Abstract
Aims
Plant growth is often limited by low soil phosphorus (P) availability, soil nitrogen (N) availability may affect plants’ responses to P supply. We studied the growth and physiological responses of alfalfa to soil P supply at different N levels.
Methods
Alfalfa (Medicago sativa L.) plants were grown in an alkaline soil supplied with different levels of P (0, 5, and 20 mg kg−1) as monopotassium phosphate, and N (50 and 100 mg kg−1) as ammonium nitrate.
Results
Plant biomass and P concentrations always showed positive responses to P addition but not to N addition, nodulation was inhibited by lower P supply and higher N supply. Roots released more phosphatase and carboxylates, mainly tartrate, into the rhizosheath at lower soil P supply and higher N supply. Roots always acidified the rhizosheath, but rhizosheath pH did not vary considerably among treatments.
Conclusions
This study demonstrates the release of tartrate as a major carboxylate as affected by soil P supply and N supply, and highlights the importance of investigating plant adaptive strategies for P acquisition from soil with different N availability for proper application of P and N fertilizers.
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References
Carpenter SR (2005) Eutrophication of aquatic ecosystems: Bistability and soil phosphorus. Proc Natl Acad Sci U S A 102:10002–10005
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
Chen H, Chen M, Li D, Mao Q, Zhang W, Mo J (2018) Responses of soil phosphorus availability to nitrogen addition in a legume and a non-legume plantation. Geoderma 322:12–18
Cordell D, White S (2015) Tracking phosphorus security: indicators of phosphorus vulnerability in the global food system. Food Secur 7:337–350
Dye C (1995) Effect of citrate and tartrate on phosphate adsorption by amorphous ferric hydroxide. Fertilizer Research 40:129–134
Earl KD, Syers JK, McLaughlin JR (1979) Origin of the effects of citrate, tartrate, and acetate on phosphate sorption by soils and synthetic gels. Soil Sci Soc Am J 43:674–678
Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142
Fageria VD (2001) Nutrient interactions in crop plants. J Plant Nutr 24:1269–1290
Fan JW, Du YL, Turner NC, Wang BR, Fang Y, Xi Y, Guo XR, Li FM (2015) Changes in root morphology and physiology to limited phosphorus and moisture in a locally-selected cultivar and an introduced cultivar of Medicago sativa L. growing in alkaline soil. Plant Soil 392:215–226
Fixen PE, Johnston AM (2012) World fertilizer nutrient reserves: a view to the future. J Sci Food Agric 92:1001–1005
He H, Peng Q, Wang X, Fan C, Pang J, Lambers H, Zhang X (2017) Growth, morphological and physiological responses of alfalfa (Medicago sativa) to phosphorus supply in two alkaline soils. Plant Soil 416:565–584
He JZ, De Cristofaro A, Violante A (1999) Comparison of adsorption of phosphate, tartrate, and oxalate on hydroxy aluminum montmorillonite complexes. Clay Clay Miner 47:226–233
Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195
Hinsinger P, Plassard C, Tang CX, Jaillard B (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant Soil 248:43–59
Ibarra-Galeana JA, Castro-Martínez C, Fierro-Coronado RA, Armenta-Bojórquez AD, Maldonado-Mendoza IE (2017) Characterization of phosphate-solubilizing bacteria exhibiting the potential for growth promotion and phosphorus nutrition improvement in maize (Zea mays L.) in calcareous soils of Sinaloa, Mexico. Ann Microbiol 67:801–811
Johnston AE, Poulton PR, Fixen PE, Curtin D (2014) Phosphorus: its efficient use in agriculture. Adv Agron 123:177–228
Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot 98:693–713
Lambers H, Thijs LP, Chapin FS (2008) Plant physiological ecology. Springer, New York, USA
Little IP (1992) The relationship between soil pH measurements in calcium chloride and water suspensions. Aust J Soil Res 30:587–592
Liu FP, Liu HQ, Zhou HL, Dong ZG, Bai XH, Bai P, Qiao JJ (2014) Isolation and characterization of phosphate-solubilizing bacteria from betel nut (Areca catechu) and their effects on plant growth and phosphorus mobilization in tropical soils. Biol Fertil Soils 50:927–937
MacDonald GK, Bennett EM, Potter PA, Ramankutty N (2011) Agronomic phosphorus imbalances across the world's croplands. Proc Natl Acad Sci U S A 108:3086–3091
Maistry PM, Muasyaa AM, Valentineb AJ, Chimphangoa SBM (2015) Balanced allocation of organic acids and biomass for phosphorus and nitrogen demand in the fynbos legume Podalyria calyptrata. J Plant Physiol 174:16–25
Mekonnen MM, Hoekstra AY (2018) Global anthropogenic phosphorus loads to freshwater and associated grey water footprints and water pollution levels: a high-resolution global study. Water Resour Res 54:345–358
Motomizu S, Wakimoto T, Toei K (1983) Spectrophotometric determination of phosphate in river waters with molybdate and malachite green. Analyst 108:361–367
Murray JD, Liu CW, Chen Y, Miller AJ (2017) Nitrogen sensing in legumes. J Exp Bot 68:1919–1926
Nuruzzaman M, Lambers H, Bolland MDA, Veneklaas EJ (2006) Distribution of carboxylates and acid phosphatase and depletion of different phosphorus fractions in the rhizosphere of a cereal and three grain legumes. Plant Soil 281:109–120
Pang J, Ryan MH, Lamberst H, Siddique KHM (2018) Phosphorus acquisition and utilisation in crop legumes under global change. Curr Opin Plant Biol 45:248–254
Pang J, Tibbett M, Denton MD, Lambers H, Siddique KHM, Bolland MDA, Revell CK, Ryan MH (2010) Variation in seedling growth of 11 perennial legumes in response to phosphorus supply. Plant Soil 328:133–143
Pang JY, Yang JY, Lambers H, Tibbett M, Siddique KHM, Ryan MH (2015) Physiological and morphological adaptations of herbaceous perennial legumes allow differential access to sources of varyingly soluble phosphate. Physiol Plant 154:511–525
Pasley HR, Cairns JE, Camberato JJ, Vyn TJ (2019) Nitrogen fertilizer rate increases plant uptake and soil availability of essential nutrients in continuous maize production in Kenya and Zimbabwe. Nutr Cycl Agroecosyst 115:373–389
Perring MP, Hedin LO, Levin SA, McGroddy M, de Mazancourt C (2008) Increased plant growth from nitrogen addition should conserve phosphorus in terrestrial ecosystems. P Natl Acad Sci USA 105:1971–1976
Phoenix GK, Booth RE, Leake JR, Read DJ, Grime JP, Lee JA (2003) Simulated pollutant nitrogen deposition increases P demand and enhances root-surface phosphatase activities of three plant functional types in a calcareous grassland. New Phytol 161:279–289
Plaxton WC, Tran HT (2011) Metabolic adaptations of phosphate-starved plants. Plant Physiol 156:1006–1015
Playsted CWS, Johnston ME, Ramage CM, Edwards DG, Cawthray GR, Lambers H (2006) Functional significance of dauciform roots: exudation of carboxylates and acid phosphatase under phosphorus deficiency in Caustis blakei (Cyperaceae). New Phytol 170:491–500
Png GK, Turner BL, Albornoz FE, Hayes PE, Lambers H, Laliberté E (2017) Greater root phosphatase activity in nitrogen-fixing rhizobial but not actinorhizal plants with declining phosphorus availability. J Ecol 105:1246–1255
Prodhan MA, Finnegan PM, Lambers H (2019) How does evolution in phosphorus-impoverished landscapes impact plant nitrogen and sulfur assimilation? Trends Plant Sci 24:69–82
Raghothama KG (1999) Phosphate acquisition. Ann Rev Plant Physiol Mol Bio 50:665–693
Raghothama KG, Karthikeyan AS (2005) Phosphate acquisition. Plant Soil 274:37–49
Regus JU, Wendlandt CE, Bantay RM, Gano-Cohen KA, Gleason NJ, Hollowell AC, O'Neill MR, Shahin KK, Sachs JL (2017) Nitrogen deposition decreases the benefits of symbiosis in a native legume. Plant Soil 414:159–170
Richardson AE, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Ryan MH, Veneklaas EJ, Lambers H, Oberson A, Culvenor RA, Simpson RJ (2011) Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant Soil 349:121–156
Shahid M, Hameed S, Tariq M, Zafar M, Ali A, Ahmad N (2015) Characterization of mineral phosphate-solubilizing bacteria for enhanced sunflower growth and yield-attributing traits. Ann Microbiol 65:1525–1536
Simpson RJ, Stefanski A, Marshall DJ, Moore AD, Richardson AE (2015) Management of soil phosphorus fertility determines the phosphorus budget of a temperate grazing system and is the key to improving phosphorus efficiency. Agric Ecosyst Environ 212:263–277
Strobel BW (2001) Influence of vegetation on low-molecular-weight carboxylic acids in soil solution - a review. Geoderma 99:169–198
Sun Z, Han J (2018) Effect of soft rock amendment on soil hydraulic parameters and crop performance in mu us Sandy land, China. Field Crop Res 222:85–93
Suriyagoda LDB, Ryan MH, Renton M, Lambers H (2010) Multiple adaptive responses of Australian native perennial legumes with pasture potential to grow in phosphorus- and moisture-limited environments. Ann Bot 105:755–767
Syers J, Johnston A, Curtin D (2008) Efficiency of soil and fertilizer phosphorus use. Reconciling changing concepts of soil phosphorus behaviour with agronomic information. Fertilizer and plant nutrition bulletin no 18 Rome, Italy: FAO
Treseder KK, Vitousek PM (2001) Effects of soil nutrient availability on investment in acquisition of N, P in Hawaiian rain forests. Ecology 82:946–954
Valentine AJ, Kleinert A, Benedito VA (2017) Adaptive strategies for nitrogen metabolism in phosphate deficient legume nodules. Plant Sci 256:46–52
Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447
Wang Y, He Y, Zhang H, Schroder J, Li C, Zhou D (2008) Phosphate mobilization by citric, tartaric, and oxalic acids in a clay loam Ultisol. Soil Sci Soc Am J 72:1263–1268
Zhang X, Davidson EA, Mauzerall DL, Searchinger TD, Dumas P, Shen Y (2015) Managing nitrogen for sustainable development. Nature 528:51–59
Zhao Q, Zeng DH (2019) Nitrogen addition effects on tree growth and soil properties mediated by soil phosphorus availability and tree species identity. Forest Ecol Manag 449:117478
Acknowledgements
This work was supported by The National Key Research and Development Plan of China (2017YFC0504504), The Natural Science Basic Research Program of Shaanxi Province (2019JM-411), The National Natural Science Foundation of China (41301570), The Light of West China Program of Chinese Academy of Sciences, and Fundamental Research Funds for Central Universities in China. We thank Xiyan Chen, College of Life Sciences, Northwest A&F University, for helping the analysis of rhizosheath carboxylates using HPLC.
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He, H., Wu, M., Guo, L. et al. Release of tartrate as a major carboxylate by alfalfa (Medicago sativa L.) under phosphorus deficiency and the effect of soil nitrogen supply. Plant Soil 449, 169–178 (2020). https://doi.org/10.1007/s11104-020-04481-9
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DOI: https://doi.org/10.1007/s11104-020-04481-9