Abstract
As phosphorus (P) is one of the most limiting elements for crop growth and development, investigating the P allocation strategy of legume species with the nitrogen (N)-fixing functions is particularly important under N and P limitation. In this study, a pot experiment in a greenhouse was conducted in 2021 with three nutrient application treatments including N and P balanced situations, N limitation, and P limitation. The growth, photosynthetic properties, and P content of three organs (leaf, stem, and root P content) and four fractions within leaves (metabolic, nucleic, lipid, and residual P content) were measured for two cultivars of the legume forage crop alfalfa. In our results, plant growth and photosynthetic capacity all decreased under nutrient limitation (P < 0.05), but photosynthetic P-use efficiency was not significantly changed under P limitation. The further analysis showed that P allocation to leaves (ranged from 22% to 29%) significantly decreased but allocations to stems (ranged from 32% to 45%) or roots (ranged from 30% to 43%) increased under nutrient limitation, and the proportions of leaf metabolic P (ranged from 45% to 75%) and nucleic acid P (ranged from 15% to 20%) were increased under P and N limitations (P < 0.05), respectively. In addition, leaf acid phosphatase activity was strongly negatively correlated with leaf residual P (r = − 0.884, P < 0.01). Our results revealed that P allocation of alfalfa was changed by nutrient limitation to increase plant P-use efficiencies, and that the allocation strategy also differed between N and P limitation, in which leaf acid phosphatase played an important role in conversion among leaf P fractions.
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Data Availability
The data that support the findings of this study are available from the corresponding author XL upon reasonable request.
References
Ågren GI (2008) Stoichiometry and nutrition of plant growth in natural communities. Annu Rev Ecol Syst 39:153–170
Ågren GI, Wetterstedt JM, Billberger MF (2012) Nutrient limitation on terrestrial plant growth–modeling the interaction between nitrogen and phosphorus. New Phytol 194:953–960. https://doi.org/10.1111/j.1469-8137.2012.04116.x
Cordell D, Rosemarin A, Schroder JJ, Smit AL (2011) Towards global phosphorus security: a systems framework for phosphorus recovery and reuse options. Chemosphere 84:747–758. https://doi.org/10.1016/j.chemosphere.2011.02.032
Denton MD, Veneklaas EJ, Freimoser FM, Lambers H (2007) Banksia species (Proteaceae) from severely phosphorus-impoverished soils exhibit extreme efficiency in the use and re-mobilization of phosphorus. Plant Cell Environ 30:1557–1565. https://doi.org/10.1111/j.1365-3040.2007.01733.x
Dissanayaka D, Ghahremani M, Siebers M, Wasaki J, Plaxton WC (2021) Recent insights into the metabolic adaptations of phosphorus-deprived plants. J Exp Bot 72:199–223. https://doi.org/10.1093/jxb/eraa482
Du E, Terrer C, Pellegrini AF, Ahlström A, van Lissa CJ, Zhao X, **a N, Wu X, Jackson RB (2020) Global patterns of terrestrial nitrogen and phosphorus limitation. Nat Geosci 13:221–226. https://doi.org/10.1038/s41561-019-0530-4
Dülger E, Heidbüchel P, Schumann T, Mettler-Altmann T, Hussner A (2017) Interactive effects of nitrate concentrations and carbon dioxide on the stoichiometry, biomass allocation and growth rate of submerged aquatic plants. Freshwat Biol 62:1094–1104. https://doi.org/10.1111/fwb.12928
Elfaki MO, Abdelatti KA (2016) Rumen content as animal feed: a review. J Vet Med Animal Prod 7:80–88
Elser JJ, Bracken M, 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. https://doi.org/10.1111/j.1461-0248.2007.01113.x
Fan J-W, Du Y-L, Turner NC, Wang B-R, Fang Y, ** Y, Guo X-R, Li F-M (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. https://doi.org/10.1007/s11104-015-2454-0
Farssi O, Mouradi M, Aziz F, Berrougui H (2022) Role of acid phosphatase and enzymatic and non-enzymatic antioxidant systems in tolerance of alfalfa (Medicago sativa L.) populations to low phosphorus availability. Agronomy Research 20:951–964. https://doi.org/10.15159/AR.22.064
Feng Y-L, Lei Y-B, Wang R-F, Callaway RM, Valiente-Banuet A, Inderjit L-P, Zheng Y-L (2009) Evolutionary tradeoffs for nitrogen allocation to photosynthesis versus cell walls in an invasive plant. Proc Natl Acad Sci 106:1853–1856. https://doi.org/10.1073/pnas.080843410
Fischer AM (2007) Nutrient remobilization during leaf senescence. In: Gan, S. (ed): Annual Reviews of Senescence Processes in Plants. Blackwell Oxford, 26:87–107. https://doi.org/10.1002/9780470988855.ch5
Ghannoum O, Evans JR, Chow WS, Andrews TJ, Conroy JP, von Caemmerer S (2005) Faster Rubisco is the key to superior nitrogen-use efficiency in NADP-malic enzyme relative to NAD-malic enzyme C4 grasses. Plant Physiol 137:638–650. https://doi.org/10.1104/pp.104.054759
Grasset C, Delolme C, Arthaud F, Bornette G (2015) Carbon allocation in aquatic plants with contrasting strategies: the role of habitat nutrient content. J Veg Sci 26:946–955. https://doi.org/10.1111/jvs.12298
Han Z, Shi J, Pang J, Yan L, Lambers H (2020) Foliar nutrient-allocation patterns in Banksia attenuata and Banksia sessilis differing in growth rate and adaptation to low-phosphorus habitats. Ann Bot 128:419–430. https://doi.org/10.1093/aob/mcab013
Hayes PE, Adem GD, Pariasca-Tanaka J, Wissuwa M (2022) Leaf phosphorus fractionation in rice to understand internal phosphorus-use efficiency. Ann Bot 129:287–302. https://doi.org/10.1093/aob/mcab138
He S, Long M, He X, Guo L, Yang J, Yang P, Hu T (2017) Arbuscular mycorrhizal fungi and water availability affect biomass and C: N: P ecological stoichiometry in alfalfa (Medicago sativa L.) during regrowth. Acta Physiol Plant 39:1–9. https://doi.org/10.1007/s11104-009-0249-x
Hidaka A, Kitayama K (2011) Allocation of foliar phosphorus fractions and leaf traits of tropical tree species in response to decreased soil phosphorus availability on Mount Kinabalu, Borneo. J Ecol 99:849–857. https://doi.org/10.1111/j.1365-2745.2011.01805.x
Hidaka A, Kitayama K (2013) Relationship between photosynthetic phosphorus-use efficiency and foliar phosphorus fractions in tropical tree species. Ecol Evol 3:4872–4880. https://doi.org/10.1002/ece3.861
Irfan M, Aziz T, Maqsood MA, Bilal HM, Siddique KH, Xu M (2020) Phosphorus (P) use efficiency in rice is linked to tissue-specific biomass and P allocation patterns. Sci Rep 10:1–14. https://doi.org/10.1038/s41598-020-61147-3
Lambers H, Brundrett MC, Raven JA, Hopper SD (2011) Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies. Plant Soil 348:7–27. https://doi.org/10.1007/s11104-011-0977-6
Lambers H, Cawthray GR, Giavalisco P, Kuo J, Laliberté E, Pearse SJ, Scheible WR, Stitt M, Teste F, Turner BL (2012) Proteaceae from severely phosphorus-impoverished soils extensively replace phospholipids with galactolipids and sulfolipids during leaf development to achieve a high photosynthetic phosphorus-use-efficiency. New Phytol 196:1098–1108. https://doi.org/10.1111/j.1469-8137.2012.04285.x
Malhotra H, Sharma S, Pandey R (2018) Phosphorus nutrition: plant growth in response to deficiency and excess. (eds) Hasanuzzaman M, Fujita M, Oku H, Nahar K, Hawrylak-Nowak B. Plant nutrients and abiotic stress tolerance. Springer, Singapore, pp 171–190. https://doi.org/10.1007/978-981-10-9044-8_7
Matzek V, Vitousek PM (2009) N: P stoichiometry and protein: RNA ratios in vascular plants: an evaluation of the growth-rate hypothesis. Ecol Lett 12:765–771. https://doi.org/10.1111/j.1461-0248.2009.01310.x
Minden V, Schaller J, Olde Venterink H (2021) Plants increase silicon content as a response to nitrogen or phosphorus limitation: a case study with Holcus lanatus. Plant Soil 462:95–108. https://doi.org/10.1007/s11104-020-04667-1
Mo Q, Za Li, Sayer EJ, Lambers H, Li Y, Zou B, Tang J, Heskel M, Ding Y, Wang F (2019) Foliar phosphorus fractions reveal how tropical plants maintain photosynthetic rates despite low soil phosphorus availability. Funct Ecol 33:503–513. https://doi.org/10.1111/1365-2435.13252
Pang J, Ryan MH, Tibbett M, Cawthray GR, Siddique KH, Bolland MD, Denton MD, Lambers H (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
Pueyo JJ, Quiñones MA, Coba de la Peña T, Fedorova EE, Lucas MM (2021) Nitrogen and phosphorus interplay in lupin root nodules and cluster roots. Front Plant Sci 12:644218. https://doi.org/10.3389/fpls.2021.644218
Rao Q, Su H, Deng X, **a W, Wang L, Cui W, Ruan L, Chen J, **e P (2020) Carbon, nitrogen, and phosphorus allocation strategy among organs in submerged macrophytes is altered by eutrophication. Front Plant Sci 11:524450. https://doi.org/10.3389/fpls.2020.524450
Raven JA (2012) Protein turnover and plant RNA and phosphorus requirements in relation to nitrogen fixation. Plant Sci 188:25–35. https://doi.org/10.1016/j.plantsci.2012.02.010
Reich PB, Oleksyn J, Wright IJ, Niklas KJ, Hedin L, Elser JJ (2010) Evidence of a general 2/3-power law of scaling leaf nitrogen to phosphorus among major plant groups and biomes. Proc Royal Soc b: Biol Sci 277:877–883. https://doi.org/10.1098/rspb.2009.1818
Sardans J, Peñuelas J (2013) Tree growth changes with climate and forest type are associated with relative allocation of nutrients, especially phosphorus, to leaves and wood. Global Ecol Biogeogr 22:494–507. https://doi.org/10.1111/geb.12015
Schlüter U, Colmsee C, Scholz U, Bräutigam A, Weber AP, Zellerhoff N, Bucher M, Fahnenstich H, Sonnewald U (2013) Adaptation of maize source leaf metabolism to stress related disturbances in carbon, nitrogen and phosphorus balance. BMC Genomics 14:1–25. https://doi.org/10.1186/1471-2164-14-442
Shane MW, McCully ME, Lambers H (2004) Tissue and cellular phosphorus storage during development of phosphorus toxicity in Hakea prostrata (Proteaceae). J Exp Bot 55:1033–1044. https://doi.org/10.1093/jxb/erh111
Sulpice R, Ishihara H, Schlereth A, Cawthray GR, Encke B, Giavalisco P, Ivakov A, Arrivault S, Jost R, Krohn N (2014) Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus-use efficiency of P roteaceae species. Plant, Cell Environ 37:1276–1298. https://doi.org/10.1111/pce.12240
Suriyagoda LDB, Lambers H, Renton M, Ryan MH (2012) Growth, carboxylate exudates and nutrient dynamics in three herbaceous perennial plant species under low, moderate and high phosphorus supply. Plant Soil 358:105–117. https://doi.org/10.1007/s11104-012-1311-7
Tairo EV, Ndakidemi PA (2013) Possible benefits of rhizobial inoculation and phosphorus supplementation on nutrition, growth and economic sustainability in grain legumes. American J Res Com 1:532–556
Tian D, Yan Z, Niklas KJ, Han W, Kattge J, Reich PB, Luo Y, Chen Y, Tang Z, Hu H (2018) Global leaf nitrogen and phosphorus stoichiometry and their scaling exponent. Natl Sci Rev 5:728–739. https://doi.org/10.1093/nsr/nwx142
Tingey DT, McKane RB, Olszyk DM, Johnson MG, Rygiewicz PT, Henry Lee E (2003) Elevated CO2 and temperature alter nitrogen allocation in Douglas-fir. Global Change Biol 9:1038–1050. https://doi.org/10.1046/j.1365-2486.2003.00646.x
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
Udvardi M, Poole PS (2013) Transport and metabolism in legume-rhizobia symbioses. Annu Rev Plant Biol 64:781–805. https://doi.org/10.1146/annurev-arplant-050312-120235
Ushio M, Fujiki Y, Hidaka A, Kitayama K (2015) Linkage of root physiology and morphology as an adaptation to soil phosphorus impoverishment in tropical montane forests. Funct Ecol 29:1235–1245. https://doi.org/10.1111/1365-2435.12424
Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE, Plaxton WC, Price CA, Scheible WR, Shane MW, White PJ (2012) Opportunities for improving phosphorus-use efficiency in crop plants. New Phytol 195:306–320. https://doi.org/10.1111/j.1469-8137.2012.04190.x
Wang L, Liu D (2018) Functions and regulation of phosphate starvation-induced secreted acid phosphatases in higher plants. Plant Sci 271:108–116. https://doi.org/10.1016/j.plantsci.2018.03.013
Wang C, Ma B, Han J, Wang Y, Gao Y, Hu X, Zhang C (2008) Photoperiod effect on phytochrome and abscisic acid in alfalfa varieties differing in fall dormancy. J Plant Nutr 31:1257–1269. https://doi.org/10.1080/01904160802135027
**e Y, Li X, Huang X, Han S, Amombo E, Wassie M, Chen L, Fu J (2019) Characterization of the Cd-resistant fungus Aspergillus aculeatus and its potential for increasing the antioxidant activity and photosynthetic efficiency of rice. Ecotoxicol Environ Saf 171:373–381. https://doi.org/10.1016/j.ecoenv.2018.11.123
Yan Z, Li P, Chen Y, Han W, Fang J (2016) Nutrient allocation strategies of woody plants: an approach from the scaling of nitrogen and phosphorus between twig stems and leaves. Sci Rep 6:20099. https://doi.org/10.1038/srep20099
Yang X, Tang Z, Ji C, Liu H, Ma W, Mohhamot A, Shi Z, Sun W, Wang T, Wang X (2014) Scaling of nitrogen and phosphorus across plant organs in shrubland biomes across Northern China. Sci Rep 4:1–7. https://doi.org/10.1038/srep05448
Yu Q, Ni X, Cheng X, Ma S, Tian D, Zhu B, Zhu J, Ji C, Tang Z, Fang J (2022) Foliar phosphorus allocation and photosynthesis reveal plants’ adaptative strategies to phosphorus limitation in tropical forests at different successional stages. Sci Total Environ 846:157456. https://doi.org/10.1016/j.scitotenv.2022.157456
Zhang J, He N, Liu C, Xu L, Yu Q, Yu G (2018) Allocation strategies for nitrogen and phosphorus in forest plants. Oikos 127:1506–1514. https://doi.org/10.1111/oik.05517
Zhang Q, **ong G, Li J, Lu Z, Li Y, Xu W, Wang Y, Zhao C, Tang Z, **e Z (2018) Nitrogen and phosphorus concentrations and allocation strategies among shrub organs: the effects of plant growth forms and nitrogen-fixation types. Plant Soil 427:305–319. https://doi.org/10.1007/s11104-018-3655-0
Zhang L, Luo X, Lambers H, Zhang G, Liu N, Zang X, **ao M, Wen D (2021) Effects of elevated CO2 concentration and nitrogen addition on foliar phosphorus fractions of Mikania micranatha and Chromolaena odorata under low phosphorus availability. Physiol Plant 173:2068–2080. https://doi.org/10.1111/ppl.13555
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This study was supported by the Postgraduate Research & Practice Innovation Program of Jiangsu Province (Yangzhou University) (Grant number: KYCX22_3559).
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XL conceived and designed the experiment; YH and CQ conducted these experiments; YH and XL wrote the manuscript and further revision; XZ, DL, JL, and LW helped in the greenhouse and laboratory experiments. YH and CQ contributed equally.
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Yafei Hu and Cheng Qian are contributed equally to this work and share first authorship.
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Hu, Y., Qian, C., Zhao, X. et al. Effects of Nitrogen and Phosphorus Limitation on the Growth and Phosphorus Allocation of Alfalfa (Medicago sativa L.). J Soil Sci Plant Nutr 24, 343–353 (2024). https://doi.org/10.1007/s42729-023-01541-8
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DOI: https://doi.org/10.1007/s42729-023-01541-8