Abstract
Aims
Phosphorus (P) export with harvested grains is a key step of the P cycle in agroecosystems. In wheat, the accumulation of P in grains originates from both exogenous and endogenous P sources. We investigated the effects of different post-anthesis P supply on P partitioning and P remobilization in two durum wheat cultivars with contrasting biomass allocation.
Methods
Wheat plants were grown on a complete nutrient solution with sufficient P until anthesis. Thereafter, half of the plants were deprived of P and the other half was maintained on the complete nutrient solution. P uptake, allocation, remobilization, and traits related to yield and grain P were determined.
Results
Modifications of post-anthesis P supply had no effect on grain yield. Grain P concentrations at maturity for deprived P supply ranged from 2.2 to 3.4 mg P g DW− 1. Without P, net P fluxes to grains essentially came from leaves (35%), roots (28%) and stems (17% ). With P, net P fluxes came mainly from post-antheis P uptake.
Conclusions
Our results suggest that when the P nutrition of durum wheat is limited after anthesis, endogenous P remobilization can sustain grain growth with minor yield penalties if the plants are well supplied during vegetative growth.
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References
Allard V, Martre P, Le Gouis J (2013) Genetic variability in biomass allocation to roots in wheat is mainly related to crop tillering dynamics and nitrogen status. Eur J Agron 46:68–76. https://doi.org/10.1016/j.eja.2012.12.004
Batten GD (1992) A review of phosphorus efficiency in wheat. Plant Soil 146(1):163–168. https://doi.org/10.1007/BF00012009
Batten GD, Wardlaw IF (1987) Senescence of the flag leaf and grain yield following late foliar and root applications of phosphate on plants of differing phosphorus status. J Plant Nutr 10(7):735–748. https://doi.org/10.1080/01904168709363605
Batten GD, Wardlaw IF, Aston MJ (1986) Growth and the distribution of phosphorus in wheat developed under various phosphorus and temperature regimes. Aust J Agric Res 37(5):459–469. https://doi.org/10.1071/ar9860459
Cogliatti DH, María GES (1990) Influx and efflux of phosphorus in roots of wheat plants in non-growth-limiting concentrations of phosphorus. J Exp Bot 41(5):601–607. https://doi.org/10.1093/jxb/41.5.601
Colomb B, Debaeke P, Jouany C, Nolot JM (2007) Phosphorus management in low input stockless cropping systems: crop and soil responses to contrasting P regimes in a 36-year experiment in southern France. Eur J Agron 26(2):154–165. https://doi.org/10.1016/j.eja.2006.09.004
Cordell D, White S (2014) Life’s bottleneck: sustaining the world’s phosphorus for a Food secure future. Annu Rev Environ Resour 39(1):161–188. https://doi.org/10.1146/annurev-environ-010213-113300
Deng Y, Teng W, Tong YP, Chen XP, Zou CQ (2018) Phosphorus efficiency mechanisms of two wheat cultivars as affected by a range of phosphorus levels in the field. Front Plant Sci, 9. https://doi.org/10.3389/fpls.2018.01614
Distelfeld A, Avni R, Fischer AM (2014) Senescence, nutrient remobilization, and yield in wheat and barley. J Exp Bot 65(14):3783–3798. https://doi.org/10.1093/jxb/ert477
Engels C, Kirkby E, White P (2012) Chapter 5 - mineral nutrition, yield and source–sink relationships. In: Marschner’s mineral nutrition of higher plants. 3rd edn. Academic Press, San Diego, pp 85–133, DOI https://doi.org/10.1016/B978-0-12-384905-2.00005-4, (to appear in print)
Etienne P, Diquelou S, Prudent M, Salon C, Maillard A, Ourry A (2018) Macro and micronutrient storage in plants and their remobilization when facing scarcity: the case of drought. Agriculture 8(1):14. https://doi.org/10.3390/agriculture8010014
Ferreira MSL, Martre P, Mangavel C, Girousse C, Rosa NN, Samson MF, Morel MH (2012) Physicochemical control of durum wheat grain filling and glutenin polymer assembly under different temperature regimes. J Cereal Sci 56(1):58–66. https://doi.org/10.1016/j.jcs.2011.11.001
González FG, Miralles DJ, Slafer GA (2011) Wheat floret survival as related to pre-anthesis spike growth. J Exp Bot 62(14):4889–4901. https://doi.org/10.1093/jxb/err182
Grant CA, Flaten DN, Tomasiewicz DJ, Sheppard SC (2001) The importance of early season phosphorus nutrition. Can J Plant Sci 81(2):211–224. https://doi.org/10.4141/P00-093
Gregersen PL, Holm PB, Krupinska K (2008) Leaf senescence and nutrient remobilisation in barley and wheat. Plant Biol 10(s1):37–49. https://doi.org/10.1111/j.1438-8677.2008.00114.x
Hammond JP, Broadley MR, White PJ (2004) Genetic responses to phosphorus deficiency. Ann Bot 94(3):323–332. https://doi.org/10.1093/aob/mch156
Iwai T, Takahashi M, Oda K, Terada Y, Yoshida KT (2012) Dynamic changes in the distribution of minerals in relation to phytic acid accumulation during rice seed development. Plant Physiol 160(4):2007–2014. https://doi.org/10.1104/pp.112.206573
Jeong K, Julia CC, Waters DLE, Pantoja O, Wissuwa M, Heuer S, Liu L, Rose TJ (2017) Remobilisation of phosphorus fractions in rice flag leaves during grain filling: implications for photosynthesis and grain yields. PLOS ONE 12(11):e0187521. https://doi.org/10.1371/journal.pone.0187521
Julia C, Wissuwa M, Kretzschmar T, Jeong K, Rose T (2016) Phosphorus uptake, partitioning and redistribution during grain filling in rice. Ann Bot 118(6):1151–1162. https://doi.org/10.1093/aob/mcw164
Maillard A, Diquélou S, Billard V, Laîné P, Garnica M, Prudent M, Garcia-Mina JM, Yvin JC, Ourry A (2015) Leaf mineral nutrient remobilization during leaf senescence and modulation by nutrient deficiency. Front Plant Sci, 6. https://doi.org/10.3389/fpls.2015.00317
Masclaux-Daubresse C, Reisdorf-Cren M, Orsel M (2008) Leaf nitrogen remobilisation for plant development and grain filling. Plant Biol 10(s1):23–36. https://doi.org/10.1111/j.1438-8677.2008.00097.x
Masoni A, Ercoli L, Mariotti M, Arduini I (2007) Post-anthesis accumulation and remobilization of dry matter, nitrogen and phosphorus in durum wheat as affected by soil type. Eur J Agron 26(3):179–186. https://doi.org/10.1016/j.eja.2006.09.006
Ozturk L, Eker S, Torun B, Cakmak I (2005) Variation in phosphorus efficiency among 73 bread and durum wheat genotypes grown in a phosphorus-deficient calcareous soil. Plant Soil 269(1):69–80. https://doi.org/10.1007/s11104-004-0469-z
Pariasca-Tanaka J, Vandamme E, Mori A, Segda Z, Saito K, Rose TJ, Wissuwa M (2015) Does reducing seed-P concentrations affect seedling vigor and grain yield of rice? Plant Soil 392 (1):253–266. https://doi.org/10.1007/s11104-015-2460-2
Peng Z, Li C (2005) Transport and partitioning of phosphorus in wheat as affected by P withdrawal during flag-leaf expansion. Plant Soil 268(1):1–11. https://doi.org/10.1007/s11104-004-0297-1
Perrier F, Yan B, Candaudap F, Pokrovsky OS, Gourdain E, Meleard B, Bussière S, Coriou C, Robert T, Nguyen C, Cornu JY (2016) Variability in grain cadmium concentration among durum wheat cultivars: impact of aboveground biomass partitioning. Plant Soil 404(1):307–320. https://doi.org/10.1007/s11104-016-2847-8
Plénet D, Mollier A, Pellerin S (2000) Growth analysis of maize field crops under phosphorus deficiency. II. Radiation-use efficiency, biomass accumulation and yield components. Plant Soil 224 (2):259–272. https://doi.org/10.1023/A:1004835621371
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna,Austria
Raboy V (1997) Accumulation and storage of phosphate and minerals. In: Cellular and molecular biology of plant seed development, advances in cellular and molecular biology of plants. Springer, Netherlands, pp 441–477, DOI https://doi.org/10.1007/978-94-015-8909-3_12, (to appear in print)
Raboy V (2001) Seeds for a better future: ’low phytate’ grains help to overcome malnutrition and reduce pollution. Trends Plant Sci 6(10):458–462. https://doi.org/10.1016/S1360-1385(01)02104-5
Römer W, Schilling G (1986) Phosphorus requirements of the wheat plant in various stages of its life cycle. Plant Soil 91(2):221–229. https://doi.org/10.1007/BF02181789
Rose TJ, Wissuwa M (2012) Chapter five - Rethinking internal phosphorus utilization efficiency: a new approach is needed to improve PUE in grain crops. In: Advances in agronomy. Academic Press, pp 185–217, DOI https://doi.org/10.1016/B978-0-12-394277-7.00005-1, (to appear in print)
Rose TJ, Rengel Z, Ma Q, Bowden JW (2007) Differential accumulation patterns of phosphorus and potassium by canola cultivars compared to wheat. J Plant Nutr Soil Sci 170(3):404–411. https://doi.org/10.1002/jpln.200625163
Rose T, Liu L, Wissuwa M (2013) Improving phosphorus efficiency in cereal crops: Is breeding for reduced grain phosphorus concentration part of the solution? Front Plant Sci, 4. https://doi.org/10.3389/fpls.2013.00444
Shewry PR, Mitchell RAC, Tosi P, Wan Y, Underwood C, Lovegrove A, Freeman J, Toole GA, Mills ENC, Ward JL (2012) An integrated study of grain development of wheat (cv. Hereward). J Cereal Sci 56(1):21–30. https://doi.org/10.1016/j.jcs.2011.11.007
Snapp SS, Lynch JP (1996) Phosphorus distribution and remobilization in bean plants as influenced by phosphorus nutrition. Crop Sci 36(4):929–935. https://doi.org/10.2135/cropsci1996.0011183X003600040019x
Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418(6898):671. https://doi.org/10.1038/nature01014
Van Veldhoven PP, Mannaerts GP (1987) Inorganic and organic phosphate measurements in the nanomolar range. Anal Biochem 161(1):45–48. https://doi.org/10.1016/0003-2697(87)90649-X
Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. Phytol 157(3):423–447. https://doi.org/10.1046/j.1469-8137.2003.00695.x
Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE, Plaxton WC, Price CA, Scheible WR, Shane MW, White PJ, Raven JA (2012) Opportunities for improving phosphorus-use efficiency in crop plants. Phytol 195(2):306–320. https://doi.org/10.1111/j.1469-8137.2012.04190.x
Villegas D, Aparicio N, Blanco R, Royo C (2001) Biomass accumulation and main stem elongation of Durum Wheat grown under Mediterranean conditions. Ann Bot 88(4):617–627. https://doi.org/10.1006/anbo.2001.1512
Wang X, Shen J, Liao H (2010) Acquisition or utilization, which is more critical for enhancing phosphorus efficiency in modern crops? Plant Sci 179(4):302–306. https://doi.org/10.1016/j.plantsci.2010.06.007
Wang F, Rose T, Jeong K, Kretzschmar T, Wissuwa M (2016) The knowns and unknowns of phosphorus loading into grains, and implications for phosphorus efficiency in cropping systems. J Exp Bot 67(5):1221–1229. https://doi.org/10.1093/jxb/erv517
White PJ, Veneklaas EJ (2012) Nature and nurture: the importance of seed phosphorus content. Plant Soil 357(1–2):1–8. https://doi.org/10.1007/s11104-012-1128-4
Yamaji N, Takemoto Y, Miyaji T, Mitani-Ueno N, Yoshida KT, Ma JF (2017) Reducing phosphorus accumulation in rice grains with an impaired transporter in the node. Nature 541(7635):92–95. https://doi.org/10.1038/nature20610
Acknowledgments
This work has been carried out with financial support from the French National Institute for Agriculture, Food and Environment (INRAE), Bordeaux Sciences Agro and in the framework of the Cluster of Excellence COTE. We thank Mark Bakker for internal revision and valuable comments on the manuscript. The authors are grateful to Jean-Yves Cornu for his help in the experimental set-up and to Sylvie Milin for plant chemical analyses.
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El Mazlouzi, M., Morel, C., Robert, T. et al. Phosphorus uptake and partitioning in two durum wheat cultivars with contrasting biomass allocation as affected by different P supply during grain filling. Plant Soil 449, 179–192 (2020). https://doi.org/10.1007/s11104-020-04444-0
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DOI: https://doi.org/10.1007/s11104-020-04444-0