Advertisement

Photosynthesis Research

, Volume 134, Issue 1, pp 59–70 | Cite as

Root-derived bicarbonate assimilation in response to variable water deficit in Camptotheca acuminate seedlings

  • Sen Rao
  • Yanyou Wu
Original Article

Abstract

Water deficit is one of the key factors that limits the carbon (C) assimilation and productivity of plants. The effect of variable water deficit on recently root-derived bicarbonate assimilation in Camptotheca acuminate seedlings was investigated. Three-month-old seedlings were subjected to three water regimes, well-watered (WW), moderate stress (MS), and severe stress (SS) induced by polyethyleneglycol, in conjunction with relatively high (H) and low (L) natural 13C-abundance of NaHCO3-labeled treatments in hydroponics for 14 days. The δ13C of the newly expanded leaves in H were generally more enriched in heavy isotopes than were those in L, indicative of the involvement of bicarbonate in aboveground tissues. The C isotope fractionation of newly expanded leaves relative to air (∆13Cair-leaves) ranged from 17.78 to 21.78‰ among the treatments. The ∆13Cair-leaves under the MS and SS treatments in H were both more negative than was that in L. A linear regression between Ci/Ca and ∆13Cair-leaves in both L and H were different from the theoretical regression. On the basis of the two end-member mixing model, the proportion of fixed CO2 supplied from bicarbonate contributing to the total photosynthetically inorganic C assimilation were 10.34, 20.05 and 16.60% under the WW, MS, and SS treatments, respectively. These results indicated that the increase in water deficit decreased the atmospheric CO2 gain but triggered a compensatory use of bicarbonate in C. acuminate seedlings.

Keywords

Water deficit Bicarbonate utilization Carbon assimilation Carbon isotope fractionation 

Notes

Acknowledgements

This work was supported by the National Key Basic Research Program of China (2013CB956701), the National Key Research and development Program of China (2016YFC0502602) and National Natural Science Foundation of China (U1612441). The authors wish to thank Yu Wang and Ning An for their technical assistance, and two anonymous reviewers and Rui Wang for valuable comments on this manuscript.

Supplementary material

11120_2017_414_MOESM1_ESM.xls (100 kb)
Supplementary material 1 (XLS 99 KB)

References

  1. Ahmed IM, Cao F, Zhang M, Chen X, Zhang G, Wu F (2013) Difference in yield and physiological features in response to drought and salinity combined stress during anthesis in Tibetan wild and cultivated barleys. PLoS ONE 8(10):e77869CrossRefPubMedPubMedCentralGoogle Scholar
  2. Ancillotti C, Bogani P, Biricolti S, Calistri E, Checchini L, Ciofi L, Gonnelli C, Del Bubba M (2015) Changes in polyphenol and sugar concentrations in wild type and genetically modified Nicotiana langsdorffii Weinmann in response to water and heat stress. Plant Physiol Biochem 97:52–61CrossRefPubMedGoogle Scholar
  3. Aubrey DP, Teskey RO (2009) Root-derived CO2 efflux via xylem stream rivals soil CO2 efflux. New Phytol 184(1):35–40CrossRefPubMedGoogle Scholar
  4. Badeck FW, Tcherkez G, Nogues S, Piel C, Ghashghaie J (2005) Post-photosynthetic fractionation of stable carbon isotopes between plant organs—a widespread phenomenon. Rapid Commun Mass Spectrom 19(11):1381–1391CrossRefPubMedGoogle Scholar
  5. Bialczyk J, Lechowsk Z (1995) Chemical composition of xylem sap of tomato grown on bicarbonate containing medium. J Plant Nutr 18(10):2005–2021CrossRefGoogle Scholar
  6. Bloemen J, Bauweraerts I, De Vos F, Vanhove C, Vandenberghe S, Boeckx P, Steppe K (2015) Fate of xylem-transported 11C- and 13C-labeled CO2 in leaves of poplar. Physiol Plant 153(4):555–564CrossRefPubMedGoogle Scholar
  7. Bloemen J, Teskey RO, McGuire MA, Aubrey DP, Steppe K (2016) Root xylem CO2 flux: an important but unaccounted-for component of root respiration. Trees 30(2):343–352CrossRefGoogle Scholar
  8. Bloom PR, Inskeep WP (1986) Factors affecting bicarbonate chemistry and iron chlorosis in soils. J Plant Nutr 9(3–7):215–228CrossRefGoogle Scholar
  9. Boxma R (1972) Bicarbonate as the most important soil factor in lime-induced chlorosis in the Netherlands. Plant Soil 37(2):233–243CrossRefGoogle Scholar
  10. Brendel O (2001) Does bulk-needle δ13C reflect short-term discrimination? Ann For Sci 58(2):135–141CrossRefGoogle Scholar
  11. Brugnoli E, Hubick KT, von Caemmerer S, Wong SC, Farquhar GD (1988) Correlation between the carbon isotope discrimination in leaf starch and sugars of C3 plants and the ratio of intercellular and atmospheric partial pressures of carbon dioxide. Plant Physiol 88(4):1418–1424CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cernusak LA, Hutley LB (2011) Stable isotopes reveal the contribution of corticular photosynthesis to growth in branches of Eucalyptus miniata. Plant Physiol 155(1):515–523CrossRefPubMedGoogle Scholar
  13. Chaves MM, Oliveira MM (2004) Mechanisms underlying plant resilience to water deficits: prospects for water-saving agriculture. J Exp Bot 55(407):2365–2384CrossRefPubMedGoogle Scholar
  14. Covarrubias JI, Rombolà AD (2013) Physiological and biochemical responses of the iron chlorosis tolerant grapevine rootstock 140 Ruggeri to iron deficiency and bicarbonate. Plant soil 370(1–2):305–315CrossRefGoogle Scholar
  15. Cranswick AM, Rook DA, Zabkiewicz JA (1987) Seasonal changes in carbohydrate concentration and composition of different tissue types of Pinus radiata trees. N Z J For Sci 17:229–245Google Scholar
  16. Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP (2002) Stable isotopes in plant ecology. Annu Rev Ecol Syst 33:507–559CrossRefGoogle Scholar
  17. De Micco V, Aronne G (2012) Morpho-anatomical traits for plant adaptation to drought. In: Plant responses to drought stress, Springer Berlin Heidelberg, p 37–61CrossRefGoogle Scholar
  18. Deng Y, Jiang Z, Qin X (2012) Water source partitioning among trees growing on carbonate rock in a subtropical region of Guangxi, China. Environ Earth Sci 66(2): 635–640CrossRefGoogle Scholar
  19. Durand M, Porcheron B, Hennion N, Maurousset L, Lemoine R, Pourtau N (2016) Water deficit enhances C export to the roots in Arabidopsis thaliana plants with contribution of sucrose transporters in both shoot and roots. Plant Physiol 170(3):1460–1479PubMedPubMedCentralGoogle Scholar
  20. Enoch HZ, Olesen JM (1993) Plant response to irrigation with water enriched with carbon dioxide. New Phytol 125(2):249–258CrossRefGoogle Scholar
  21. Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Biol 40(1):503–537CrossRefGoogle Scholar
  22. Ford CR, Wurzburger N, Hendrick RL, Teskey RO (2007) Soil DIC uptake and fixation in Pinus taeda seedlings and its C contribution to plant tissues and ectomycorrhizal fungi. Tree Physiol 27(3):375–383CrossRefPubMedGoogle Scholar
  23. Gillon JS, Griffiths H (1997) The influence of (photo)respiration on carbon isotope discrimination in plants. Plant Cell Environ 20(10):1217–1230CrossRefGoogle Scholar
  24. Göttlicher S, Knohl A, Wanek W, Buchmann N, Richter A (2006) Short-term changes in carbon isotope composition of soluble carbohydrates and starch: from canopy leaves to the root system. Rapid Commun Mass Spectrom 20(4):653–660CrossRefPubMedGoogle Scholar
  25. Grossiord C, Mareschal L, Epron D (2012) Transpiration alters the contribution of autotrophic and heterotrophic components of soil CO2 efflux. New Phytol 194(3):647–653CrossRefPubMedGoogle Scholar
  26. Hang H, Wu Y (2016) Quantification of photosynthetic inorganic carbon utilisation via a bidirectional stable carbon isotope tracer. Acta Geochimica 35(2):130–137CrossRefGoogle Scholar
  27. Hu B, Simon J, Rennenberg H (2013) Drought and air warming affect the species-specific levels of stress-related foliar metabolites of three oak species on acidic and calcareous soil. Tree Physiol 33(5):489–504CrossRefPubMedGoogle Scholar
  28. IPCC (2014) Climate Change 2014: Synthesis Report. In: Core Writing Team, Pachauri RK, Meyer LA (eds) Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, Switzerland, pp 19–29Google Scholar
  29. Jung V, Albert CH, Violle C, Kunstler G, Loucougaray G, Spiegelberger T (2014) Intraspecific trait variability mediates the response of subalpine grassland communities to extreme drought events. J Ecol 102(1):45–53CrossRefGoogle Scholar
  30. Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63(4):1593–1608CrossRefPubMedPubMedCentralGoogle Scholar
  31. Kumar MS, Ali K, Dahuja A, Tyagi A (2015) Role of phytosterols in drought stress tolerance in rice. Plant Physiol Biochem 96:83–89CrossRefPubMedGoogle Scholar
  32. Lamade E, Tcherkez G, Darlan NH, Rodrigues RL, Fresneau C, Mauve C, Lamothe-Sibold M, Sketriené D, Ghashghaie J (2016) Natural 13C distribution in oil palm (Elaeis guineensis Jacq.) and consequences for allocation pattern. Plant cell Environ 39(1):199–212CrossRefPubMedGoogle Scholar
  33. Lambers H, Chapin III FS, Pons TL (2008) Photosynthesis, respiration, and long-distance transport. In: Plant physiological ecology. Springer, New York, pp 11–99Google Scholar
  34. Lauteri M, Haworth M, Serraj R, Monteverdi MC, Centritto M (2014) Photosynthetic diffusional constraints affect yield in drought stressed rice cultivars during flowering. PloS ONE 9(10):e109054CrossRefPubMedPubMedCentralGoogle Scholar
  35. Levy PE, Meir P, Allen SJ, Jarvis PG (1999) The effect of aqueous transport of CO2 in xylem sap on gas exchange in woody plants. Tree Physiol 19(1):53–58CrossRefPubMedGoogle Scholar
  36. Martínez-Lüscher J, Morales F, Sánchez-Díaz M, Delrot S, Aguirreolea J, Gomès E, Pascual I (2015) Climate change conditions (elevated CO2 and temperature) and UV-B radiation affect grapevine (Vitis vinifera cv. Tempranillo) leaf carbon assimilation, altering fruit ripening rates. Plant Sci 236:168–176CrossRefPubMedGoogle Scholar
  37. Masyagina O, Prokushkin A, Kirdyanov A, Artyukhov A, Udalova T, Senchenkov S, Rublev A (2016) Intraseasonal carbon sequestration and allocation in larch trees growing on permafrost in Siberia after 13C labeling (two seasons of 2013–2014 observation). Photosynth Res 131(1):267–274Google Scholar
  38. McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytologist 178(4):719–739CrossRefPubMedGoogle Scholar
  39. Millero FJ (2003) Physicochemical controls on seawater. Treatise Geochem 6:1–21Google Scholar
  40. Moroney JV, Bartlett SG, Samuelsson G (2001) Carbonic anhydrases in plants and algae. Plant Cell Environ 24(2):141–153CrossRefGoogle Scholar
  41. Msilini N, Attia H, Bouraoui N, M’rah S, Ksouri R, Lachaâl M, Ouerghi Z (2009) Responses of Arabidopsis thaliana to bicarbonate-induced iron deficiency. Acta Physiol Plant 31(4):849–853CrossRefGoogle Scholar
  42. O’Leary MH (1981) Carbon isotope fractionation in plants. Phytochemistry 20(4):553–567CrossRefGoogle Scholar
  43. Pan G, He S, Cao J, Tao Y, Sun Y (2002) Variation of δ13C in karst soil in Yaji Karst Experiment Site, Guilin. Chin Sci Bull 47(6):500–503CrossRefGoogle Scholar
  44. Pandey DM, Goswami CL, Kumar B, Jain S (2000) Hormonal regulation of photosynthetic enzymes in cotton under water stress. Photosynthetica 38(3):403–407CrossRefGoogle Scholar
  45. Pang J, Yang J, Ward P, Siddique KH, Lambers H, Tibbett M, Ryan M (2011) Contrasting responses to drought stress in herbaceous perennial legumes. Plant Soil 348(1–2):299–314CrossRefGoogle Scholar
  46. Ramírez DA, Parra A, de Dios VR, Moreno JM (2012) Differences in morpho-physiological leaf traits reflect the response of growth to drought in a seeder but not in a resprouter Mediterranean species. Funct Plant Biol 39(4):332–341CrossRefGoogle Scholar
  47. Rombolà AD, Gogorcena Y, Larbi A, Morales F, Baldi E, Marangoni B, Tagliavini M, Abadía J (2005) Iron deficiency-induced changes in carbon fixation and leaf elemental composition of sugar beet (Beta vulgaris) plants. Plant soil 271(1–2):39–45CrossRefGoogle Scholar
  48. Rovira P, Vallejo VR (2008) Changes in δ13C composition of soil carbonates driven by organic matter decomposition in a Mediterranean climate: a field incubation experiment. Geoderma 144(3):517–534CrossRefGoogle Scholar
  49. Salomons W, Mook WG (1986) Isotope geochemistry of carbonates in the weathering zone. Handb Environ Isotope Geochem 2:239–269Google Scholar
  50. Sapeta H, Costa JM, Lourenco T, Maroco J, Van der Linde P, Oliveira MM (2013) Drought stress response in Jatropha curcas: growth and physiology. Environ Exp Bot 85:76–84CrossRefGoogle Scholar
  51. Stringer JW, Kimmerer TW (1993) Refixation of xylem sap CO2 in Populus deltoides. Physiol Plant 89(2):243–251CrossRefGoogle Scholar
  52. Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R (2014) Abiotic and biotic stress combinations. New Phytol 203(1):32–43CrossRefPubMedGoogle Scholar
  53. Tang YT, Cloquet C, Deng THB, Sterckeman T, Echevarria G, Yang WJ, Morel JL, Qiu RL (2016) Zinc isotope fractionation in the hyperaccumulator Noccaea caerulescens and the nonaccumulating plant Thlaspi arvense at low and high Zn supply. Environ Sci Technol 50(15):8020–8027CrossRefPubMedGoogle Scholar
  54. Teskey RO, McGuire MA (2007) Measurement of stem respiration of sycamore (Platanus occidentalis L.) trees involves internal and external fluxes of CO2 and possible transport of CO2 from roots. Plant Cell Environ 30(5):570–579CrossRefPubMedGoogle Scholar
  55. van der Weele CM, Spollen WG, Sharp RE, Baskin TI (2000) Growth of Arabidopsis thaliana seedlings under water deficit studied by control of water potential in nutrient-agar media. J Exp Bot 51(350):1555–1562CrossRefPubMedGoogle Scholar
  56. Wang Z, Xu Y, Chen T, Zhang H, Yang J, Zhang J (2015) Abscisic acid and the key enzymes and genes in sucrose-to-starch conversion in rice spikelets in response to soil drying during grain filling. Planta 241(5):1091–1107CrossRefPubMedGoogle Scholar
  57. Wegner LH, Zimmermann U (2004) Bicarbonate-induced alkalinization of the xylem sap in intact maize seedlings as measured in situ with a novel xylem pH probe. Plant Physiol 136(3):3469–3477CrossRefPubMedPubMedCentralGoogle Scholar
  58. Wu YY, Xing DK (2012) Effect of bicarbonate treatment on photosynthetic assimilation of inorganic carbon in two plant species of Moraceae. Photosynthetica 50(4):587–594CrossRefGoogle Scholar
  59. Yang CW, Xu HH, Wang LL, Liu J, Shi DC, Wang DL (2009) Comparative effects of salt-stress and alkali-stress on the growth, photosynthesis, solute accumulation, and ion balance of barley plants. Photosynthetica 47(1):79–86CrossRefGoogle Scholar
  60. Yasir TA, Min D, Chen X, Condon AG, Hu YG (2013) The association of carbon isotope discrimination (∆) with gas exchange parameters and yield traits in Chinese bread wheat cultivars under two water regimes. Agric Water Manag 119:111–120CrossRefGoogle Scholar
  61. Ying YQ, Song LL, Jacobs DF, Mei L, Liu P, Jin SH, Wu JS (2014) Physiological response to drought stress in Camptotheca acuminata seedlings from two provenances. Front Plant Sci 6:361Google Scholar
  62. Yu JH, Yuan SS, Tang ZH, Li DW, Zu YG (2012) Degradation and ecological functions of RubiscoLSU during severe drought stress leaves of Camptotheca acuminata. Adv Mater Res 518:5429–5435CrossRefGoogle Scholar
  63. Zivcak M, Brestic M, Balatova Z, Drevenakova P, Olsovska K, Kalaji HM, Yang X, Allakhverdiev SI (2013) Photosynthetic electron transport and specific photoprotective responses in wheat leaves under drought stress. Photosynth Res 117(1–3):529–546CrossRefPubMedGoogle Scholar
  64. Zuo Y, Ren L, Zhang F, Jiang RF (2007) Bicarbonate concentration as affected by soil water content controls iron nutrition of peanut plants in a calcareous soil. Plant Physiol Biochem 45(5):357–364CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  1. 1.State Key Laboratory of Environmental Geochemistry, Institute of GeochemistryChinese Academy of SciencesGuiyangPeople’s Republic of China
  2. 2.University of Chinese Academy of SciencesBeijingPeople’s Republic of China

Personalised recommendations