Eurasian Journal of Soil Science

Volume 13, Issue 1, Jan 2024, Pages 79 - 88
DOI: 10.18393/ejss.1399856
Stable URL: http://ejss.fess.org/10.18393/ejss.1399856
Copyright © 2024 The authors and Federation of Eurasian Soil Science Societies



Enhancing phosphorus use efficiency in wheat grown on alkaline calcareous soils

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Abbas,M., Irfan,M., Shah,J., Sial,N., Depar,N., 2024. Enhancing phosphorus use efficiency in wheat grown on alkaline calcareous soils. Eurasian J Soil Sci 13(1):79 - 88. DOI : 10.18393/ejss.1399856
Abbas,M.,Irfan,M.Shah,J.Sial,N.,& Depar,N. Enhancing phosphorus use efficiency in wheat grown on alkaline calcareous soils Eurasian Journal of Soil Science, 13(1):79 - 88. DOI : 10.18393/ejss.1399856
Abbas,M.,Irfan,M.Shah,J.Sial,N., and ,Depar,N."Enhancing phosphorus use efficiency in wheat grown on alkaline calcareous soils" Eurasian Journal of Soil Science, 13.1 (2024):79 - 88. DOI : 10.18393/ejss.1399856
Abbas,M.,Irfan,M.Shah,J.Sial,N., and ,Depar,N. "Enhancing phosphorus use efficiency in wheat grown on alkaline calcareous soils" Eurasian Journal of Soil Science,13(Jan 2024):79 - 88 DOI : 10.18393/ejss.1399856
M,Abbas.M,Irfan.J,Shah.N,Sial.N,Depar "Enhancing phosphorus use efficiency in wheat grown on alkaline calcareous soils" Eurasian J. Soil Sci, vol.13, no.1, pp.79 - 88 (Jan 2024), DOI : 10.18393/ejss.1399856
Abbas,Muhammad ;Irfan,Muhammad ;Shah,Javaid Ahmed ;Sial,Niaz Ali ;Depar,Nizamuddin Enhancing phosphorus use efficiency in wheat grown on alkaline calcareous soils. Eurasian Journal of Soil Science, (2024),13.1:79 - 88. DOI : 10.18393/ejss.1399856

How to cite

Abbas, M., Irfan, M., Shah, J., Sial, N., Depar, N., 2024. Enhancing phosphorus use efficiency in wheat grown on alkaline calcareous soils. Eurasian J. Soil Sci. 13(1): 79 - 88. DOI : 10.18393/ejss.1399856

Author information

Muhammad Abbas , Soil & Environmental Sciences Division, Nuclear Institute of Agriculture (NIA), Tandojam-70060, Pakistan
Muhammad Irfan , Soil & Environmental Sciences Division, Nuclear Institute of Agriculture (NIA), Tandojam-70060, Pakistan
Javaid Ahmed Shah , Soil & Environmental Sciences Division, Nuclear Institute of Agriculture (NIA), Tandojam-70060, Pakistan
Niaz Ali Sial , Soil & Environmental Sciences Division, Nuclear Institute of Agriculture (NIA), Tandojam-70060, Pakistan
Nizamuddin Depar , Soil & Environmental Sciences Division, Nuclear Institute of Agriculture (NIA), Tandojam-70060, Pakistan

Publication information

Article first published online : 04 Dec 2023
Manuscript Accepted : 30 Nov 2023
Manuscript Received: 16 Aug 2023
DOI: 10.18393/ejss.1399856
Stable URL: http://ejss.fesss.org/10.18393/ejss.1399856

Abstract

Phosphorus (P) use efficiency is crucial for sustainable wheat production, particularly on alkaline calcareous soils. This study investigates the relative importance of two factors; P acquisition efficiency (PAE) and P utilization efficiency (PUtE), in determining P use efficiency (PUE) in wheat. A field trial with ten wheat genotypes was conducted under two P levels (no P application and P application at 110 kg P2O5 ha−1). Results revealed significant genetic variability in PUE, PAE, and PUtE among wheat genotypes under varying P availabilities. Genotypes MK-4 and MK-8 exhibited superior PUE, making them ideal candidates for soils with differing P levels. PAE played a more substantial role in influencing PUE, with PUtE contributing less to the variability. The findings underscore the importance of improving PAE, particularly for wheat genotypes grown in P-deficient conditions. Moreover, selecting genotypes with lower grain P concentration can enhance PUtE, contributing to improved PUE. These insights can improve breeding efforts and crop management practices to enhance P use efficiency in wheat, ultimately reducing production costs and fertilizer demand, especially in P-limited alkaline calcareous soils.

Keywords

Alkaline-calcareous soil, P acquisition efficiency, P utilization efficiency, P use efficiency, wheat genotypes.

Corresponding author

References

Abbas, M., Irfan, M., Shah, J.A., 2018a. Differential performance of wheat genotypes for grain yield, phosphorus uptake and utilization at low and high phosphorus: Evaluation of PUE in wheat genotypes. Proceedings of the Pakistan Academy of Sciences: B. Life and Environmental Sciences 55(2): 55-64.

Abbas, M., Shah, J.A., Irfan, M., Memon, M.Y., 2018b. Remobilization and utilization of phosphorus in wheat cultivars under induced phosphorus deficiency. Journal of Plant Nutrition 41(12): 1522-1533.

Amtmann, A., Armengaud, P., 2009. Effects of N, P, K and S on metabolism: new knowledge gained from multi-level analysis. Current Opinion in Plant Biology 12(3): 275-283.

Baker, A., Ceasar, S.A., Palmer, A.J., Paterson, J.B., Qi, W., Muench, S.P., Baldwin, S.A., 2015. Replace, reuse, recycle: improving the sustainable use of phosphorus by plants. Journal of Experimental Botany 66(12): 3523-3540.

Bayuelo-Jiménez, J.S., Ochoa-Cadavid, I., 2014. Phosphorus acquisition and internal utilization efficiency among maize landraces from the central Mexican highlands. Field Crops Research 156: 123-134.

Beebe, S.E., Rojas‐Pierce, M., Yan, X., Blair, M.W., Pedraza, F., Munoz, F., Tohme, J., Lynch, J.P., 2006. Quantitative trait loci for root architecture traits correlated with phosphorus acquisition in common bean. Crop Science 46(1): 413-423.

Byrne, S.L., Foito, A., Hedley, P.E., Morris, J.A., Stewart, D., Barth, S., 2011. Early response mechanisms of perennial ryegrass (Lolium perenne) to phosphorus deficiency. Annals of Botany 107(2): 243-254.

Chapman, H.D., Pratt, F.P., 1961. Ammonium vandate-molybdate method for determination of phosphorus. In: Methods of analysis for soils, plants and waters. Division of Agricultural Sciences, University of California, pp. 184-203.

Cordell, D., Drangert, J.O., White, S., 2009. The story of phosphorus: global food security and food for thought. Global Environmental Change 19(2): 292-305.

Gemenet, D.C., Hash, C.T., Sanogo, M.D., Sy, O., Zangre, R.G., Leiser, W.L., Haussmann, B.I., 2015. Phosphorus uptake and utilization efficiency in West African pearl millet inbred lines. Field Crops Research 171: 54-66.

Gill, H.S., Singh, A., Sethi, S.K., Behl, R.K., 2004. Phosphorus uptake and use efficiency in different varieties of bread wheat (Triticum aestivum L). Archives of Agronomy and Soil Science 50(6): 563-572.

Gomez, K.A., Gomez, A.A., 1984. Statistical procedures for agricultural research. John Wiley & Sons, New York. 657p.

Government of Pakistan, 2022. Pakistan Economic Survey 2021-22. Ministry of Finance, Islamabad, Pakistan.

Irfan, M., Abbas, M., Shah, J.A. and Memon, M.Y., 2018. Internal and external phosphorus requirements for optimum grain yield are associated with P-utilization efficiency of wheat cultivars. Communications in Soil Science and Plant Analysis 49(22): 2843-2853.

Karthikeyan, A.S., Jain, A., Nagarajan, V.K., Sinilal, B., Sahi, S.V., Raghothama, K.G., 2014. Arabidopsis thaliana mutant lpsi reveals impairment in the root responses to local phosphate availability. Plant Physiology and Biochemistry 77: 60-72.

Kochian, L.V., 2012. Rooting for more phosphorus. Nature 488(7412): 466-467.

Korkmaz, K., İbrikçi, H., Karnez, E., Buyuk, G., Ryan, J., Ulger, A.C., Oguz, H., 2009. Phosphorus use efficiency of wheat genotypes grown in calcareous soils. Journal of Plant Nutrition 32(12): 2094-2106.

Lambers, H., Cawthray, G.R., Giavalisco, P., Kuo, J., Laliberté, E., Pearse, S.J., Scheible, W.R., Stitt, M., Teste, F., Turner, B.L., 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 Phytologist 196(4): 1098-1108.

Liu, H., Shi, Z., Ma, F., Xu, Y., Han, G., Zhang, J., Liu, D., An, D., 2022. Identification and validation of plant height, spike length and spike compactness loci in common wheat (Triticum aestivum L.). BMC Plant Biology 22(1): 568.

Manschadi, A.M., Kaul, H.P., Vollmann, J., Eitzinger, J., Wenzel, W., 2014. Developing phosphorus-efficient crop varieties - an interdisciplinary research framework. Field Crops Research 162: 87-98.

Manske, G.G.B., Ortiz-Monasterio, J.I., Van Ginkel, M., Gonzalez, R.M., Fischer, R.A., Rajaram, S., Vlek, P.L.G., 2001. Importance of P uptake efficiency versus P utilization for wheat yield in acid and calcareous soils in Mexico. European Journal of Agronomy 14(4): 261-274.

Marschner, H. 2012. Marschner's mineral nutrition of higher plants. 3rd edition. Academic Press, Elsevier. 672p.

McDonald, G., Bovill, W., Taylor, J., Wheeler, R., 2015. Responses to phosphorus among wheat genotypes. Crop and Pasture Science 66(5): 430-444.

Memon, K.S., 2005. Soil & fertilizer phosphorus. In: Soil Science. Bashir, A. Bantel, R., (Eds.). National Book Foundation, Islamabad, Pakistan. pp. 291-316.

Miller, R.O., 1998. Nitric-perchloric acid wet digestion in an open vessel. In: Handbook of reference methods for plant analysis. Kalra, Y.P. (Ed.). CRC Press, Washington D.C., USA. pp. 57-61.

Moll, R.H., Kamprath, E.J., Jackson, W.A., 1982. Analysis and interpretation of factors which contribute to efficiency of nitrogen utilization. Agronomy Journal 74(3): 562-564.

NFDC, 2019-2020. National Fertilizer Development Center (NFDC). Crop Wise Usage of Fertilizer. Ministry of National Food Security and Research, Government of Pakistan, Islamabad. Available at [Access date: 16.08.2023]: http://www.nfdc.gov.pk/

Niu, Y.F., Chai, R.S., Jin, G.L., Wang, H., Tang, C.X., Zhang, Y.S., 2013. Responses of root architecture development to low phosphorus availability: a review. Annals of Botany 112(2): 391-408.

Olsen, S.R., 1954. Estimation of available phosphorus in soils by extraction with sodium bicarbonate, Circular No. 939. US Department of Agriculture, Washington, D.C. USA. 19p.

Panigrahy, M., Rao, D.N., Sarla, N., 2009. Molecular mechanisms in response to phosphate starvation in rice. Biotechnology Advances 27(4): 389-397.

Parentoni, S.N., Souza Júnior, C.L.D., 2008. Phosphorus acquisition and internal utilization efficiency in tropical maize genotypes. Pesquisa Agropecuária Brasileira 43: 893-901.

Rose, T.J. and Wissuwa, M., 2012. Rethinking internal phosphorus utilization efficiency: a new approach is needed to improve PUE in grain crops. Advances in Agronomy 116: 185-217.

Rose, T.J., Rose, M.T., Pariasca-Tanaka, J., Heuer, S., Wissuwa, M., 2011. The frustration with utilization: why have improvements in internal phosphorus utilization efficiency in crops remained so elusive?. Frontiers in Plant Science 2: 73.

Ruark, M.D., Kelling, K.A., Good, L.W., 2014. Environmental concerns of phosphorus management in potato production. American Journal of Potato Research 91(2): 132-144.

Sandaña, P., Pinochet, D., 2014. Grain yield and phosphorus use efficiency of wheat and pea in a high yielding environment. Journal of Soil Science and Plant Nutrition 14(4): 973-986.

Sandaña, P., 2016. Phosphorus uptake and utilization efficiency in response to potato genotype and phosphorus availability. European Journal of Agronomy 76: 95-106.

Smith, S.E., Read, D.J., 2010. Mycorrhizal Symbiosis. Academic Press, 787p.

Sulpice, R., Ishihara, H., Schlereth, A., Cawthray, G.R., Encke, B., Giavalisco, P., Ivakov, A., Arrivault, S., Jost, R., Krohn, N., Kuo, J., aliberté, E., Pearse, S.J., Raven, J.A., Scheible, W.R., Teste, F., Veneklaas, E.J., Stitt, M., Lambers, H., 2014. Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus‐use efficiency of Proteaceae species. Plant, Cell & Environment 37(6): 1276-1298.

Thornton, M.K., Novy, R.G., Stark, J.C., 2014. Improving phosphorus use efficiency in the future. American Journal of Potato Research 91(2): 175-179.

Valle, S.R., Pinochet, D., Calderini, D.F., 2011. Uptake and use efficiency of N, P, K, Ca and Al by Al-sensitive and Al-tolerant cultivars of wheat under a wide range of soil Al concentrations. Field Crops Research 121(3): 392-400.

Van de Wiel, C.C.M., van der Linden, C.G., Scholten, O.E., 2016. Improving phosphorus use efficiency in agriculture: opportunities for breeding. Euphytica 207(1): 1-22.

Wang, X., Shen, J., Liao, H., 2010. Acquisition or utilization, which is more critical for enhancing phosphorus efficiency in modern crops?. Plant Science 179(4): 302-306.

White, P.J., Veneklaas, E.J., 2012. Nature and nurture: the importance of seed phosphorus content. Plant and Soil 357(1): 1-8.

White, P.J., George, T.S., Gregory, P.J., Bengough, A.G., Hallett, P.D., McKenzie, B.M., 2013. Matching roots to their environment. Annals of Botany 112(2): 207-222.

Yang, H., Chen, R., Chen, Y., Li, H., Wei, T., Xie, W. and Fan, G., 2022. Agronomic and physiological traits associated with genetic improvement of phosphorus use efficiency of wheat grown in a purple lithomorphic soil. The Crop Journal 10(4): 1151-1164.

Yaseen, M., Malhi, S.S., 2009a. Variation in yield, phosphorus uptake, and physiological efficiency of wheat genotypes at adequate and stress phosphorus levels in soil. Communications in Soil Science and Plant Analysis 40(19-20): 3104-3120.

Yaseen, M., Malhi, S.S., 2009b. Differential growth performance of 15 wheat genotypes for grain yield and phosphorus uptake on a low phosphorus soil without and with applied phosphorus fertilizer. Journal of Plant Nutrition 32(6): 1015-1043.

Abstract

Phosphorus (P) use efficiency is crucial for sustainable wheat production, particularly on alkaline calcareous soils. This study investigates the relative importance of two factors; P acquisition efficiency (PAE) and P utilization efficiency (PUtE), in determining P use efficiency (PUE) in wheat. A field trial with ten wheat genotypes was conducted under two P levels (no P application and P application at 110 kg P2O5 ha−1). Results revealed significant genetic variability in PUE, PAE, and PUtE among wheat genotypes under varying P availabilities. Genotypes MK-4 and MK-8 exhibited superior PUE, making them ideal candidates for soils with differing P levels. PAE played a more substantial role in influencing PUE, with PUtE contributing less to the variability. The findings underscore the importance of improving PAE, particularly for wheat genotypes grown in P-deficient conditions. Moreover, selecting genotypes with lower grain P concentration can enhance PUtE, contributing to improved PUE. These insights can improve breeding efforts and crop management practices to enhance P use efficiency in wheat, ultimately reducing production costs and fertilizer demand, especially in P-limited alkaline calcareous soils.

Keywords: Alkaline-calcareous soil, P acquisition efficiency, P utilization efficiency, P use efficiency, wheat genotypes.

References

Abbas, M., Irfan, M., Shah, J.A., 2018a. Differential performance of wheat genotypes for grain yield, phosphorus uptake and utilization at low and high phosphorus: Evaluation of PUE in wheat genotypes. Proceedings of the Pakistan Academy of Sciences: B. Life and Environmental Sciences 55(2): 55-64.

Abbas, M., Shah, J.A., Irfan, M., Memon, M.Y., 2018b. Remobilization and utilization of phosphorus in wheat cultivars under induced phosphorus deficiency. Journal of Plant Nutrition 41(12): 1522-1533.

Amtmann, A., Armengaud, P., 2009. Effects of N, P, K and S on metabolism: new knowledge gained from multi-level analysis. Current Opinion in Plant Biology 12(3): 275-283.

Baker, A., Ceasar, S.A., Palmer, A.J., Paterson, J.B., Qi, W., Muench, S.P., Baldwin, S.A., 2015. Replace, reuse, recycle: improving the sustainable use of phosphorus by plants. Journal of Experimental Botany 66(12): 3523-3540.

Bayuelo-Jiménez, J.S., Ochoa-Cadavid, I., 2014. Phosphorus acquisition and internal utilization efficiency among maize landraces from the central Mexican highlands. Field Crops Research 156: 123-134.

Beebe, S.E., Rojas‐Pierce, M., Yan, X., Blair, M.W., Pedraza, F., Munoz, F., Tohme, J., Lynch, J.P., 2006. Quantitative trait loci for root architecture traits correlated with phosphorus acquisition in common bean. Crop Science 46(1): 413-423.

Byrne, S.L., Foito, A., Hedley, P.E., Morris, J.A., Stewart, D., Barth, S., 2011. Early response mechanisms of perennial ryegrass (Lolium perenne) to phosphorus deficiency. Annals of Botany 107(2): 243-254.

Chapman, H.D., Pratt, F.P., 1961. Ammonium vandate-molybdate method for determination of phosphorus. In: Methods of analysis for soils, plants and waters. Division of Agricultural Sciences, University of California, pp. 184-203.

Cordell, D., Drangert, J.O., White, S., 2009. The story of phosphorus: global food security and food for thought. Global Environmental Change 19(2): 292-305.

Gemenet, D.C., Hash, C.T., Sanogo, M.D., Sy, O., Zangre, R.G., Leiser, W.L., Haussmann, B.I., 2015. Phosphorus uptake and utilization efficiency in West African pearl millet inbred lines. Field Crops Research 171: 54-66.

Gill, H.S., Singh, A., Sethi, S.K., Behl, R.K., 2004. Phosphorus uptake and use efficiency in different varieties of bread wheat (Triticum aestivum L). Archives of Agronomy and Soil Science 50(6): 563-572.

Gomez, K.A., Gomez, A.A., 1984. Statistical procedures for agricultural research. John Wiley & Sons, New York. 657p.

Government of Pakistan, 2022. Pakistan Economic Survey 2021-22. Ministry of Finance, Islamabad, Pakistan.

Irfan, M., Abbas, M., Shah, J.A. and Memon, M.Y., 2018. Internal and external phosphorus requirements for optimum grain yield are associated with P-utilization efficiency of wheat cultivars. Communications in Soil Science and Plant Analysis 49(22): 2843-2853.

Karthikeyan, A.S., Jain, A., Nagarajan, V.K., Sinilal, B., Sahi, S.V., Raghothama, K.G., 2014. Arabidopsis thaliana mutant lpsi reveals impairment in the root responses to local phosphate availability. Plant Physiology and Biochemistry 77: 60-72.

Kochian, L.V., 2012. Rooting for more phosphorus. Nature 488(7412): 466-467.

Korkmaz, K., İbrikçi, H., Karnez, E., Buyuk, G., Ryan, J., Ulger, A.C., Oguz, H., 2009. Phosphorus use efficiency of wheat genotypes grown in calcareous soils. Journal of Plant Nutrition 32(12): 2094-2106.

Lambers, H., Cawthray, G.R., Giavalisco, P., Kuo, J., Laliberté, E., Pearse, S.J., Scheible, W.R., Stitt, M., Teste, F., Turner, B.L., 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 Phytologist 196(4): 1098-1108.

Liu, H., Shi, Z., Ma, F., Xu, Y., Han, G., Zhang, J., Liu, D., An, D., 2022. Identification and validation of plant height, spike length and spike compactness loci in common wheat (Triticum aestivum L.). BMC Plant Biology 22(1): 568.

Manschadi, A.M., Kaul, H.P., Vollmann, J., Eitzinger, J., Wenzel, W., 2014. Developing phosphorus-efficient crop varieties - an interdisciplinary research framework. Field Crops Research 162: 87-98.

Manske, G.G.B., Ortiz-Monasterio, J.I., Van Ginkel, M., Gonzalez, R.M., Fischer, R.A., Rajaram, S., Vlek, P.L.G., 2001. Importance of P uptake efficiency versus P utilization for wheat yield in acid and calcareous soils in Mexico. European Journal of Agronomy 14(4): 261-274.

Marschner, H. 2012. Marschner's mineral nutrition of higher plants. 3rd edition. Academic Press, Elsevier. 672p.

McDonald, G., Bovill, W., Taylor, J., Wheeler, R., 2015. Responses to phosphorus among wheat genotypes. Crop and Pasture Science 66(5): 430-444.

Memon, K.S., 2005. Soil & fertilizer phosphorus. In: Soil Science. Bashir, A. Bantel, R., (Eds.). National Book Foundation, Islamabad, Pakistan. pp. 291-316.

Miller, R.O., 1998. Nitric-perchloric acid wet digestion in an open vessel. In: Handbook of reference methods for plant analysis. Kalra, Y.P. (Ed.). CRC Press, Washington D.C., USA. pp. 57-61.

Moll, R.H., Kamprath, E.J., Jackson, W.A., 1982. Analysis and interpretation of factors which contribute to efficiency of nitrogen utilization. Agronomy Journal 74(3): 562-564.

NFDC, 2019-2020. National Fertilizer Development Center (NFDC). Crop Wise Usage of Fertilizer. Ministry of National Food Security and Research, Government of Pakistan, Islamabad. Available at [Access date: 16.08.2023]: http://www.nfdc.gov.pk/

Niu, Y.F., Chai, R.S., Jin, G.L., Wang, H., Tang, C.X., Zhang, Y.S., 2013. Responses of root architecture development to low phosphorus availability: a review. Annals of Botany 112(2): 391-408.

Olsen, S.R., 1954. Estimation of available phosphorus in soils by extraction with sodium bicarbonate, Circular No. 939. US Department of Agriculture, Washington, D.C. USA. 19p.

Panigrahy, M., Rao, D.N., Sarla, N., 2009. Molecular mechanisms in response to phosphate starvation in rice. Biotechnology Advances 27(4): 389-397.

Parentoni, S.N., Souza Júnior, C.L.D., 2008. Phosphorus acquisition and internal utilization efficiency in tropical maize genotypes. Pesquisa Agropecuária Brasileira 43: 893-901.

Rose, T.J. and Wissuwa, M., 2012. Rethinking internal phosphorus utilization efficiency: a new approach is needed to improve PUE in grain crops. Advances in Agronomy 116: 185-217.

Rose, T.J., Rose, M.T., Pariasca-Tanaka, J., Heuer, S., Wissuwa, M., 2011. The frustration with utilization: why have improvements in internal phosphorus utilization efficiency in crops remained so elusive?. Frontiers in Plant Science 2: 73.

Ruark, M.D., Kelling, K.A., Good, L.W., 2014. Environmental concerns of phosphorus management in potato production. American Journal of Potato Research 91(2): 132-144.

Sandaña, P., Pinochet, D., 2014. Grain yield and phosphorus use efficiency of wheat and pea in a high yielding environment. Journal of Soil Science and Plant Nutrition 14(4): 973-986.

Sandaña, P., 2016. Phosphorus uptake and utilization efficiency in response to potato genotype and phosphorus availability. European Journal of Agronomy 76: 95-106.

Smith, S.E., Read, D.J., 2010. Mycorrhizal Symbiosis. Academic Press, 787p.

Sulpice, R., Ishihara, H., Schlereth, A., Cawthray, G.R., Encke, B., Giavalisco, P., Ivakov, A., Arrivault, S., Jost, R., Krohn, N., Kuo, J., aliberté, E., Pearse, S.J., Raven, J.A., Scheible, W.R., Teste, F., Veneklaas, E.J., Stitt, M., Lambers, H., 2014. Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus‐use efficiency of Proteaceae species. Plant, Cell & Environment 37(6): 1276-1298.

Thornton, M.K., Novy, R.G., Stark, J.C., 2014. Improving phosphorus use efficiency in the future. American Journal of Potato Research 91(2): 175-179.

Valle, S.R., Pinochet, D., Calderini, D.F., 2011. Uptake and use efficiency of N, P, K, Ca and Al by Al-sensitive and Al-tolerant cultivars of wheat under a wide range of soil Al concentrations. Field Crops Research 121(3): 392-400.

Van de Wiel, C.C.M., van der Linden, C.G., Scholten, O.E., 2016. Improving phosphorus use efficiency in agriculture: opportunities for breeding. Euphytica 207(1): 1-22.

Wang, X., Shen, J., Liao, H., 2010. Acquisition or utilization, which is more critical for enhancing phosphorus efficiency in modern crops?. Plant Science 179(4): 302-306.

White, P.J., Veneklaas, E.J., 2012. Nature and nurture: the importance of seed phosphorus content. Plant and Soil 357(1): 1-8.

White, P.J., George, T.S., Gregory, P.J., Bengough, A.G., Hallett, P.D., McKenzie, B.M., 2013. Matching roots to their environment. Annals of Botany 112(2): 207-222.

Yang, H., Chen, R., Chen, Y., Li, H., Wei, T., Xie, W. and Fan, G., 2022. Agronomic and physiological traits associated with genetic improvement of phosphorus use efficiency of wheat grown in a purple lithomorphic soil. The Crop Journal 10(4): 1151-1164.

Yaseen, M., Malhi, S.S., 2009a. Variation in yield, phosphorus uptake, and physiological efficiency of wheat genotypes at adequate and stress phosphorus levels in soil. Communications in Soil Science and Plant Analysis 40(19-20): 3104-3120.

Yaseen, M., Malhi, S.S., 2009b. Differential growth performance of 15 wheat genotypes for grain yield and phosphorus uptake on a low phosphorus soil without and with applied phosphorus fertilizer. Journal of Plant Nutrition 32(6): 1015-1043.



Eurasian Journal of Soil Science