Plant and Soil

, Volume 404, Issue 1–2, pp 277–291 | Cite as

Allocation of photosynthestically-fixed carbon in plant and soil during growth of reed (Phragmites australis) in two saline soils

  • Ling Li
  • Shaojun QiuEmail author
  • Yinping Chen
  • Xingliang Xu
  • Ximei Zhao
  • Peter Christie
  • Minggang XuEmail author
Regular Article



Terrestrial carbon (C) sequestration is derived mainly from plant photosysthetically-fixed C deposition but soil organic C (SOC) content in saline soils is generally low due to low deposition of C from restricted plant growth. It is important to explore the effects of soil salinity on the allocation of photosynthetically-fixed C to better understand C sequestration in saline wetland soils.


We conducted a pot experiment in which reed (Phragmites australis) was grown in a low salinity (LS) soil and a high salinity (HS) soil from the Yellow River Delta under flooded conditions. The allocation of photosynthetically-fixed C into plant tissues, SOC, dissolved organic C (DOC), microbial biomass C (MBC), particulate organic C (POC), and mineral-associated organic C (MAOC) was determined using a 13C pulse-labeling method after four labeling events during the 125-day-long reed growing season and destructive sampling immediately at the end of six hours of pulse labeling (end 6-h) and on the final harvest day (final day).


In most cases soil salinity, reed growth stage, or reed biomass significantly (P < 0.05) affected the deposition of photosynthetically-fixed C into the plant-soil system. At all four pulses at end 6-h the high salinity soil had significantly (P < 0.05) lower percentage net assimilated 13C in the roots and significantly higher (P < 0.05) percentage net assimilated 13C in the soil than did the low salinity soil. At both end 6-h and on the final day the high salinity soil had significantly (P < 0.05) lower SO13C, and significantly (P < 0.05) higher DO13C/SO13C ratio than the low salinity soil except for pulses 3 and 4 on the final day. The majority of photosynthetically-fixed C in soil was deposited into MAOC pools and >80 % of deposited SO13C was present as MAOC in the high salinity soil due to its significantly (P < 0.05) higher clay content compared with the low salinity soil.


Soil salinity affected the allocation of photosynthetically-fixed C in the plant-soil system, and soil texture altered the allocation of rhizodeposition C in different soil particles.


Soil salinity Soil organic C pools Photosynthetically-fixed C 13C pulse labeling Flooded pot experiment 



This work was funded by the National Natural Science Foundation of China (41101220), the Outstanding Young Scientist Research Award Fund of Shandong Province, China (BS2011HZ001), the “973” program (2013CB127405), and National Nonprofit Institute Research Grant of CAAS (IARRP-2015-27).

Supplementary material

11104_2016_2840_MOESM1_ESM.doc (599 kb)
ESM 1 (DOC 599 kb)


  1. Amato M, Ladd JN (1992) Decomposition of C-14 labeled glucose and legume material in soil–properties influencing the accumulation of organic residue-C and microbial biomass-C. Soil Biol Biochem 24:455–464CrossRefGoogle Scholar
  2. An T, Schaeffer S, Li S, Fu S, Pei J, Li H, Zhuang J, Radosevich M, Wang J (2015) Carbon fluxes from plants to soil and dynamics of microbial immobilization under plastic film mulching and fertilizer application using 13C pulse-labeling. Soil Biol Biochem 80:53–61CrossRefGoogle Scholar
  3. Angers DA, Recous S, Aita C (1997) Fate of carbon and nitrogen in water-stable aggregates during decomposition of 13C15N-labelled wheat straw in situ. Eur J Soil Sci 48:295–300CrossRefGoogle Scholar
  4. Bahn M, Schmitt M, Siegwolf R, Richter A, Brüggemann N (2009) Does photosynthesis affect grassland soil-respired CO2 and its carbon isotope composition on a diurnal timescale? New Phytol 182:451–460CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bassirirad H, Radin JW, Matsuda K (1991) Temperature dependent water and ion-transport properties of barley and Sorghum roots. 1. Relationship to leaf growth. Plant Physiol 97:426–432CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bhattacharyya P, Roy KS, Neogi S, Manna MC, Adhya TK, Rao KS, Nayak AK (2013) Influence of elevated carbon dioxide and temperature on belowground carbon allocation and enzyme activities in tropical flooded soil planted with rice. Environ Monit Assess 185:8659–8671CrossRefPubMedGoogle Scholar
  7. Barré P, Fernandez-Ugalde O, Virto I, Velde B, Chenu C (2014) Impact of phyllosilicate mineralogy on organic carbon stabilization in soils: incomplete knowledge and exciting prospects. Geoderma 235–236:382–395CrossRefGoogle Scholar
  8. Blagodatskaya E, Littschwager J, Lauerer M, Kuzyakov Y (2010) Growth rates of rhizosphere microorganisms depend on competitive abilities of plants and N supply. Plant Biosyst 144:408–413CrossRefGoogle Scholar
  9. Briedis C, Sá JCM, Caires EF, Navarro JF, Inagaki TM, Boer A, Neto CQ, Ferreira AO, Canalli LB, Santos JB (2012) Soil organic matter pools and carbon-protection mechanisms in aggregate classes influenced by surface liming in a no-till system. Geoderma 170:80–88CrossRefGoogle Scholar
  10. Chambers LG, Osborne TZ, Reddy KR (2013) Effect of salinity-altering pulsing events on soil organic carbon loss along an intertidal wetland gradient: a laboratory experiment. Biogeochemistry 115:363–383CrossRefGoogle Scholar
  11. Chmura GL, Anisfeld SC, Cahoon DR, Lynch JC (2003) Global carbon sequestration in tidal, saline wetland soils. Global Biogeochem Cy 17:GB1111. doi: 10.1029/2002GB001917 CrossRefGoogle Scholar
  12. Conde E, Cardenas M, Ponce-Mendoza A, Luna-Guido ML, Cruz-Mondragόn C, Dendooven L (2005) The impacts of inorganic nitrogen application on mineralization of 14C-labelled maize and glucose, and on priming effect in saline alkaline soil. Soil Biol Biochem 37:681–691CrossRefGoogle Scholar
  13. Dendooven L, Alcántare-Hernández RJ, Valenzuela-Encinas C, Valenzuela-Encinas C, Luna-Guido M, Ferez-Guevara F, Marsh R (2010) Dynamics of carbon and nitrogen in an extreme alkaline saline soil: A review. Soil Biol Biochem 42:865–877CrossRefGoogle Scholar
  14. Denef K, Six J (2005) Clay mineralogy determines the importance of biological versus abiotic processes for macroaggregate formation and stabilization. Eur J Soil Sci 56:469–479CrossRefGoogle Scholar
  15. Denef K, Six J, Bossuyt H, Frey SD, Elliott ET, Merckx R, Paustian K (2001) Influence of dry-wet cycles on the interrelationship between aggregate, particulate organic matter, and microbial community dynamics. Soil Biol Biochem 33:1599–1611CrossRefGoogle Scholar
  16. Dijkstra FA, Cheng W, Johnson DW (2006) Plant biomass influences rhizosphere priming effects on soil organic matter decomposition in two differently managed soils. Soil Biol Biochem 38:2519–2526CrossRefGoogle Scholar
  17. Elgharably A, Marschner P (2011) Microbial activity and biomass and N and P availability in a saline sandy loam amended with inorganic N and lupin residues. Eur J Soil Biol 47:310–315CrossRefGoogle Scholar
  18. Engloner AI (2009) Structure, growth dynamics and biomass of reed (Phragmites australis) – A review. Flora 204:331–346CrossRefGoogle Scholar
  19. Euliss NH Jr, Gleason RA, Olness A, McDougal RL, Murkin HR, Robarts RD, Bourbonniere RA, Warner BG (2006) North American prairie wetlands are important nonforested land-based carbon storage sites. Sci Total Environ 361:179–188CrossRefPubMedGoogle Scholar
  20. FAO (2002) Key to the FAO soil units in the FAO/Unesco soil map of the world. Available at (verified 17 Nov. 2011). FAO, Rome
  21. Gao J, Lei G, Zhang X, Wang G (2014) Can δ13C abundance, water-soluble carbon, and light fraction carbon be potential indicators of soil organic carbon dynamics in Zoigê wetland? Catena 119:21–27CrossRefGoogle Scholar
  22. Ge T, Yuan H, Zhu H, Wu X, Nie S, Liu C, Tong C, Wu J, Brookes P (2012) Biological carbon assimilation and dynamics in a flooded rice-soil system. Soil Biol Biochem 48:39–46CrossRefGoogle Scholar
  23. Gonzalez JM, Laird DA (2003) Carbon sequestration in clay mineral fractions from C-14-labeled plant residues. Soil Sci Soc Am J 67:1715–1720CrossRefGoogle Scholar
  24. González-Alcaraz MN, Egea C, Jiménez-Cárceles FJ, Párraga I, María-Cervantes A, Delgado MJ, Álvarez-Rogel J (2012) Storage of organic carbon, nitrogen and phosphorus in the soil-plant system of Phragmites australis stands from a eutrophicated Mediterranean salt marsh. Geoderma 185–186:61–67CrossRefGoogle Scholar
  25. Gorai M, Ennajeh M, Khemira H, Neffati M (2010) Combined effect of NaCl-salinity and hypoxia on growth, photosynthesis, water relations and solute accumulation in Phragmites australis plants. Flora 205:462–470CrossRefGoogle Scholar
  26. Guan S, Dou S, Chen G, Wang G, Zhuang J (2015) Isotopic characterization of sequestration and transformation of plant residue carbon in relation to soil aggregation dynamics. Appl Soil Ecol 96:18–24CrossRefGoogle Scholar
  27. Han G, Yang L, Yu J, Wang G, Mao P, Gao Y (2013) Environmental controls on net ecosystem CO2 exchange over a Reed (Phragmites australis) wetland in the Yellow River Delta, China. Estuar Coasts 36:401–413CrossRefGoogle Scholar
  28. Hurry CR, James EA, Thompson RM (2013) Connectivity, genetic structure and stress response of Phragmites australis: Issues for restoration in a salinising wetland system. Aquat Bot 104:138–146CrossRefGoogle Scholar
  29. Inubushi K, Brookes PC, Jenkinson DS (1991) Soil microbial biomass C, N and ninhydrin-N in aerobic and anerobic soil measured by the fumigation-extraction method. Soil Biol Biochem 23:737–741CrossRefGoogle Scholar
  30. Jenkinson DS (1988) Determination of microbial biomass carbon and nitrogen in soil. In: Wilson JR (ed) Advances in nitrogen cycling in agricultural ecosystems. CAB International, Wallingford, UK, pp. 368–386Google Scholar
  31. Johnson D, Leake JR, Ostle N, Ineson P, Read DJ (2002) In situ 13CO2 pulse-labelling of upland grassland demonstrates a rapid pathway of carbon flux from arbuscular mycorrhizal mycelia to the soil. New Phytol 153:327–334CrossRefGoogle Scholar
  32. Kalbitz K, Schmerwitz J, Schwesig D, Matzner E (2003) Biodegradation of soil-derived dissolved organic matter as related to its properties. Geoderma 113:273–291CrossRefGoogle Scholar
  33. Kalbitz K, Solinger S, Park JH, Michalzik B, Matzner E (2000) Controls on the dynamics of dissolved organic matter in soils: a review. Soil Sci 165:277–304CrossRefGoogle Scholar
  34. Keiluweit M, Bougoure JJ, Nico PS, Pett-Ridge J, Weber PK, Kleber M (2015) Mineral protection of soil carbon counteracted by root exudates. Nat Clim Chang. doi: 10.1038/NCLIMATE2580 Google Scholar
  35. Kirwan ML, Mudd SM (2012) Responses of salt-marsh carbon accumulation to climate change. Nature 489:550–553CrossRefPubMedGoogle Scholar
  36. Kuzyakov Y, Blagodatskaya E (2015) Microbial hotspots and hot moments in soil: Concept & review. Soil Biol Biochem 83:184–199CrossRefGoogle Scholar
  37. Kuzyakov Y, Domanski G (2000) Carbon input by plants into the soil. Review J Plant Nutri Soil Sci 163:421–431CrossRefGoogle Scholar
  38. Kuzyakov Y, Gavrichkova O (2010) Time lag between photosynthesis and carbon dioxide efflux from soil: a review of mechanisms and controls. Glob Chang Biol 16:3386–3406CrossRefGoogle Scholar
  39. Kuzyakov Y, Kretzschmar A, Stahr K (1999) Contribution of Lolium perenne rhizodeposition to carbon turnover of pasture soil. Plant Soil 231:127–136CrossRefGoogle Scholar
  40. Lal R (2004) Soil carbon sequestration impacts on global climate change and food security. Science 304:1623–1627CrossRefPubMedGoogle Scholar
  41. Li J, Pu L, Zhu M, Zhang J, Li P, Dai X, Xu Y, Liu L (2014) Evolution of soil properties following reclamation in coastal areas: A review. Geoderma 226-227:130–139CrossRefGoogle Scholar
  42. Li XG, Shi XM, Wang DJ, Zhou W (2012) Effect of alkalized magnesic salinity on soil respiration changes with substrate availability and incubation time. Biol Fertil Soils 48:597–602CrossRefGoogle Scholar
  43. Liu G, Zhang L, Zhang Q, Musyimi Z, Jiang Q (2014) Spatio-temporal dynamics of wetland landscape patterns based on remote sensing in Yellow River Delta, China. Wetlands 34:787–801CrossRefGoogle Scholar
  44. Lou Y, Li Z, Zhang T, Liang Y (2004) CO2 emissions from subtropical arable soils of China. Soil Biol Biochem 36:1835–1842CrossRefGoogle Scholar
  45. Lu Q, Gao Z, Zhao Z, Ning J, Bi X (2014) Dynamics of wetlands and their effects on carbon emissions in China coastal region – Case study in Bohai Economic Rim. Ocean Coast Manag 87:61–67CrossRefGoogle Scholar
  46. Lu Y, Conrad R (2005) In situ stable isotope probing of methanogenic archaea in the rice rhizosphere. Science 309:1088CrossRefPubMedGoogle Scholar
  47. Lu Y, Watanabe A, Kimura M (2002) Input and distribution of photosynthesized carbon in a flooded rice soil. Global Biogeochem Cy 16:321–328CrossRefGoogle Scholar
  48. Lu Y, Watanabe A, Kimura M (2003) Carbon dynamics of rhizodeposits, root- and shoot-residues in a rice soil. Soil Biol Biochem 35:1223–1230CrossRefGoogle Scholar
  49. Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere. Plant Soil 129:1–10CrossRefGoogle Scholar
  50. Manchanda G, Garg N (2008) Salinity and its effects on the functional biology of legumes. Acta Physiol Plant 30:595–618CrossRefGoogle Scholar
  51. Martins MR, Angers DA, Corá JE (2012) Co-accumulation of microbial residues and particulate organic matter in the surface layer of a no-till Oxisol under different crops. Soil Biol Biochem 50:208–213CrossRefGoogle Scholar
  52. Mauchamp A, Blanch S, Grillas P (2001) Effects of submergence on the growth of Phragmites australis seedlings. Aquat Bot 69:147–164CrossRefGoogle Scholar
  53. Mavi MS, Marschner P, Chittleborough DJ, Cox JM, Sanderman J (2012) Salinitiy and sodicity affect soil respiration and dissolved organic matter dynamics differentially in soils varying in texture. Soil Biol Biochem 45:8–13CrossRefGoogle Scholar
  54. McNally SR, Laughlin DC, Rutledge S, Dodd MB, Six J, Schipper LA (2015) Root carbon inputs under moderately diverse sward and conventional ryegrass-clover pasture: implications for soil carbon sequestration. Plant Soil. doi: 10.1007/s11104-015-2463-z Google Scholar
  55. Meng F, Dungait JAJ, Zhang X, He M, Guo Y, Wu W (2013) Investigation of photosynthate-C allocation 27 days after 13C-pulse labeling of Zea mays L. at different growth stages. Plant Soil 373:755–764CrossRefGoogle Scholar
  56. Micwood AJ, Boutton TW (1998) Soil carbonate decomposition by acid had little effect on the δ13C or organic matter. Soil Biol Biochem 30:1301–1307CrossRefGoogle Scholar
  57. Morrissey E, Gillespie J, Morina J, Franklin RB (2014) Salinity affects microbial activity and soil organic matter content in tidal wetland. Glob Chang Biol 20:1351–1362CrossRefPubMedGoogle Scholar
  58. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681CrossRefPubMedGoogle Scholar
  59. Nicolás C, Kennedy JN, Hernández T, García C, Six J (2014) Soil aggregation in a semiarid soil amended with composted and non-composted sewage sludge-Afield experiment. Geodema 219–220:24–31CrossRefGoogle Scholar
  60. Pausch J, Tian J, Riederer M, Kuzyakov Y (2013) Estimation of rhizodeposition at field scale: upscaling of a 14C labeling study. Plant Soil 364:273–285CrossRefGoogle Scholar
  61. Qiu SJ, Ju XT, Ingwersen J, Qin ZC, Li L, Streck T, Christie P, Zhang FS (2010) Changes in soil carbon and nitrogen pools after shifting from conventional cereal to greenhouse vegetable production. Soil Tillage Res 107:80–87CrossRefGoogle Scholar
  62. Rangel-Castro JI, Prosser JI, Scrimgeour CM, Smith P, Ostle N, Ineson P, Meharg A, Killham K (2004) Carbon flow in an upland grassland: effect of liming on the flux of recently photosynthesized carbon to rhizosphere soil. Glob Chang Biol 10:2100–2108CrossRefGoogle Scholar
  63. Rennenberg H, Loreto F, Polle A, Brilli F, Fares S, Beniwal RS, Gessler A (2006) Physiological responses of forest trees to heat and drought. Plant Biol 8:556–571CrossRefPubMedGoogle Scholar
  64. Richert M, Saarnio S, Juutinen S, Silvola J, Augustin J, Merbach W (2000) Distribution of assimilated carbon in the system Phragmites australis-waterlogged peat soil after carbon-14 pulse labelling. Biol Fertil Soils 32:1–7CrossRefGoogle Scholar
  65. Saidy AR, Smernik RJ, Baldock JA, Kaiser K, Sanderman J, Macdonald LM (2012) Effects of clay mineralogy and hydrous iron oxides on labile organic carbon stabilization. Geoderma 173–174:104–110CrossRefGoogle Scholar
  66. Salvo L, Hernández J, Ernst O (2010) Distribution of soil organic carbon in different size fractions, under pasture and crop rotations with conventional tillage and no-till systems. Soil Tillage Res 109:116–122CrossRefGoogle Scholar
  67. Schmitt A, Pausch J, Kuzyakov Y (2013) C and N allocation in soil under ryegrass and alfalfa estimated by 13C and 15N labeling. Plant Soil 368:581–590CrossRefGoogle Scholar
  68. Six J, Conant RT, Paul EA, Paustian K (2002) Stabilization mechanisms of soil organic matter: Implications for C-saturation of soils. Plant Soil 241:155–176CrossRefGoogle Scholar
  69. Toosi ER, Doane TA, Horwath WR (2012) Abiotic solubilization of soil organic matter, a less-seen aspect of dissolved organic matter production. Soil Biol Biochem 50:12–21CrossRefGoogle Scholar
  70. Torn MS, Kleber M, Zavaleta ES, Zhu B, Field CB, Trumbore SE (2013) A dual isotope approach to isolate soil carbon pools of different turnover times. Biogeosciences 10:8067–8081CrossRefGoogle Scholar
  71. Wang S, Xu J, Zhou C (2002) Using remote sensing to estimate the change of carbon storage: a case study in the estuary of Yellow River Delta. Int J Remote Sens 23:1565–1580CrossRefGoogle Scholar
  72. Wang W, Liu J, Zhang B, Zhang J, Li X, Y Y (2015) Critical evaluation of particle size distribution models using soil data obtained with a laser diffraction method. Soil Sci 178: 194–204Google Scholar
  73. Wang ZY, Xin YZ, Gao DM, Li FM, Morgan J, Xing BS (2010) Microbial community characteristics in a degraded wetland of the Yellow River Delta. Pedosphere 20:466–478CrossRefGoogle Scholar
  74. Warembourg FR, Estelrich HD (2001) Plant phenology and soil fertility effects on below-ground carbon allocation for an annual (Bromus madritensis) and a perennial (Bromus erectus) grass species. Soil Biol Biochem 33:1291–1303CrossRefGoogle Scholar
  75. Wong VNL, Greene RSB, Dalal RC, Murphy BW (2010) Soil carbon dynamics in saline and sodic soils: a review. Soil Use Manag 26:2–11CrossRefGoogle Scholar
  76. Xiao C, Janssens I A,, Liu P, Zhou Z, Sun OJ (2007) Irrigation and enhanced soil carbon input effects on below-ground carbon cycling in semiarid temperate grasslands. New Phytol 174: 835–846CrossRefPubMedGoogle Scholar
  77. Yadav S, Irfan M, Ahmad A, Hayat S (2011) Causes of salinity and plant manifestations to salt stress: A review. J Environ Biol 32:667–685PubMedGoogle Scholar
  78. Zeller B, Dambrine E (2011) Coarse particulate organic matter is the primary source of mineral N in the topsoil of three beech forests. Soil Biol Biochem 43:542–550CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.National Engineering Laboratory for Improving Quality of Arable Land, Ministry of Agriculture Key Laboratory of Plant Nutrition and Fertilizers, Institute of Agricultural Resources and Regional PlanningChinese Academy of Agricultural SciencesBeijingChina
  2. 2.Shandong Key laboratory of Eco-Enviromental Science for Yellow River DeltaBinzhou UniversityBinzhou CityChina
  3. 3.Key Laboratory of Ecosystem Network Observation and Modelling, Institute of Geographic Sciences and Natural Resources ResearchChinese Academy of SciencesBeijingChina
  4. 4.Agri-Food and Biosciences InstituteBelfastUK

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