Abstract
Aims
Plant P acquisition strategies are driven by multiple belowground morphological and physiological traits as well as interactions among these traits. This study aimed to characterize the relationships among traits involved in P acquisition to explore tradeoffs and the main P-acquisition strategies and their mediation by soil type.
Methods
Ten morphological and physiological traits involved in P acquisition were measured across 13 species grown in controlled conditions in two contrasting soils with moderate P limitation.
Results
Tradeoffs between thicker and thinner roots were observed, with thicker roots exhibiting greater carboxylate release or phosphatase activity in the rhizosheath. Tradeoffs and coordination amongst traits were strongly mediated by soil type. Multivariate analysis of functional traits involved in P acquisition highlighted four main P-acquisition strategies relying primarily on morphological traits, physiological traits or a combination thereof.
Conclusions
The diversity of strategies demonstrates a potential for functional diversity benefits in cultivated plant communities via preferential access to different P pools leading to complementarities and reduced competition for resource acquisition. Overall, our results underpin functionally-complementary multispecies crop designs, enhancing P availability and cycling efficiency.
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Abbreviations
- ΔpH:
-
Change in rhizosheath pH
- PME:
-
Phosphomonoesterase activity
- RLD:
-
Root length density
- SLA:
-
Specific leaf area
- SRL:
-
Specific root length
References
Bouwman AF, Beusen AHW, Lassaletta L et al (2017) Lessons from temporal and spatial patterns in global use of N and P fertilizer on cropland. Sci Rep 7:40366. https://doi.org/10.1038/srep40366
Campos P, Borie F, Cornejo P, et al (2018) Phosphorus Acquisition Efficiency Related to Root Traits: Is Mycorrhizal Symbiosis a Key Factor to Wheat and Barley Cropping? Front Plant Sci 9:752. https://doi.org/10.3389/fpls.2018.00752
Cawthray GR (2003) An improved reversed-phase liquid chromatographic method for the analysis of low-molecular mass organic acids in plant root exudates. J Chromatogr A 1011:233–240. https://doi.org/10.1016/S0021-9673(03)01129-4
Clarholm M, Skyllberg U, Rosling A (2015) Organic acid induced release of nutrients from metal-stabilized soil organic matter – The unbutton model. Soil Biol Biochem 84:168–176. https://doi.org/10.1016/j.soilbio.2015.02.019
Damon PM, Bowden B, Rose T, Rengel Z (2014) Crop residue contributions to phosphorus pools in agricultural soils: A review. Soil Biol Biochem 74:127–137. https://doi.org/10.1016/j.soilbio.2014.03.003
Dube E, Chiduza C, Muchaonyerwa P (2014) High biomass yielding winter cover crops can improve phosphorus availability in soil. South Afr J Sci 110:1–4. https://doi.org/10.1590/sajs.2014/20130135
Duputel M, Van Hoye F, Toucet J, Gérard F (2013) Citrate adsorption can decrease soluble phosphate concentration in soil: Experimental and modeling evidence. Appl Geochem 39:85–92. https://doi.org/10.1016/j.apgeochem.2013.09.017
FAO (2014) World reference base for soil resources 2014: international soil classification system for naming soils and creating legends for soil maps. FAO, Rome
Faucon M-P, Houben D, Lambers H (2017) Plant Functional Traits: Soil and Ecosystem Services. Trends Plant Sci 22:385–394. https://doi.org/10.1016/j.tplants.2017.01.005
García-Albacete M, Martín A, Cartagena MC (2012) Fractionation of phosphorus biowastes: Characterisation and environmental risk. Waste Manag 32:1061–1068. https://doi.org/10.1016/j.wasman.2012.02.003
Giles CD, George TS, Brown LK et al (2017) Does the combination of citrate and phytase exudation in Nicotiana tabacum promote the acquisition of endogenous soil organic phosphorus? Plant Soil 412:43–59. https://doi.org/10.1007/s11104-016-2884-3
Haling RE, Brown LK, Bengough AG, et al (2013) Root hairs improve root penetration, root–soil contact, and phosphorus acquisition in soils of different strength. Journal of Experimental Botany 64:3711–3721. https://doi.org/10.1093/jxb/ert200
Haling RE, Brown LK, Stefanski A et al (2018) Differences in nutrient foraging among Trifolium subterraneum cultivars deliver improved P-acquisition efficiency. Plant Soil 424:539–554. https://doi.org/10.1007/s11104-017-3511-7
Hallama M, Pekrun C, Lambers H, Kandeler E (2019) Hidden miners – the roles of cover crops and soil microorganisms in phosphorus cycling through agroecosystems. Plant Soil 434:7–45. https://doi.org/10.1007/s11104-018-3810-7
Hoffland E, Findenegg GR, Nelemans JA (1989) Solubilization of rock phosphate by rape. Plant Soil 113:161–165
Huang X, Su J, Li S et al (2019) Functional diversity drives ecosystem multifunctionality in a Pinus yunnanensis natural secondary forest. Sci Rep 9:6979. https://doi.org/10.1038/s41598-019-43475-1
Jones DL, Dennis PG, Owen AG, van Hees PAW (2003) Organic acid behavior in soils – misconceptions and knowledge gaps. Plant Soil 248:31–41. https://doi.org/10.1023/A:1022304332313
Kong D, Wang J, Wu H et al (2019) Nonlinearity of root trait relationships and the root economics spectrum. Nat Commun 10:2203. https://doi.org/10.1038/s41467-019-10245-6
Lambers H, Shane MW, Cramer MD et al (2006) Root Structure and Functioning for Efficient Acquisition of Phosphorus: Matching Morphological and Physiological Traits. Ann Bot 98:693–713. https://doi.org/10.1093/aob/mcl114
Lambers H, Hayes PE, Laliberté E et al (2015) Leaf manganese accumulation and phosphorus-acquisition efficiency. Trends Plant Sci 20:83–90. https://doi.org/10.1016/j.tplants.2014.10.007
Lange B, Pourret O, Meerts P et al (2016) Copper and cobalt mobility in soil and accumulation in a metallophyte as influenced by experimental manipulation of soil chemical factors. Chemosphere 146:75–84. https://doi.org/10.1016/j.chemosphere.2015.11.105
Lê S, Josse J, Husson F (2008) FactoMineR: An R Package for Multivariate Analysis. J Stat Softw 25. https://doi.org/10.18637/jss.v025.i01
Li L, Tilman D, Lambers H, Zhang F-S (2014) Plant diversity and overyielding: insights from belowground facilitation of intercropping in agriculture. New Phytol 203:63–69. https://doi.org/10.1111/nph.12778
Li H, Liu B, McCormack ML et al (2017) Diverse belowground resource strategies underlie plant species coexistence and spatial distribution in three grasslands along a precipitation gradient. New Phytol 216:1140–1150. https://doi.org/10.1111/nph.14710
Lynch JP (2015) Root phenes that reduce the metabolic costs of soil exploration: opportunities for 21st century agriculture: New roots for agriculture. Plant Cell Environ 38:1775–1784. https://doi.org/10.1111/pce.12451
Lyu Y, Tang H, Li H et al (2016) Major Crop Species Show Differential Balance between Root Morphological and Physiological Responses to Variable Phosphorus Supply. Front Plant Sci 7:15. https://doi.org/10.3389/fpls.2016.01939
Ma Z, Guo D, Xu X et al (2018) Evolutionary history resolves global organization of root functional traits. Nature 555:94–97. https://doi.org/10.1038/nature25783
Maltais-Landry G, Scow K, Brennan E (2014) Soil phosphorus mobilization in the rhizosphere of cover crops has little effect on phosphorus cycling in California agricultural soils. Soil Biol Biochem 78:255–262. https://doi.org/10.1016/j.soilbio.2014.08.013
Maltais-Landry G (2015) Legumes have a greater effect on rhizosphere properties (pH, organic acids and enzyme activity) but a smaller impact on soil P compared to other cover crops. Plant Soil 394:139–154. https://doi.org/10.1007/s11104-015-2518-1
Menezes-Blackburn D, Giles C, Darch T et al (2018) Opportunities for mobilizing recalcitrant phosphorus from agricultural soils: a review. Plant Soil 427:5–16. https://doi.org/10.1007/s11104-017-3362-2
Nobile C, Houben D, Michel E et al (2019) Phosphorus-acquisition strategies of canola, wheat and barley in soil amended with sewage sludges. Sci Rep 9:14878. https://doi.org/10.1038/s41598-019-51204
Nuruzzaman M, Lambers H, Bolland MD, Veneklaas EJ (2005) Phosphorus benefits of different legume crops to subsequent wheat grown in different soils of Western Australia. Plant Soil 271:175–187. https://doi.org/10.1007/s11104-004-2386-6
Olsen SR (1954) Estimation of Available Phosphorus in Soils by Extraction with Sodium Bicarbonate. U.S. Department of Agriculture
Pang J, Ryan MH, Tibbett M et al (2010) Variation in morphological and physiological parameters in herbaceous perennial legumes in response to phosphorus supply. Plant Soil 331:241–255. https://doi.org/10.1007/s11104-009-0249-x
Pang J, Bansal R, Zhao H et al (2018) The carboxylate-releasing phosphorus-mobilizing strategy can be proxied by foliar manganese concentration in a large set of chickpea germplasm under low phosphorus supply. New Phytol 219:518–529. https://doi.org/10.1111/nph.15200
Pearse SJ, Veneklaas EJ, Cawthray GR et al (2006) Carboxylate release of wheat, canola and 11 grain legume species as affected by phosphorus status. Plant Soil 288:127–139
Petchey OL, Gaston KJ (2006) Functional diversity: back to basics and looking forward. Ecol Lett 9:741–758. https://doi.org/10.1111/j.1461-0248.2006.00924.x
Raven JA, Lambers H, Smith SE, Westoby M (2018) Costs of acquiring phosphorus by vascular land plants: patterns and implications for plant coexistence. New Phytol 217:1420–1427. https://doi.org/10.1111/nph.14967
Richardson AE, Lynch JP, Ryan PR et al (2011) Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant Soil 349:121–156. https://doi.org/10.1007/s11104-011-0950-4
Rose TJ, Hardiputra B, Rengel Z (2010) Wheat, canola and grain legume access to soil phosphorus fractions differs in soils with contrasting phosphorus dynamics. Plant Soil 326:159–170. https://doi.org/10.1007/s11104-009-9990-4
Roumet C, Birouste M, Picon-Cochard C et al (2016) Root structure-function relationships in 74 species: evidence of a root economics spectrum related to carbon economy. New Phytol 210:815–826. https://doi.org/10.1111/nph.13828
Sanchez G (2013) PLS path modeling with R. Berkeley Trowchez Ed 383:2013
Sgrò CM, Hoffmann AA (2004) Genetic correlations, tradeoffs and environmental variation. Heredity 93:241–248. https://doi.org/10.1038/sj.hdy.6800532
Shen J, Yuan L, Zhang J et al (2011) Phosphorus Dynamics: From Soil to Plant. Plant Physiol 156:997–1005. https://doi.org/10.1104/pp.111.175232
Simpson RJ, Oberson A, Culvenor RA et al (2011) Strategies and agronomic interventions to improve the phosphorus-use efficiency of farming systems. Plant Soil 349:89–120. https://doi.org/10.1007/s11104-011-0880-1
Smith SE, Smith FA (2011) Roles of Arbuscular Mycorrhizas in Plant Nutrition and Growth: New Paradigms from Cellular to Ecosystem Scales. Annu Rev Plant Biol 62:227–250. https://doi.org/10.1146/annurev-arplant-042110-103846
Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307. https://doi.org/10.1016/0038-0717(69)90012-1
Teng W, Deng Y, Chen X-P et al (2013) Characterization of root response to phosphorus supply from morphology to gene analysis in field-grown wheat. J Exp Bot 64:1403–1411. https://doi.org/10.1093/jxb/ert023
Wang Y, Lambers H (2019) Root-released organic anions in response to low phosphorus availability: recent progress, challenges and future perspectives. Plant Soil 1–22. https://doi.org/10.1007/s11104-019-03972-8
Weemstra M, Mommer L, Visser EJW et al (2016) Towards a multidimensional root trait framework: a tree root review. New Phytol 211:1159–1169. https://doi.org/10.1111/nph.14003
Wen Z, Li H, Shen J, Rengel Z (2017) Maize responds to low shoot P concentration by altering root morphology rather than increasing root exudation. Plant Soil 416:377–389. https://doi.org/10.1007/s11104-017-3214-0
Wen Z, Li H, Shen Q et al (2019) Tradeoffs among root morphology, exudation and mycorrhizal symbioses for phosphorus-acquisition strategies of 16 crop species. New Phytol 223:882–895. https://doi.org/10.1111/nph.15833
Wendling M, Büchi L, Amossé C et al (2016) Influence of root and leaf traits on the uptake of nutrients in cover crops. Plant Soil 409:419–434. https://doi.org/10.1007/s11104-016-2974-2
Xue Y, Xia H, Christie P et al (2016) Crop acquisition of phosphorus, iron and zinc from soil in cereal/legume intercropping systems: a critical review. Ann Bot 117:363–377. https://doi.org/10.1093/aob/mcv182
Yacoumas A, Honvault N, Houben D et al (2020) Contrasting Response of Nutrient Acquisition Traits in Wheat Grown on Bisphenol A-Contaminated Soils. Water Air Soil Pollut 231:23. https://doi.org/10.1007/s11270-019-4383-7
Yu R-P, Zhang W-P, Yu Y-C et al (2020) Linking shifts in species composition induced by grazing with root traits for phosphorus acquisition in a typical steppe in Inner Mongolia. Sci Total Environ 712:136495. https://doi.org/10.1016/j.scitotenv.2020.136495
Yuan HM, Blackwell M, Mcgrath S et al (2016) Morphological responses of wheat (Triticum aestivum L.) roots to phosphorus supply in two contrasting soils. J Agric Sci 154:98–108. https://doi.org/10.1017/S0021859615000702
Zhang D, Zhang C, Tang X et al (2016) Increased soil phosphorus availability induced by faba bean root exudation stimulates root growth and phosphorus uptake in neighbouring maize. New Phytol 209:823–831. https://doi.org/10.1111/nph.13613
Zhou M, Bai W, Zhang Y, Zhang W-H (2018) Multi-dimensional patterns of variation in root traits among coexisting herbaceous species in temperate steppes. J Ecol 106:2320–2331. https://doi.org/10.1111/1365-2745.12977
Acknowledgements
The authors thank Vivescia for their financial and technical assistance. We also thank Aurore Coutelier, Matthieu Forster, Philippe Jacolot, Céline Roisin and Erika Samain for their technical assistance. The project received funding from the ANRT (Association Nationale Recherche Technologie).
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Nicolas Honvault carried out the experiment and wrote the manuscript with support from Michel-Pierre Faucon, David Houben and Hans Lambers. Stéphane Firmin and Cécile Nobile helped process the data and perform the analyses. All authors contributed to the final version of the manuscript.
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Honvault, N., Houben, D., Nobile, C. et al. Tradeoffs among phosphorus-acquisition root traits of crop species for agroecological intensification. Plant Soil 461, 137–150 (2021). https://doi.org/10.1007/s11104-020-04584-3
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DOI: https://doi.org/10.1007/s11104-020-04584-3