Nitrogen and phosphorus availability affect wheat carbon allocation pathways: rhizodeposition and mycorrhizal symbiosis
Bahareh Bicharanloo
A B , Milad Bagheri Shirvan A , Claudia Keitel A and Feike A. Dijkstra A
+ Author Affiliations
- Author Affiliations
A Sydney Institute of Agriculture, School of Life and Environmental Sciences, The University of Sydney, Camden, NSW 2570, Australia.
B Corresponding author: bahareh.bicharanloo@sydney.edu.au
Soil Research 58(2) 125-136 https://doi.org/10.1071/SR19183
Submitted: 9 July 2019 Accepted: 18 November 2019 Published: 4 December 2019
Abstract
Plants allocate their photosynthetic carbon (C) belowground through rhizodeposition, which can be incorporated into microbial biomass and organic matter, but can also be directly shared with arbuscular mycorrhizal fungi (AMF). In this study, we investigated how both rhizodeposition and AMF colonisation are affected by nitrogen (N) and phosphorus (P) availability in soil systems, and in turn, how these C allocation pathways influenced plant P uptake in four different wheat genotypes with variable root traits. Wheat genotypes (249, Suntop, Scout and IAW2013) were grown in pots and labelled continuously during their growth period with 13CO2 to determine rhizodeposition. We applied two levels of N (25 and 100 kg ha–1) and P (10 and 40 kg ha–1) fertiliser. Plant root traits, plant P content, soil available P and N, microbial biomass C and P, and AMF colonisation were examined. We constructed a structural equation model to show how C allocation to rhizodeposition and AMF colonisation depended on P and N availability, and how these pathways affected plant P uptake and grain yield. Wheat genotypes with fine roots (Suntop, Scout and IAW2013) were associated with AMF colonisation for plant P uptake, and the genotype with the largest root biomass (249) provided more C to rhizodeposition. Both rhizodeposition and AMF colonisation increased plant P and grain yield under low P and high N availability respectively, while root biomass and root traits, such as specific root length and proportion of fine roots, determined which C allocation pathway was employed by the plant.
Additional keywords: C allocation, 13C labelling, mycorrhizal colonisation, microbial biomass phosphorus, root traits, phosphorus uptake.
References
Aldén L, Demoling F, Bååth E (2001) Rapid method of determining factors limiting bacterial growth in soil. Applied and Environmental Microbiology 67, 1830–1838.| Rapid method of determining factors limiting bacterial growth in soil.Crossref | GoogleScholarGoogle Scholar | 11282640PubMed |
Bago B, Pfeffer P, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiology 124, 949–958.
| Carbon metabolism and transport in arbuscular mycorrhizas.Crossref | GoogleScholarGoogle Scholar | 11080273PubMed |
Bakhshandeh S, Corneo PE, Mariotte P, Kertesz MA, Dijkstra FA (2017) Effect of crop rotation on mycorrhizal colonization and wheat yield under different fertilizer treatments. Agriculture, Ecosystems & Environment 247, 130–136.
| Effect of crop rotation on mycorrhizal colonization and wheat yield under different fertilizer treatments.Crossref | GoogleScholarGoogle Scholar |
Bakhshandeh S, Corneo PE, Yin L, Dijkstra FA (2019) Drought and heat stress reduce yield and alter carbon rhizodeposition of different wheat genotypes. Journal Agronomy & Crop Science 205, 157–167.
| Drought and heat stress reduce yield and alter carbon rhizodeposition of different wheat genotypes.Crossref | GoogleScholarGoogle Scholar |
Baptist F, Aranjuelo I, Legay N, Lopez-Sangil L, Molero G, Rovira P, Nogués S (2015) Rhizodeposition of organic carbon by plants with contrasting traits for resource acquisition: responses to different fertility regimes. Plant and Soil 394, 391–406.
| Rhizodeposition of organic carbon by plants with contrasting traits for resource acquisition: responses to different fertility regimes.Crossref | GoogleScholarGoogle Scholar |
Bécard G, Piché Y (1989) Fungal growth stimulation by CO2 and root exudates in vesicular-arbuscular mycorrhizal symbiosis. Applied and Environmental Microbiology 55, 2320–2325.
Beck T, Joergensen RG, Kandeler E, Makeschin F, Nuss E, Oberholzer HR, Scheu S (1997) An inter-laboratory comparison of ten different ways of measuring soil microbial biomass C. Soil Biology & Biochemistry 29, 1023–1032.
| An inter-laboratory comparison of ten different ways of measuring soil microbial biomass C.Crossref | GoogleScholarGoogle Scholar |
Bonfante P, Anca IA (2009) Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annual Review of Microbiology 63, 363–383.
| Plants, mycorrhizal fungi, and bacteria: a network of interactions.Crossref | GoogleScholarGoogle Scholar | 19514845PubMed |
Bowsher AW, Evans S, Tiemann LK, Friesen ML (2018) Effects of soil nitrogen availability on rhizodeposition in plants: a review. Plant and Soil 423, 59–85.
| Effects of soil nitrogen availability on rhizodeposition in plants: a review.Crossref | GoogleScholarGoogle Scholar |
Brookes PC, Powlson DS, Jenkinson DS (1982) Measurement of microbial biomass phosphorus in soil. Soil Biology & Biochemistry 14, 319–329.
| Measurement of microbial biomass phosphorus in soil.Crossref | GoogleScholarGoogle Scholar |
Bureau of Meteorology (2018) Climate data online. Available at http://www.bom.gov.au/climate/data [verified 6 September 2018].
Chowdhury S, Farrell M, Bolan N (2014) Photoassimilated carbon allocation in a wheat plant-soil system as affected by soil fertility and land-use history. Plant and Soil 383, 173–189.
| Photoassimilated carbon allocation in a wheat plant-soil system as affected by soil fertility and land-use history.Crossref | GoogleScholarGoogle Scholar |
Cieslinski G, Van Rees KCJ, Szmigielska AM, Huang PM (1997) Low molecular weight organic acids released from roots of durum wheat and flax into sterile nutrient solutions. Journal of Plant Nutrition 20, 753–764.
| Low molecular weight organic acids released from roots of durum wheat and flax into sterile nutrient solutions.Crossref | GoogleScholarGoogle Scholar |
Corneo PE, Suenaga H, Kertesz MA, Dijkstra FA (2016) Effect of twenty four wheat genotypes on soil biochemical and microbial properties. Plant and Soil 404, 141–155.
| Effect of twenty four wheat genotypes on soil biochemical and microbial properties.Crossref | GoogleScholarGoogle Scholar |
Corneo PE, Keitel C, Kertesz MA, Dijkstra FA (2017) Variation in specific root length among 23 wheat genotypes affects leaf δ13C and yield. Agriculture, Ecosystems & Environment 246, 21–29.
| Variation in specific root length among 23 wheat genotypes affects leaf δ13C and yield.Crossref | GoogleScholarGoogle Scholar |
Dijkstra FA, Cheng W (2007) Interactions between soil and tree roots accelerate long-term soil carbon decomposition. Ecology Letters 10, 1046–1053.
| Interactions between soil and tree roots accelerate long-term soil carbon decomposition.Crossref | GoogleScholarGoogle Scholar | 17910623PubMed |
Fioreze SL, Castoldi G, Pivetta LA, Pivetta LG, Fernandes DM, Büll LT (2012) Tillering of two wheat genotypes as affected by phosphorus levels. Acta Scientiarum. Agronomy 34, 331–338.
| Tillering of two wheat genotypes as affected by phosphorus levels.Crossref | GoogleScholarGoogle Scholar |
Grace JB, Anderson TM, Olff H, Scheiner SM (2010) On the specification of structural equation models for ecological systems. Ecological Monographs 80, 67–87.
| On the specification of structural equation models for ecological systems.Crossref | GoogleScholarGoogle Scholar |
Gregory PJ, Palta JA, Batts GR (1995) Root systems and root:mass ratio-carbon allocation under current and projected atmospheric conditions in arable crops. Plant and Soil 187, 221–228.
| Root systems and root:mass ratio-carbon allocation under current and projected atmospheric conditions in arable crops.Crossref | GoogleScholarGoogle Scholar |
Haghighi M, Mohmmadnia S, Pessarakli M (2016) Effects of mycorrhiza colonization on growth, root exudates, antioxidant activity and photosynthesis trait of cucumber grown in Johnson modified nutrient solution. Journal of Plant Nutrition 39, 2079–2091.
| Effects of mycorrhiza colonization on growth, root exudates, antioxidant activity and photosynthesis trait of cucumber grown in Johnson modified nutrient solution.Crossref | GoogleScholarGoogle Scholar |
Henry F, Nguyen C, Paterson E, Sim A, Robin C (2005) How does nitrogen availability alter rhizodeposition in Lolium multiflorum Lam. during vegetative growth? Plant and Soil 269, 181–191.
| How does nitrogen availability alter rhizodeposition in Lolium multiflorum Lam. during vegetative growth?Crossref | GoogleScholarGoogle Scholar |
Heuck C, Weig A, Spohn M (2015) Soil microbial biomass C:N:P stoichiometry and microbial use of organic phosphorus. Soil Biology and Biochemistry 85, 119–129.
| Soil microbial biomass C:N:P stoichiometry and microbial use of organic phosphorus.Crossref | GoogleScholarGoogle Scholar |
Hodge A, Storer K (2015) Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. Plant and Soil 386, 1–19.
| Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems.Crossref | GoogleScholarGoogle Scholar |
Hunter PJ, Teakle GR, Bending GD (2014) Root traits and microbial community interactions in relation to phosphorus availability and acquisition, with particular reference to Brassica. Frontiers in Plant Science 5, 1–18.
| Root traits and microbial community interactions in relation to phosphorus availability and acquisition, with particular reference to Brassica.Crossref | GoogleScholarGoogle Scholar |
IPCC (2013) Climate change 2013: The physical science basis. 1535 (Cambridge University Press: Cambridge, UK and New York, NY, USA). Available at https://www.ipcc.ch/report/ar5/wg1/ [verified 21 November 2019].
Isbell R (2002) ‘The Australian soil classification.’ (CSIRO Publishing: Melbourne,Vic., Australia).
Jackson ML (1958) ‘Soil chemical analysis.’ (Verlag, Prentice Hall Inc.: Englewood Cliffs, NJ, USA)
Johnson NC, Wilson GWT, Wilson JA, Miller RM, Bowker MA (2015) Mycorrhizal phenotypes and the Law of the Minimum. New Phytologist 205, 1473–1484.
| Mycorrhizal phenotypes and the Law of the Minimum.Crossref | GoogleScholarGoogle Scholar | 25417818PubMed |
Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytologist 163, 459–480.
| Plant and mycorrhizal regulation of rhizodeposition.Crossref | GoogleScholarGoogle Scholar |
Jungk A (2001) Root hairs and the acquisition of plant nutrients from soil. Journal of Plant Nutrition and Soil Science 164, 121–129.
| Root hairs and the acquisition of plant nutrients from soil.Crossref | GoogleScholarGoogle Scholar |
Kaiser C, Kilburn MR, Clode PL, Fuchslueger L, Koranda M, Cliff JB, Solaiman ZM, Murphy DV (2015) Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway vs direct root exudation. New Phytologist 205, 1537–1551.
| Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway vs direct root exudation.Crossref | GoogleScholarGoogle Scholar | 25382456PubMed |
Konvalinková T, Püschel D, Řezáčová V, Gryndlerová H, Jansa J (2017) Carbon flow from plant to arbuscular mycorrhizal fungi is reduced under phosphorus fertilization. Plant and Soil 419, 319–333.
| Carbon flow from plant to arbuscular mycorrhizal fungi is reduced under phosphorus fertilization.Crossref | GoogleScholarGoogle Scholar |
Kuzyakov Y, Domanski G (2000) Carbon input by plants into the soil. Journal of Plant Nutrition and Soil Science 163, 421–431.
| Carbon input by plants into the soil.Crossref | GoogleScholarGoogle Scholar |
Land S, von Alten H, Schönbeck F (1993) The influence of host plant, nitrogen fertilization and fungicide application on the abundance and seasonal dynamics of vesicular-arbuscular mycorrhizal fungi in arable soils of northern Germany. Mycorrhiza 2, 157–166.
| The influence of host plant, nitrogen fertilization and fungicide application on the abundance and seasonal dynamics of vesicular-arbuscular mycorrhizal fungi in arable soils of northern Germany.Crossref | GoogleScholarGoogle Scholar |
Lazarević B, Lošák T, Manschadi AM (2018) Arbuscular mycorrhizae modify winter wheat root morphology and alleviate phosphorus deficit stress. Plant, Soil and Environment 64, 47–52.
| Arbuscular mycorrhizae modify winter wheat root morphology and alleviate phosphorus deficit stress.Crossref | GoogleScholarGoogle Scholar |
Liu W (2009) Correlation between specific fine root length and mycorrhizal colonization of maize in different soil types. Frontiers of Agriculture in China 3, 13–15.
| Correlation between specific fine root length and mycorrhizal colonization of maize in different soil types.Crossref | GoogleScholarGoogle Scholar |
Maherali H (2014) Is there an association between root architecture and mycorrhizal growth response? New Phytologist 204, 192–200.
| Is there an association between root architecture and mycorrhizal growth response?Crossref | GoogleScholarGoogle Scholar | 25041241PubMed |
McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular arbuscular mycorrhizal fungi. New Phytologist 115, 495–501.
| A new method which gives an objective measure of colonization of roots by vesicular arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |
Melino V, Fiene G, Enju A, Cai J, Buchner P, Heuer S (2015) Genetic diversity for root plasticity and nitrogen uptake in wheat seedlings. Functional Plant Biology 42, 942–956.
| Genetic diversity for root plasticity and nitrogen uptake in wheat seedlings.Crossref | GoogleScholarGoogle Scholar |
Milcu A, Allan E, Roscher C, Jenkins T, Meyer ST, Flynn D, Bessler H, Buscot F, Engels C, Gubsch M, Konig S, Lipowsky A, Loranger J, Renker C, Scherber C, Schmid B, Thebault E, Wubet T, Weisser WW, Scheu S, Eisenhauer N (2013) Functionally and phylogenetically diverse plant communities key to soil biota. Ecology 94, 1878–1885.
| Functionally and phylogenetically diverse plant communities key to soil biota.Crossref | GoogleScholarGoogle Scholar | 24015531PubMed |
Nahar K (2017) Understanding the contribution of root traits for phosphorus responsiveness of wheat. PhD Thesis, University of Adelaide. https://digital.library.adelaide.edu.au/dspace/bitstream/2440/109805/2/02whole.pdf
Nguyen C (2009) Rhizodeposition of organic C by plant: mechanisms and controls. In ‘Sustainable agriculture’. (Eds E Lichtfouse, M Navarrete, P Debaeke, S Véronique, C Alberola) pp. 97–123. (Springer: Dordrecht, Netherlands)
Pausch J, Kuzyakov Y (2018) Carbon input by roots into the soil: quantification of rhizodeposition from root to ecosystem scale. Global Change Biology 24, 1–12.
| Carbon input by roots into the soil: quantification of rhizodeposition from root to ecosystem scale.Crossref | GoogleScholarGoogle Scholar | 28752603PubMed |
Pearson JN, Jakobsen I (1993) Symbiotic exchange of carbon and phosphorus between cucumber and three arbuscular mycorrhizal fungi. New Phytologist 124, 481–488.
| Symbiotic exchange of carbon and phosphorus between cucumber and three arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |
Pendall E, Mosier AR, Morgan JA (2004) Rhizodeposition stimulated by elevated CO2 in a semiarid grassland. New Phytologist 162, 447–458.
| Rhizodeposition stimulated by elevated CO2 in a semiarid grassland.Crossref | GoogleScholarGoogle Scholar |
Püschel D, Janoušková M, Hujslová M, Slavíková R, Gryndlerová H, Jansa J (2016) Plant–fungus competition for nitrogen erases mycorrhizal growth benefits of Andropogon gerardii under limited nitrogen supply. Ecology and Evolution 6, 4332–4346.
| Plant–fungus competition for nitrogen erases mycorrhizal growth benefits of Andropogon gerardii under limited nitrogen supply.Crossref | GoogleScholarGoogle Scholar | 27386079PubMed |
Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiology 156, 989–996.
| Soil microorganisms mediating phosphorus availability update on microbial phosphorus.Crossref | GoogleScholarGoogle Scholar | 21606316PubMed |
Rodríguez D, Andrade FH, Goudriaan J (1999) Effects of phosphorus nutrition on tiller emergence in wheat. Plant and Soil 209, 283–295.
| Effects of phosphorus nutrition on tiller emergence in wheat.Crossref | GoogleScholarGoogle Scholar |
Rosseel Y (2012) lavaan: An R package for structural equation modeling. Journal of Statistical Software 48, 1–36.
| lavaan: An R package for structural equation modeling.Crossref | GoogleScholarGoogle Scholar |
Ryan MH, van Herwaarden AF, Angus JF, Kirkegaard JA (2005) Reduced growth of autumn-sown wheat in a low-P soil is associated with high colonisation by arbuscular mycorrhizal fungi. Plant and Soil 270, 275–286.
| Reduced growth of autumn-sown wheat in a low-P soil is associated with high colonisation by arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |
Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Journal of Plant Physiology 116, 447–453.
| Phosphorus uptake by plants: from soil to cell.Crossref | GoogleScholarGoogle Scholar |
Schenck zu Schweinsberg-Mickan M, Jörgensen RG, Müller T (2012) Rhizodeposition: its contribution to microbial growth and carbon and nitrogen turnover within the rhizosphere. Journal of Plant Nutrition and Soil Science 175, 750–760.
| Rhizodeposition: its contribution to microbial growth and carbon and nitrogen turnover within the rhizosphere.Crossref | GoogleScholarGoogle Scholar |
Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycological Research 105, 1413–1421.
| A new fungal phylum, the Glomeromycota: phylogeny and evolution.Crossref | GoogleScholarGoogle Scholar |
Smith SE, Manjarrez M, Stonor R, McNeill A, Smith FA (2015) Indigenous arbuscular mycorrhizal (AM) fungi contribute to wheat phosphate uptake in a semi-arid field environment, shown by tracking with radioactive phosphorus. Applied Soil Ecology 96, 68–74.
| Indigenous arbuscular mycorrhizal (AM) fungi contribute to wheat phosphate uptake in a semi-arid field environment, shown by tracking with radioactive phosphorus.Crossref | GoogleScholarGoogle Scholar |
Spohn M, Kuzyakov Y (2013) Phosphorus mineralization can be driven by microbial need for carbon. Soil Biology & Biochemistry 61, 69–75.
| Phosphorus mineralization can be driven by microbial need for carbon.Crossref | GoogleScholarGoogle Scholar |
Spohn M, Ermak A, Kuzyakov Y (2013) Microbial gross organic phosphorus mineralization can be stimulated by root exudates – A 33P isotopic dilution study. Soil Biology & Biochemistry 65, 254–263.
| Microbial gross organic phosphorus mineralization can be stimulated by root exudates – A 33P isotopic dilution study.Crossref | GoogleScholarGoogle Scholar |
Stewart JWB, Tiessen H (1987) Dynamics of soil organic phosphorus. Biogeochemistry 4, 41–60.
| Dynamics of soil organic phosphorus.Crossref | GoogleScholarGoogle Scholar |
Sun Z, Chen Q, Han X, Bol R, Qu B, Meng F (2018) Allocation of photosynthesized carbon in an intensively farmed winter wheat–soil system as revealed by 14CO2 pulse labelling. Scientific Reports 8, 3160
| Allocation of photosynthesized carbon in an intensively farmed winter wheat–soil system as revealed by 14CO2 pulse labelling.Crossref | GoogleScholarGoogle Scholar | 29453440PubMed |
Suri VK, Choudhary AK, Chander G, Verma TS (2011) Influence of vesicular arbuscular mycorrhizal fungi and applied phosphorus on root colonization in wheat and plant nutrient dynamics in a phosphorus-deficient acid Alfisol of Western Himalayas. Communications in Soil Science and Plant Analysis 42, 1177–1186.
| Influence of vesicular arbuscular mycorrhizal fungi and applied phosphorus on root colonization in wheat and plant nutrient dynamics in a phosphorus-deficient acid Alfisol of Western Himalayas.Crossref | GoogleScholarGoogle Scholar |
Toljander JF, Lindahl BD, Paul LR, Elfstrand M, Finlay RD (2007) Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial growth and community structure. FEMS Microbiology Ecology 61, 295–304.
| Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial growth and community structure.Crossref | GoogleScholarGoogle Scholar | 17535297PubMed |
Treseder KK (2013) The extent of mycorrhizal colonization of roots and its influence on plant growth and phosphorus content. Plant and Soil 371, 1–13.
| The extent of mycorrhizal colonization of roots and its influence on plant growth and phosphorus content.Crossref | GoogleScholarGoogle Scholar |
Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biology & Biochemistry 19, 703–707.
| An extraction method for measuring soil microbial biomass C.Crossref | GoogleScholarGoogle Scholar |
Vierheilig H, Coughlan AP, Wyss U, Piche Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Applied and Environmental Microbiology 64, 5004–5007.
Viscarra Rossel RA, Bui EN (2016) A new detailed map of total phosphorus stocks in Australian soil. The Science of the Total Environment 542, 1040–1049.
| A new detailed map of total phosphorus stocks in Australian soil.Crossref | GoogleScholarGoogle Scholar | 26520615PubMed |
Waters MT, Gutjahr C, Bennett T, Nelson DC (2017) Strigolactone signaling and evolution. Annual Review of Plant Biology 68, 291–322.
| Strigolactone signaling and evolution.Crossref | GoogleScholarGoogle Scholar | 28125281PubMed |
Welc M, Ravnskov S, Kieliszewska-Rokicka B, Larsen J (2010) Suppression of other soil microorganisms by mycelium of arbuscular mycorrhizal fungi in root-free soil. Soil Biology & Biochemistry 42, 1534–1540.
| Suppression of other soil microorganisms by mycelium of arbuscular mycorrhizal fungi in root-free soil.Crossref | GoogleScholarGoogle Scholar |
Zhang L, Xu M, Liu Y, Zhang F, Hodge A, Feng G (2016) Carbon and phosphorus exchange may enable cooperation between an arbuscular mycorrhizal fungus and a phosphate-solubilizing bacterium. New Phytologist 210, 1022–1032.
| Carbon and phosphorus exchange may enable cooperation between an arbuscular mycorrhizal fungus and a phosphate-solubilizing bacterium.Crossref | GoogleScholarGoogle Scholar | 27074400PubMed |
Zhu J, Zhang C, Lynch JP (2010) The utility of phenotypic plasticity of root hair length for phosphorus acquisition. Functional Plant Biology 37, 313–322.
| The utility of phenotypic plasticity of root hair length for phosphorus acquisition.Crossref | GoogleScholarGoogle Scholar |
