefGoogle Scholar
  14. Clark NM, Apple ME, Nowak RS (2010) The effects of elevated CO2 on root respiration rates of two Mojave Desert shrubs. Global Change Biol 16:1566–1575CrossRefGoogle Scholar
  15. Crous K, Reich PB, Hunter MD, Ellsworth DS (2010) Maintenance of leaf N controls the photosynthetic CO2 response of grassland species exposed to 9 years of free-air CO2 enrichment. Global Change Biol 16:2076–2088CrossRefGoogle Scholar
  16. Demmig-Adams B, Adams WW III (2006) Tansley review: photoprotection in an ecological context: the remarkable complexity of thermal dissipation. New Phytol 172:11–21PubMedCrossRefGoogle Scholar
  17. Ellsworth DS, Reich PB, Naumburg ES, Koch GW, Kubiske ME, Smith SD (2004) Photosynthesis, carboxylation and leaf nitrogen responses of 16 species to elevated pCO2 across four free-air CO2 enrichment experiments in forest, grassland and desert. Global Change Biol 10:2121–2138CrossRefGoogle Scholar
  18. Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33:317–345CrossRefGoogle Scholar
  19. Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90CrossRefGoogle Scholar
  20. Farquhar GD, Hubick KT, Condon AG, Richards RA (1989) Carbon isotope fractionation and water-use efficiency. In: Rundel PW, Ehleringer JR, Nagy KA (eds) Stable isotopes in ecological research (Ecological Studies vol 68). Springer, Berlin, pp 21–40Google Scholar
  21. Farrar J, Pollock C, Gallagher J (2000) Sucrose and the integration of metabolism in vascular plants. Plant Sci 154:1–11PubMedCrossRefGoogle Scholar
  22. Franklin O, McMurtrie R, Iversen CM, Crous KY, Finzi A, Tissue DT, Ellsworth DS, Oren R, Norby RJ (2009) Forest fine-root production and nitrogen use under elevated CO2: contrasting responses in evergreen and deciduous trees explained by a common principle. Global Change Biol 15:132–144CrossRefGoogle Scholar
  23. Gilmore AM, Yamamoto HY (1991) Resolution of lutein and zeaxanthin using a non-encapped, lightly carbon-loaded C18 high-performance liquid chromatographic column. J Chromatogr 543:137–145CrossRefGoogle Scholar
  24. Hamerlynck EP, Huxman TE, Nowak RS, Redar S, Loik ME, Jordan DN, Zitzer SF, Coleman JS, Seemann JR, Smith SD (2000) Photosynthetic responses of Larrea tridentata to a step-increase in atmospheric CO2 at the Nevada Desert FACE Facility. J Arid Environ 44:425–436CrossRefGoogle Scholar
  25. Hamerlynck EP, Huxman TE, Charlet TN, Smith SD (2002) Effects of elevated CO2 (FACE) on the functional ecology of the drought-deciduous Mojave Desert shrub, Lycium andersonii. Environ Exp Bot 48:93–106CrossRefGoogle Scholar
  26. Harley PC, Thomas RB, Reynolds JF, Strain BR (1992) Modelling photosynthesis of cotton grown in elevated CO2. Plant Cell Environ 15:271–282CrossRefGoogle Scholar
  27. Housman DC, Naumburg E, Huxman TE, Charlet TN, Nowak RS, Smith SD (2006) Increases in desert shrub productivity under elevated CO2 vary with water availability. Ecosystems 9:374–385CrossRefGoogle Scholar
  28. Huxman TE, Hamerlynck EP, Moore BD, Smith SD, Jordan DN, Zitzer SF, Nowak RS, Coleman JS, Seemann JR (1998) Photosynthetic down-regulation in Larrea tridentata exposed to elevated atmospheric CO2: interaction with drought under glasshouse and field (FACE) exposure. Plant Cell Environ 21:1153–1161CrossRefGoogle Scholar
  29. Hymus GJ, Ellsworth DS, Baker NR, Long SP (1999) Does free-air carbon dioxide enrichment affect photochemical energy use by evergreen trees in different seasons? A chlorophyll fluorescence study of mature loblolly pine. Plant Physiol 120:1183–1191PubMedCrossRefGoogle Scholar
  30. Jifon JL, Wolfe DW (2002) Photosynthetic acclimation to elevated CO2 in Phaseolus vulgaris L is altered by growth response to nitrogen supply. Glob Change Biol 8:1018–1027CrossRefGoogle Scholar
  31. Jin V, Evans RD (2007) Elevated CO2 affects microbial carbon substrate use and N cycling in Mojave Desert soils. Glob Change Biol 13:1–12CrossRefGoogle Scholar
  32. Jin V, Evans RD (2010) Microbial 13C utilization patterns via stable isotope probing of phospholipid biomarkers in Mojave Desert soils exposed to ambient and elevated atmospheric CO2. Glob Change Biol 16:2334–2344CrossRefGoogle Scholar
  33. Jordan DB, Ogren WL (1984) The CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase. Dependence on ribulose-bisphosphate concentration, pH and temperature. Planta 161:308–313Google Scholar
  34. Jordan DN, Zitzer SF, Hendrey GR, Lewin KF, Nagy J, Nowak RS, Smith SD, Coleman JS, Seemann JR (1999) Biotic, abiotic and performance aspects of the Nevada Desert free-air CO2 zent (FACE) facility. Global Change Biol 6:659–668CrossRefGoogle Scholar
  35. Kodama N, Ferrio JP, Brüggemann N, Gessler A (2010) Short-term dynamics of the carbon isotope composition of CO2 emitted from a wheat agroecosystem—physiological and environmental controls. Plant Biol 13:115–125Google Scholar
  36. Körner C, Asshoff R, Bignucolo O, Hättenschwiler S, Keel SG, Peláez-Riedl S, Pepin S, Siegwolf RTW, Zotz G (2005) Carbon flux and growth in mature deciduous forest trees exposed to elevated CO2. Science 309:1360–1362PubMedCrossRefGoogle Scholar
  37. Lacointe A, Kajji A, Daudet FA, Archer P, Frossard JS (1993) Mobilization of carbon reserves in young walnut trees. Acta bot Gallica 140:435–441Google Scholar
  38. Lemon ER (1983) CO2 and plants: the response of plants to rising levels of atmospheric carbon dioxide (AAAS Selected Symposium 84). Westview, BoulderGoogle Scholar
  39. Lewis JD, Wang XZ, Griffin KL, Tissue DT (2002) Effects of age and ontogeny on photosynthetic responses of a determinate annual plant to elevated CO2 concentrations. Plant Cell Environ 25:359–368CrossRefGoogle Scholar
  40. Logan BA, Combs A, Myers K, Kent R, Stanley L, Tissue DT (2009) Seasonal response of photosynthetic electron transport and energy dissipation in the eighth year of exposure to elevated atmospheric CO2 (FACE) in Pinus taeda (loblolly pine). Tree Physiol 29:789–797PubMedCrossRefGoogle Scholar
  41. Long SP, Ainsworth EA, Rogers A, Ort DR (2004) Rising atmospheric carbon dioxide: plants FACE the future. Annu Rev Plant Biol 55:591–628PubMedCrossRefGoogle Scholar
  42. Moore BD, Cheng SH, Sims D, Seemann JR (1999) The biochemical and molecular basis for photosynthetic acclimation to elevated atmospheric CO2. Plant Cell Environ 22:567–582CrossRefGoogle Scholar
  43. Morgan JA, Skinner RH, Hanson JD (2001) Nitrogen and CO2 affect regrowth and biomass partitioning differently in forage of three functional groups. Crop Sci 41:78–86CrossRefGoogle Scholar
  44. Naumburg E, Housman DC, Huxman TE, Charlet TN, Loik ME, Smith SD (2003) Photosynthetic responses of Mojave Desert shrubs to free air CO2 enrichment are greatest during wet years. Global Change Biol 9:276–285CrossRefGoogle Scholar
  45. Naumburg E, Loik ME, Smith SD (2004) Photosynthetic responses of Larrea tridentata to seasonal temperature extremes under elevated CO2. New Phytol 162:323–330CrossRefGoogle Scholar
  46. Nogués S, Tcherkez G, Cornic G, Ghashghaie J (2004) Respiratory carbon metabolism following illumination in intact French bean leaves using 13C/12C isotope labeling. Plant Physiol 136:3245–3254PubMedCrossRefGoogle Scholar
  47. Nogués S, Aranjuelo I, Pardo T, Azcón-Bieto J (2008) Assessing the stable-carbon isotopic composition of intercellular CO2 in a CAM plant at two CO2 levels. Rapid Comm Mass Spectr 22:1017–1022CrossRefGoogle Scholar
  48. Nowak RS, Zitzer SF, Babcock D, Smith-Longozo V, Charlet TN, Coleman JS, Seemann JR, Smith SD (2004) Elevated atmospheric CO2 does not conserve soil moisture in the Mojave Desert. Ecology 85:93–99CrossRefGoogle Scholar
  49. Richter A, Wanek W, Werner RA, Ghashghaie J, Jäggi M, Gessler A, Brugnoli E, Hettmann E, Göttlicher SG, Salmon Y, Bathellier C, Kodama N, Nogués S, SØe A, Volders F, Sörgel K, Blöchl A, Siegwolf RTW, Buchmann N, Gleixner G (2009) Preparation of starch and soluble sugars of plant material for the analyses of carbon isotope composition: a comparison of methods. Rapid Comm Mass Spectr 23:2476–2488CrossRefGoogle Scholar
  50. Schaeffer SM (2005) Determining the effects of global change on soil nitrogen cycling in arid ecosystems (Ph.D. thesis). University of Arkansas, FayettevilleGoogle Scholar
  51. Sharifi MR, Meinzer FC, Nilsen ET, Rundel PW, Virginia RA, Jarrell WM, Herman DJ, Clark PC (1988) Effects of manipulation of water and nitrogen supplies on the quantitative phenology of Larrea tridentata (creosote bush) in the Sonoran Desert of California. Am J Bot 75:1163–1174CrossRefGoogle Scholar
  52. Smith SD, Nowak RS (1990) Ecophysiology of plants in the intermountain lowlands. In: Osmond CB, Pitelka LF, Hidy GM (eds) Plant biology of the basin and range. Springer, New York, pp 182–196Google Scholar
  53. Smith SD, Monson RK, Anderson JE (1997) Physiological ecology of North American desert plants. Springer, BerlinGoogle Scholar
  54. Tcherkez G, Nogues S, Bleton J, Cornic G, Badeck F, Ghashghaie J (2003) Metabolic origin of carbon isotope composition of leaf dark-respired CO2 in French bean. Plant Physiol 131:237–244PubMedCrossRefGoogle Scholar
  55. Theobald JC, Mitchell RAC, Parry MAJ, Lawlor DW (1998) Estimating the excess investment in ribulose-1,5-bisphosphate carboxylase/oxygenase in leaves of spring wheat grown under elevated CO2. Plant Physiol 118:945–955Google Scholar
  56. Thomas RB, Strain BR (1991) Root restriction as a factor in photosynthetic acclimation of cotton seedlings grown in elevated carbon dioxide. Plant Physiol 96:627–634PubMedCrossRefGoogle Scholar
  57. Tissue DT, Thomas RB, Strain BR (1993) Long-term effects of elevated CO2 and nutrients on photosynthesis and rubisco in loblolly pine seedlings. Plant Cell Environ 16:859–865CrossRefGoogle Scholar
  58. Tissue DT, Griffin KL, Turnbull MT, Whitehead D (2001) Canopy position and needle age affect photosynthetic response in field-grown Pinus taeda after five years exposure to elevated carbon dioxide partial pressure. Tree Physiol 21:915–923PubMedGoogle Scholar
  59. Tissue DT, Griffin KL, Turnbull MH, Whitehead D (2005) Stomatal and non-stomatal limitations to photosynthesis in four tree species in a temperate rainforest dominated by Dacrydium cupressinum in New Zealand. Tree Physiol 25:447–456PubMedGoogle Scholar
  60. von Felten S, Hättenschwiler S, Saurer M, Siegwolf R (2007) Carbon allocation in shoots of alpine treeline conifers in a CO2 enriched environment. Trees 21:283–294CrossRefGoogle Scholar
  61. Wallace A, Bamberg SA, Cha JW (1974) Quantitative studies of roots of perennial plants in the Mojave Desert. Ecology 55:1160–1162CrossRefGoogle Scholar
  62. Wullschleger SD (1993) Biochemical limitations to carbon assimilation in C3 plants—a retrospective analysis of the ACi curves from 109 species. J Exp Bot 44:907–920CrossRefGoogle Scholar
  63. Zak DR, Pregitzer KS, King JS, Holmes WE (2000) Elevated atmospheric CO2, fine roots and the response of soil microorganisms: a review and hypothesis. New Phytol 147:201–222CrossRefGoogle Scholar
  64. Zhu C, Zhu J, Zeng Q, Liu G, Xie Z, Tang H, Cao J, Zhao X (2009) Elevated CO2 accelerates flag senescence in wheat due to ear photosynthesis which causes greater ear nitrogen sink capacity and ear carbon sink limitation. Funct Plant Biol 36:291–299CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Iker Aranjuelo
    • 1
    • 3
  • Allison L. Ebbets
    • 4
    • 5
  • R. Dave Evans
    • 6
  • David T. Tissue
    • 7
    • 8
  • Salvador Nogués
    • 2
  • Natasja van Gestel
    • 7
  • Paxton Payton
    • 7
  • Volker Ebbert
    • 9
  • Williams W. Adams III
    • 9
  • Robert S. Nowak
    • 3
  • Stanley D. Smith
    • 4
  1. 1.Fisiologia Vegetal y AgrobiologiaInstituto de Agrobiotecnología, Universidad Pública de Navarra-CSIC-Gobierno de NavarraMutilva BajaSpain
  2. 2.Unitat de Fisologia Vegetal, Facultat de BiologiaUniversitat de BarcelonaBarcelonaSpain
  3. 3.Department of Natural Resources and Environmental ScienceUniversity of NevadaReno NevadaUSA
  4. 4.School of Life SciencesUniversity of NevadaLas VegasUSA
  5. 5.Stratus Consulting, Inc.BoulderUSA
  6. 6.School of Biological SciencesWashington State UniversityPullman WashingtonUSA
  7. 7.Department of Biological SciencesTexas Tech UniversityLubbockUSA
  8. 8.Hawkesbury Institute for the EnvironmentUniversity of Western SydneyRichmondAustralia
  9. 9.Department of Ecology and Evolutionary BiologyUniversity of ColoradoBoulderUSA

Personalised recommendations