Abstract
Drought exacerbates the limitation of phosphorus (P) deficiency to crop growth and agricultural production. Leaf P resorption is an efficient strategy that a plant develops to cope with P deficiency. However, few studies have explored the involvement of phosphatases in leaf P resorption. A controlled field experiment with P fertilization and irrigation was conducted with lucerne (Medicago sativa L.) during 2016–2018 to assess the influence of P fertilization and water supply on soil nutrient status, soil and leaf phosphatases, and leaf P resorption in the Loess Plateau of eastern Gansu Province, China. Water supply decreased leaf P resorption efficiency (PRE) of lucerne, which was interactively affected by P fertilization. The P fertilization decreased leaf PRE under lower water supply, while increased leaf PRE under higher water supply. Water supply and P fertilization affected leaf acid phosphatase (ACPleaf) activity in a stand age-specific way, while barely affected soil phosphatases activities. The ACPleaf activity was lower in the 2-year stand than 3-year stand. Leaf PRE was negatively correlated with soil P stock (SPS), while leaf P concentration was positively correlated with SPS. The ACPleaf activity was negatively correlated with leaf total P concentration, while soil phosphatases activities were positively correlated with SPS. Leaf PRE was directly positively correlated with the senesced leaf ACP activity, while had no significant correlation with soil phosphatases activities. The study confirms partly the effects of water supply and P fertilization on regulating leaf P resorption, and further reveals the mechanism from the biochemical aspect. The findings have highlighted that ACPleaf plays a role in leaf P reabsorbing process, but soil phosphatases do not. Therefore, an increase in ACPleaf activity induced by P deficiency may lead to an increase in leaf PRE. In addition, the role of soil phosphatases in affecting leaf P resorption needs more exploration.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs42729-022-01087-1/MediaObjects/42729_2022_1087_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs42729-022-01087-1/MediaObjects/42729_2022_1087_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs42729-022-01087-1/MediaObjects/42729_2022_1087_Fig3_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs42729-022-01087-1/MediaObjects/42729_2022_1087_Fig4_HTML.png)
Similar content being viewed by others
Data Availability
The datasets generated and analyzed during the current study are available from the corresponding author upon reasonable request.
References
Aerts R, Chapin FS (2000) The mineral nutrition of wild plants revisited: a reevaluation of processes and patterns. Adv Ecol Res 30:1–67. https://doi.org/10.1016/S0065-2504(08)60016-1
An B, **ao WW, Zhu N (2022) Characteristics of change in diurnal precipitation in the Loess Plateau during 1960–2017. Res of Soil Water Conserv 29:132-138.144. https://doi.org/10.13869/j.cnki.rswc.2022.02.013. (in Chinese with an English abstract)
Balemi T, Negisho K (2012) Management of soil phosphorus and plant adaptation mechanisms to phosphorus stress for sustainable crop production: a review. J Soil Sci Plant Nut 12:547–562. https://doi.org/10.4067/S0718-95162012005000015
Brealey L (1951) The determination of potassium in fertilizers by flame photometry. Analyst 76:340–343. https://doi.org/10.1039/an9517600340
Cheng Y, Peng L, Xu G, Li Z, Cheng S (2018) Effects of soil erosion and land use on spatial distribution of soil total phosphorus in a small watershed on the Loess Plateau, China. Soil till Res 184:142–152. https://doi.org/10.1016/j.still.2018.07.011
Fife DN, Nambiar EKS, Saur E (2008) Retranslocation of foliar nutrients in evergreen tree species planted in a Mediterranean environment. Tree Physiol 28:187–196. https://doi.org/10.1093/treephys/28.2.187
Fornasier F, Dudal Y, Quiquampoix H, Dick RP (2011) Enzyme extraction from soil. In: Dick RP (ed) Methods of soil enzymology. Chapter 16. John Wiley & Sons, Ltd, pp371–383
Gianfreda L, Bollag JM (1996) Influence of natural and anthropogenic factors on enzyme activity in soil. In: Stotzky G, Bollag JM (eds) Soil biochemistry, vol 9. Marcel Dekker, New York, pp 123–194
Gómez-García E, Diéguez-Aranda U, Cunha M, Roque R-S (2016) Comparison of harvest-related removal of aboveground biomass, carbon and nutrients in pedunculate oak stands and in fast-growing tree stands in NW Spain. Forest Ecol Manag 365:119–127. https://doi.org/10.1016/j.foreco.2016.01.021
Heuck C, Weig A, Spohn M (2015) Soil microbial biomass C:N: P stoichiometry and microbial use oforganic phosphorus. Soil Biol Biochem 85:119–129. https://doi.org/10.1016/j.soilbio.2015.02.029
Hofmann K, Heuck C, Spohn M (2016) Phosphorus resorption by young beech trees and soil phosphatase activity as dependent on phosphorus availability. Oecologia 181:369–379. https://doi.org/10.1007/s00442-016-3581-x
Holub P, Ivan T (2010) The effect of enhanced nitrogen on aboveground biomass allocation and nutrient resorption in the fern Athyrium distentifolium. Plant Ecol 207:373–380. https://doi.org/10.1007/s11258-009-9681-5
Holz M, Zarebanadkouki M, Carminati A, Hovind J, Spohn M (2019) Increased water retention in the rhizosphere allows for high phosphatase activity in drying soil. Plant Soil. https://doi.org/10.1007/s11104-019-04234-3
Huang JJ, Wang XH, Yan ER (2007) Leaf nutrient concentration, nutrient resorption and litter decomposition in an evergreen broad-leaved forest in eastern China. Forest Ecol Manag 239:150–158. https://doi.org/10.1016/j.foreco.2006.11.019
Killingbeck K, Whitford W (2001) Nutrient resorption in shrubs growing by design, and by default in Chihuahuan Desert arroyos. Oecologia 128:351–359. https://doi.org/10.1007/s004420100668
Kjeldahl J (1883) A new method for the determination of nitrogen. Chem News 48:101–102. https://doi.org/10.1007/BF02514058
Kumar R, Shastri B (2017) Role of phosphate-solubilising microorganisms in sustainable agricultural development. Agro-Environmental Sustainability. Springer, Cham. pp 271–303. https://doi.org/10.1007/978-3-319-49724-2_13
Lambers H, Finnegan PM, Jost R, Plaxton WC, Shane MW, Stitt M (2015) Phosphorus nutrition in Proteaceae and beyond. Nat Plants 1:15109. https://doi.org/10.1038/nplants.2015.109
Liu MG, Yang M, Yang HM (2021) Biomass production and nutritional characteristics of quinoa subjected to cutting and sowing date in the midwestern China. Grassl Sci 67:215–224. https://doi.org/10.1111/grs.12307
Lu JY, Liu MG, Yang M, **e JH, Yang HM, Li LL (2020) Leaf resorption and stoichiometry of N and P of 1, 2 and 3 year-old lucerne under one-time P fertilization. Soil till Res 197:10448. https://doi.org/10.1016/j.still.2019.104481
Lu JY, Yang M, Liu MG, Lu YX, Yang HM (2019a) Nitrogen and phosphorus fertilizations alter nitrogen, phosphorus and potassium resorption of alfalfa in the Loess Plateau of China. J Plant Nutr 42:2234–2246. https://doi.org/10.1080/01904167.2019.1648668
Lu JY, Yang M, Liu MG, Wang YY, Yang HM (2019b) Leaf stoichiometry and resorption of N and P in Lucerne at different growth stages under different water supplies. J Plant Nutr 42:501–511. https://doi.org/10.1080/01904167.2019.1567776
Lu RK (2000) Methods for agrochemical analysis of soils. Agricultural Science and Technology Press, Bei**g (in Chinese)
Lü XT, Freschet GT, Kazakou E, Wang ZW, Zhou LS, Han XG (2015) Contrasting responses in leaf nutrient-use strategies of two dominant grass species along a 30-yr temperate steppe grazing exclusion chronosequence. Plant Soil 387:69–79. https://doi.org/10.1007/s11104-014-2282-7
Lü XT, Han XG (2010) Nutrient resorption responses to water and nitrogen amendment in semi-arid grassland of Inner Mongolia, China. Plant Soil 327:481–491. https://doi.org/10.1007/s11104-009-0078-y
Lyliana Y, Rentería-Víctor JJ (2011) Rainfall drives leaf traits and leaf nutrient resorption in a tropical dry forest in Mexico. Oecologia 165:201–211. https://doi.org/10.1007/s00442-010-1704-3
Lynch JP (2007) Roots of the second green revolution. Aust J Bot 55:493–512. https://doi.org/10.1016/S0264-410X(02)00552-2
Mao R, Song CC, Zhang XH, Wang XW, Zhang ZH (2013) Response of leaf, sheath and stem nutrient resorption to 7 years of N addition in freshwater wetland of Northeast China. Plant Soil 364:385–394. https://doi.org/10.1007/s11104-012-1370-9
Marklein AR, Houlton BZ (2012) Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytol 193:696–704. https://doi.org/10.1111/j.1469-8137.2011.03967.x
Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soil. In Bünemann E, Oberson A, Frossard E (eds.) Phosphorus in Action, Soil Biology 26, pp 215–243. https://doi.org/10.1007/978-3-642-15271-9_9
Nielsen UN, Ball BA (2015) Impacts of altered precipitation regimes on soil communities and biogeochemistry in arid and semi-arid ecosystems. Global Change Biol 21:1407–1421. https://doi.org/10.1111/gcb.12789
Olander LP, Vitousek PM (2000) Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry 49:175–191. https://doi.org/10.1023/A:1006316117817
Olsen SR (1954) Estimation of Available Phosphorus in Soils by Extraction with Sodium Bicarbonate. No. 939. US Department of Agriculture, Printing Office, Washington, DC
Plassard C (2018) Lack of phosphorus reserves and remobilization in grey poplar (Populus × canescens): an exception among deciduous tree species? Tree Physiol 38:1–5. https://doi.org/10.1093/treephys/tpx170
Plaxton WC, Tran HT (2011) Metabolic adaptations of phosphate-starved plants. Plant Physiol 156:1006–1015. https://doi.org/10.1104/pp.111.175281
Puget P, Lal R (2005) Soil organic carbon and nitrogen in a Mollisol in central Ohio as affected by tillage and land use. Soil till Res 80:201–213. https://doi.org/10.1016/j.still.2004.03.018
Rentería LY, Jaramillo VJ (2011) Rainfall drives leaf traits and leaf nutrient resorption in a tropical dry forest in Mexico. Oecologia 165:201–211. https://doi.org/10.1007/s00442-010-1704-3
Richardson AE, Hadobas PA, Hayes JE (2010) Acid phosphomonoesterase and phytase activities of wheat (Triticum aestivum L.) roots and utilization of organic phosphorus substrates by seedlings grown in sterile culture. Plant Cell Environ 23:397–405. https://doi.org/10.1046/j.1365-3040.2000.00557.x
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. https://doi.org/10.1007/s11104-011-0950-4
Robinson WD, Carson I, Ying S, Ellis K, Plaxton WC (2012) Eliminating the purple acid phosphatase AtPAP26 in Arabidopsis thaliana delays leaf senescence and impairs phosphorus remobilization. New Phytol 196:1024–1029. https://doi.org/10.1111/nph.12006
Sattari SZ, Bouwman AF, Giller KE, Ittersum MV (2012) Residual soil phosphorus as the missing piece in the global phosphorus crisis puzzle. P Natl Acad Sci U S A 109:6348–6353. https://doi.org/10.1073/pnas.1113675109
See CR, Yanai RD, Fisk MC, Vadeboncoeur MA, Quintero BA, Fahey TJ (2015) Soil nitrogen affects phosphorus recycling: foliar resorption and plant-soil feedbacks in a northern hardwood forest. Ecology 96:2488–2498. https://doi.org/10.1890/15-0188.1
Sharma SB, Sayyed RZ, Trivedi MH, Gobi TA (2013) Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. Springer plus 2:587. https://doi.org/10.1186/2193-1801-2-587
Song JG, Liu W, Zhao ZJ, Lin S, Wu WL, Mao DR (2001) Effects of desiccation of soil samples on easily mineralizing nitrogen. J Plant Nut Fert 7:183–188. https://doi.org/10.11674/zwyf.2001.0211
Spohn M, Carminati A, Kuzyakov Y (2013) Soil zymography - a novel in situ method for map** distribution of enzyme activity in soil. Soil Biol Biochem 58:275–280. https://doi.org/10.1016/j.soilbio.2012.12.004
Tabatabai MA (1994) Soil enzymes. In: Weaver RW, Angle S, Bottomley P, Bezdicek D, Smith S, Tabatabai A, Wollum A (eds.) Methods of soil analysis. Part 2: microbiological and biochemical properties. SSSA Book Series No. 5. Soil Science Society of America, Inc, Madison, WI, pp 775-833
Tang LY, Han WX, Chen YH, Fang JY (2013) Resorption proficiency and efficiency of leaf nutrients in woody plants in eastern China. J Plant Ecol 6:408–417. https://doi.org/10.1093/jpe/rtt013
Tarnocai C (1998) The amount of organic carbon in various soil orders and ecological provinces in Canada. In: Lal R, Kimble JM, Follett RLF, Stewart BA (eds) Soil processes and the carbon cycle: Advances in soil science. CRC Press, New York, pp 81–92
Tsujii Y, Onoda Y, Kitayama K (2017) Phosphorus and nitrogen resorption from different chemical fractions in senescing leaves of tropical tree species on Mount Kinabalu, Borneo. Oecologia 185:171–180. https://doi.org/10.1007/s00442-017-3938-9
Tully KL, Lawrence D (2013) Soil nutrient availability and reproductive effort drive patterns in nutrient resorption in Pentaclethra macroloba. Ecology 94:930–940. https://doi.org/10.1890/12-0781.1
Turner BL, Wright SJ (2014) The response of microbial biomass and hydrolytic enzymes to a decade of nitrogen, phosphorus, and potassium addition in a lowland tropical rain forest. Biogeochemistry 117:115–130. https://doi.org/10.1007/s10533-013-9848-y
Vance C (2003) Phosphorus acquisition and use: critical adaptations by plants securing a nonrenewable resource. New Phytol 157:423–447. https://doi.org/10.1046/j.1469-8137.2003.00695.x
Venterink HO, Wassen MJ, Verkroost AWM, de Ruiter PC (2003) Species richness-productivity patterns differ between N-, P-, and K-limited wetlands. Ecology 84:2191–2199. https://doi.org/10.1890/01-0639
Vergutz L, Manzoni S, Porporato A, Novais RF, Jackson RB (2012) Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecol Monogr 82:205–220. https://doi.org/10.1890/11-0416.1
Wang RZ, Creamer CA, Wang X, He P, Xu ZW, Jiang Y (2016) The effects of a 9-year nitrogen and water addition on soil aggregate phosphorus and sulfur availability in a semi-arid grassland. Ecol Indic 61:806–814. https://doi.org/10.1016/j.ecolind.2015.10.033
Wang ZN, Lu JY, Yang HM, Zhang X, Luo CL, Zhao YX (2014) Resorption of nitrogen, phosphorus and potassium from leaves of lucerne stands of different ages. Plant Soil 383:301–312. https://doi.org/10.1007/s11104-014-2166-x
Xu MP, Zhong ZK, Sun ZY, Han XH, Ren CJ, Yang GH (2020) Soil available phosphorus and moisture drive nutrient resorption patterns in plantations on the Loess Plateau. Forest Ecol Manag 461:117910. https://doi.org/10.1016/j.foreco.2020.117910
Yan X, Liao H, Trull MC, Beebe SE, Lynch JP (2001) Induction of a major leaf acid phosphatase does not confer adaptation to low phosphorus availability in common bean. Plant Physiol 125:1901–1911. https://doi.org/10.1104/pp.125.4.1901
Yang M, Yang HM (2021) Utilization of soil residual phosphorus and internal reuse of phosphorus by crops. PeerJ 9:e11704. https://doi.org/10.7717/peerj.11704
Yuan ZY, Chen HYH (2009a) Global-scale patterns of nutrient resorption associated with latitude, temperature and precipitation. Global Ecol Biogeogr 18:11–18. https://doi.org/10.1111/j.1466-8238.2008.00425.x
Yuan ZY, Chen HYH (2009b) Global trends in senesced-leaf nitrogen and phosphorus. Global Ecol Biogeogr 18:532–542. https://doi.org/10.1111/j.1466-8238.2009.00474.x
Yuan ZY, Chen HYH (2015) Negative effects of fertilization on plant nutrient resorption. Ecology 96:373–380. https://doi.org/10.1890/14-0140.1
Yun SJ, Kaeppler SM (2001) Induction of maize acid phosphatase activities under phosphorus starvation. Plant Soil 237:109–115. https://doi.org/10.1023/A:1013329430212
Zeng WJ, Chen JB, Liu HY, Wang W (2018) Soil respiration and its autotrophic and heterotrophic components in response to nitrogen addition among different degraded temperate grasslands. Soil Biol Biochem 124:255–265. https://doi.org/10.1016/j.soilbio.2018.06.019
Acknowledgements
We appreciated very much the help from Dr Jiaoyun Lu, Ms Feifei You, and Mr Juncheng Li for assistance in field sampling and lab measurement. As Newton said, “If I have seen further, it is by standing on the shoulders of giants”; this work would be impossible without the previous valuable researches.
Funding
This work was supported by the National Natural Science Foundation of China (grant number 32201475 and 32171679) and the earmarked fund for China Agriculture Research System of MOF and MARA (CARS-34).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
42729_2022_1087_MOESM1_ESM.jpg
Supplementary file1 (JPG 1489 KB) Fig. S1 Ternary diagrams showing stoichiometric relationships of N, P, and K in the green leaves of lucerne as a function of stand age (a), P fertilization (b) and water supply (c). Dashed lines indicate the critical ratios of N:P (14.5), N:K (2.1), and K:P (3.4) dividing the plots into 4 sections. Three of the sections show N limitation (N:P<14.5 and N:K<2.1), P limitation or P+N co-limitation (N:P>14.5 and K:P>3.4), K limitation or K+N co-limitation (N:K>2.1 and K:P<3.4), while for the central triangle section, the stoichiometric ratio cannot tell the type of nutrient limitation or whether this is non-NPK limitation (Venterink et al. 2003). 1, 2, and 3, stand age. HW, high water supply; LW, low water supply; NW, normal water supply.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Yang, M., Lu, Y., Mu, L. et al. Leaf and Soil Phosphatases and the Correlations with Leaf P Resorption of Lucerne Under P Fertilization and Irrigation. J Soil Sci Plant Nutr 23, 842–853 (2023). https://doi.org/10.1007/s42729-022-01087-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42729-022-01087-1