Abstract
Background and aims
Alterations in root growth and rhizosphere processes in maize (Zea mays L.) occur under phosphorus (P) deficiency, but the dynamics of root morphological and physiological modifications with increasing shoot P concentration remain unclear. This study investigated root responses to a wide gradient in shoot P status.
Methods
A range of maize shoot P concentrations (1.0–4.0 mg g−1) was established using controlled pot experiment with eleven rates of P supply from 0 to 1200 mg P kg−1 soil. Root morphology and rhizosphere processes were characterized 28 days after planting.
Results
Maize reached maximum biomass at shoot P concentration of 2.7 mg g−1. Root morphological responses (i.e. total root length, specific root length and proportion of fine roots) showed a strong increasing trend with decreasing shoot P concentration (1.1–1.3 mg g−1), but they decreased when shoot P concentration was extremely low (below 1.1 mg g−1). In contrast, with increasing shoot P concentration, root morphological responses decreased, but root physiological responses (rhizosphere acidification, acid phosphatase activity and carboxylate exudation in the rhizosphere) were enhanced, and no decrease was noted even at high shoot P concentration (4.0 mg g−1) corresponding to excess P supply.
Conclusions
Increasing maize shoot P concentration induced a decrease in root morphological responses and an enhancement in root exudation, with maize response to P deficiency being dependent on root morphological rather than physiological traits.
Similar content being viewed by others
References
Alvey S, Bagayoko M, Neumann G, Buerkert A (2001) Cereal/legume rotations affect chemical properties and biological activities in two west African soils. Plant Soil 231:45–54
Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266
Barrett-Lennard EG, Dracup M, Greenway H (1993) Role of extracellular phosphatases in the phosphorus-nutrition of clover. J Exp Bot 44:1595–1600
Barry D, Miller M (1989) Phosphorus nutritional requirement of maize seedlings for maximum yield. Agron J 81:95–99
Bates TR, Lynch JP (2001) Root hairs confer a competitive advantage under low phosphorus availability. Plant Soil 236:243–250
Bollons HM, Barraclough PB (1999) Assessing the phosphorus status of winter wheat crops: inorganic orthophosphate in whole shoots. J Agr Sci-Cambridge 133:285–295
Braschkat JJ, Randall PJ (2004) Excess cation concentrations in shoots and roots of pasture species of importance in South-Eastern Australia. Aust J Exp Agr 44:883–892
Carvalhais LC, Dennis PG, Fedoseyenko D, Hajirezaei MR, Borriss R, von Wiren N (2011) Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency. J Plant Nutr Soil Sc 174:3–11
Ciereszko I, Szczygla A, Zebrowska E (2011) Phosphate deficiency affects acid phosphatase activity and growth of two wheat varieties. J Plant Nutr 34:815–829
Corrales I, Amenos M, Poschenrieder C, Barcelo J (2007) Phosphorus efficiency and root exudates in two contrasting tropical maize varieties. J Plant Nutr 30:887–900
Deng Y, Chen K, Teng W, Zhan A, Tong Y, Feng G, Cui Z, Zhang F, Chen X (2014) Is the inherent potential of maize roots efficient for soil phosphorus acquisition? PLoS One 9:e90287
Denton MD, Veneklaas EJ, Freimoser FM, Lambers H (2007) Banksia species (Proteaceae) from severely phosphorus-impoverished soils exhibit extreme efficiency in the use and remobilization of phosphorus. Plant Cell Environ 30:1557–1565
Drew MC (1975) Comparison of the effects of localized supply of phosphate, nitrate, ammonium, and potassium on the growth of the seminal root system and shoot of barley. New Phytol 75:479–490
Eissenstat DM (1992) Costs and benefits of constructing roots of small diameter. J Plant Nutr 15:763–782
Faget M, Blossfeld S, von Gillhaussen P, Schurr U, Temperton VM (2013) Disentangling who is who during rhizosphere acidification in root interactions: combining fluorescence with optode techniques. Front Plant Sci 4:392
Fernandez MC, Rubio G (2015) Root morphological traits related to phosphorus-uptake efficiency of soybean, sunflower, and maize. J Plant Nutr Soil Sci 178:807–815
Gaume A, Machler F, De Leon C, Narro L, Frossard E (2001) Low-P tolerance by maize (Zea mays L.) genotypes: significance of root growth, and organic acids and acid phosphatase root exudation. Plant Soil 228:253–264
George T, Gregory P, Robinson J, Buresh R (2002a) Changes in phosphorus concentrations and pH in the rhizosphere of some agroforestry and crop species. Plant Soil 246:65–73
George T, Gregory P, Wood M, Read D, Buresh R (2002b) Phosphatase activity and organic acids in the rhizosphere of potential agroforestry species and maize. Soil Biol Biochem 34:1487–1494
George T, Fransson A-M, Hammond JP, White PJ (2011) Phosphorus nutrition: rhizosphere processes, plant response and adaptations. In: Bünemann E, Oberson A, Frossard E (eds) Phosphorus in action: biological processes in soil phosphorus cycling. Springer Berlin Heidelberg, Berlin
Giehl RFH, Gruber BD, von Wirén N (2014) It’s time to make changes: modulation of root system architecture by nutrient signals. J Exp Bot 65:769–778
Gilbert G, Knight J, Vance C, Allan D (1999) Acid phosphatase activity in phosphorus-deficient white lupin roots. Plant Cell Environ 22:801–810
Hajabbasi M, Schumacher T (1994) Phosphorus effects on root growth and development in two maize genotypes. Plant Soil 158:39–46
Hermans C, Hammond JP, White PJ, Verbruggen N (2006) How do plants respond to nutrient shortage by biomass allocation? Trends Plant Sci 11:610–617
Hill JO, Simpson RJ, Moore AD, Chapman DF (2006) Morphology and response of roots of pasture species to phosphorus and nitrogen nutrition. Plant Soil 286:7–19
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
Hinsinger P, Gobran GR, Gregory PJ, Wenzel WW (2005) Rhizosphere geometry and heterogeneity arising from root-mediated physical and chemical processes. New Phytol 168:293–303
Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162:9–24
Jing J, Rui Y, Zhang F, Rengel Z, Shen J (2010) Localized application of phosphorus and ammonium improves growth of maize seedlings by stimulating root proliferation and rhizosphere acidification. Field Crop Res 119:355–364
Johnson CM, Ulrich A (1959) Analytical methods for use in plant analysis. University of California, Agricultural Experiment Station, Berkeley
Johnston AE, Poulton PR, Fixen PE, Curtin D (2014) Phosphorus: its efficient use in agriculture. Adv Agron 123:177–228
Jones CA (1983) A survey of the variability in tissue nitrogen and phosphorus concentrations in maize and grain-sorghum. Field Crop Res 6:133–147
Jones DL (1998) Organic acids in the rhizosphere - a critical review. Plant Soil 205:25–44
Jones D, Nguyen C, Finlay R (2009) Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant Soil 321:5–33
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, Finnegan PM, Laliberte E, Pearse SJ, Ryan MH, Shane MW, Veneklaas EJ (2011) Update on phosphorus nutrition in Proteaceae. Phosphorus nutrition of proteaceae in severely phosphorus-impoverished soils: are there lessons to be learned for future crops? Plant Physiol 156:1058–1066
Li L, Li SM, Sun JH, Zhou LL, Bao XG, Zhang HG, Zhang FS (2007) Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus-deficient soils. P Natl Acad Sci USA 104:11192–11196
Li H, Shen J, Zhang F, Tang C, Lambers H (2008) Is there a critical level of shoot phosphorus concentration for cluster-root formation in Lupinus albus? Funct Plant Biol 35:328–336
Li H, Shen J, Zhang F, Marschner P, Cawthray G, Rengel Z (2010a) Phosphorus uptake and rhizosphere properties of intercropped and monocropped maize, faba bean, and white lupin in acidic soil. Biol Fertil Soils 46:79–91
Li H, Shen J, Zhang F, Lambers H (2010b) Localized application of soil organic matter shifts distribution of cluster roots of white lupin in the soil profile due to localized release of phosphorus. Ann Bot 105:585–593
Li Y, Niu S, Yu G (2016) Aggravated phosphorus limitation on biomass production under increasing nitrogen loading: a meta-analysis. Glob Chang Biol 22:934–943
Liu Y, Mi GH, Chen FJ, Zhang JH, Zhang FS (2004) Rhizosphere effect and root growth of two maize (Zea mays L.) genotypes with contrasting P efficiency at low P availability. Plant Sci 167:217–223
Liu H, White PJ, Li C (2016) Biomass partitioning and rhizosphere responses of maize and faba bean to phosphorus deficiency. Crop Pasture Sci 67:847–856
Lopez-Arredondo DL, Leyva-Gonzalez MA, Gonzalez-Morales SI, Lopez-Bucio J, Herrera-Estrella L (2014) Phosphate nutrition: improving low-phosphate tolerance in crops. Annu Rev Plant Biol 65:95–123
Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol 156:1041–1049
Lynch JP (2015) Root phenes that reduce the metabolic costs of soil exploration: opportunities for 21st century agriculture. Plant Cell Environ 38:1775–1784
Lyu Y, Tang H, Li H, Zhang F, Rengel Z, Whalley WR, Shen J (2016) Major crop species show differential balance between root morphological and physiological responses to variable phosphorus supply. Front Plant Sci 7. doi:10.3389/fpls.2016.01939
Maistry PM, Muasya AM, Valentine AJ, Chimphango SBM (2014) Increasing nitrogen supply stimulates phosphorus acquisition mechanisms in the fynbos species Aspalathus linearis. Funct Plant Biol 42:52–62
Marschner P (2012) Marschner’s mineral nutrition of higher plants, third edn. Academic Press, Elsevier, New York
Marschner P, Solaiman Z, Rengel Z (2007) Brassica genotypes differ in growth, phosphorus uptake and rhizosphere properties under P-limiting conditions. Soil Biol Biochem 39:87–98
Miguel MA, Postma JA, Lynch JP (2015) Phene synergism between root hair length and basal root growth angle for phosphorus acquisition. Plant Physiol 167:1430–1439
Mollier A, Pellerin S (1999) Maize root system growth and development as influenced by phosphorus deficiency. J Exp Bot 50:487–497
Neumann G (2006) Quantitative determination of acid phosphatase activity in the rhizosphere and on the root surface. In: Luster J, Finlay R (eds) Handbook of methods used in rhizosphere research–online edition. http//www.rhizo.at/handbook
Neumann G, Römheld V (1999) Root excretion of carboxylic acids and protons in phosphorus-deficient plants. Plant Soil 211:121–130
Neumann G, Römheld V (2001) The release of root exudates as affected by the plant physiological status. In: Pinto R, Varanini Z, Nannipieri Z (eds) The rhizosphere: biochemistry and organic substances at the soil-plant interface. Marcel Dekker Inc., New York
Oburger E, Schmidt H (2016) New methods to unravel rhizosphere processes. Trends Plant Sci 21:243–255
Olsen SR, Cole C, Watanabe FS, Dean L (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA Circular 939. U.S. Government Printing Office, Washington, DC
Pang J, Ryan MH, Tibbett M, Cawthray GR, Siddique KHM, Bolland MDA, Denton MD, Lambers H (2009) Variation in morphological and physiological parameters in herbaceous perennial legumes in response to phosphorus supply. Plant Soil 331:241–255
Pearse SJ, Veneklaas EJ, Cawthray G, Bolland MD, Lambers H (2006) Triticum aestivum Shows a greater biomass response to a supply of aluminium phosphate than Lupinus albus, despite releasing fewer carboxylates into the rhizosphere. New Phytol 169:515–524
Pearse SJ, Veneklaas EJ, Cawthray G, Bolland MD, Lambers H (2007) Carboxylate composition of root exudates does not relate consistently to a crop species’ ability to use phosphorus from aluminium, iron or calcium phosphate sources. New Phytol 173:181–190
Plénet D, Etchebest S, Mollier A, Pellerin S (2000) Growth analysis of maize field crops under phosphorus deficiency. Plant Soil 223:119–132
Postma JA, Dathe A, Lynch JP (2014) The optimal lateral root branching density for maize depends on nitrogen and phosphorus availability. Plant Physiol 166:590–602
Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Biol 50:665–693
Rengel Z, Marschner P (2005) Nutrient availability and management in the rhizosphere: exploiting genotypic differences. New Phytol 168:305–312
Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability: update on microbial phosphorus. Plant Physiol 156:989–996
Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339
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
Ryan P, Delhaize E, Jones D (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Biol 52:527–560
Sachay JE, Wallace RL, Johns MA (1991) Phosphate stress response in hydroponically grown maize. Plant Soil 132:85–90
Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116:447–453
Shane MW, De Vos M, De Roock S, Lambers H (2003a) Shoot P status regulates cluster-root growth and citrate exudation in Lupinus albus grown with a divided root system. Plant Cell Environ 26:265–273
Shane MW, De Vos M, de Roock S, Cawthray GR, Lambers H (2003b) Effects of external phosphorus supply on internal phosphorus concentration and the initiation, growth and exudation of cluster roots in Hakea prostrata R. Br. Plant Soil 248:209–219
Shen J, Rengel Z, Tang C, Zhang F (2003) Role of phosphorus nutrition in development of cluster roots and release of carboxylates in soil-grown Lupinus albus. Plant Soil 248:199–206
Shen J, Li H, Neumann G, Zhang F (2005) Nutrient uptake, cluster root formation and exudation of protons and citrate in Lupinus albus as affected by localized supply of phosphorus in a split-root system. Plant Sci 168:837–845
Shen J, Yuan L, Zhang J, Li H, Bai Z, Chen X, Zhang W, Zhang F (2011) Phosphorus dynamics: from soil to plant. Plant Physiol 156:997–1005
Solaiman Z, Marschner P, Wang D, Rengel Z (2007) Growth, P uptake and rhizosphere properties of wheat and canola genotypes in an alkaline soil with low P availability. Biol Fertil Soils 44:143
Spohn M, Kuzyakov Y (2013) Distribution of microbial- and root-derived phosphatase activities in the rhizosphere depending on P availability and C allocation-coupling soil zymography with 14C imaging. Soil Biol Biochem 67:106–113
Spohn M, Carminati A, Kuzyakov Y (2013) Soil zymography - a novel in situ method for mapping distribution of enzyme activity in soil. Soil Biol Biochem 58:275–280
Spohn M, Treichel NS, Cormann M, Schloter M, Fischer D (2015) Distribution of phosphatase activity and various bacterial phyla in the rhizosphere of Hordeum vulgare L. depending on P availability. Soil Biol Biochem 89:44–51
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 358:100–112
Tang C, Han XZ, Qiao YF, Zheng SJ (2009) Phosphorus deficiency does not enhance proton release by roots of soybean [Glycine max (L.) Murr.] Environ Exp Bot 67:228–234
Tang XY, Placella SA, Dayde F, Bernard L, Robin A, Journet EP, Justes E, Hinsinger P (2016) Phosphorus availability and microbial community in the rhizosphere of intercropped cereal and legume along a P-fertilizer gradient. Plant Soil 407:119–134
Tarafdar J, Claassen N (1988) Organic phosphorus compounds as a phosphorus source for higher plants through the activity of phosphatases produced by plant roots and microorganisms. Biol Fertil Soils 5:308–312
Teng W, Deng Y, Chen X, Xu X, Chen R, Lv Y, Zhao Y, Zhao X, He X, Li B, Tong Y, Zhang F, Li Z (2013) Characterization of root response to phosphorus supply from morphology to gene analysis in field-grown wheat. J Exp Bot 64:1403–1411
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
Veneklaas EJ, Stevens T, Cawthray GR, Turner NC, Grigg AM, Lambers H (2003) Chickpea and white lupin rhizosphere carboxylates vary with soil properties and enhance phosphorus uptake. Plant Soil 248:187–197
Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20:5–15
Wang B, Shen J, Zhang W, Zhang F, Neumann G (2007) Citrate exudation from white lupin induced by phosphorus deficiency differs from that induced by aluminum. New Phytol 176:581–589
Wang X, Pearse SJ, Lambers H (2013) Cluster-root formation and carboxylate release in three Lupinus species as dependent on phosphorus supply, internal phosphorus concentration and relative growth rate. Ann Bot 112:1449–1459
Wouterlood M, Cawthray GR, Turner S, Lambers H, Veneklaas EJ (2004a) Rhizosphere carboxylate concentrations of chickpea are affected by genotype and soil type. Plant Soil 261:1–10
Wouterlood M, Cawthray GR, Scanlon TT, Lambers H, Veneklaas EJ (2004b) Carboxylate concentrations in the rhizosphere of lateral roots of chickpea (Cicer arietinum) increase during plant development, but are not correlated with phosphorus status of soil or plants. New Phytol 162:745–753
Wouterlood M, Lambers H, Veneklaas EJ (2005) Plant phosphorus status has a limited influence on the concentration of phosphorus-mobilising carboxylates in the rhizosphere of chickpea. Funct Plant Biol 32:153–159
Yadav R, Tarafdar J (2001) Influence of organic and inorganic phosphorus supply on the maximum secretion of acid phosphatase by plants. Biol Fertil Soils 34:140–143
Yuan ZY, Chen HYH (2012) A global analysis of fine root production as affected by soil nitrogen and phosphorus. P Roy Soc B-Biol Sci 279:3796–3802
Yun SJ, Kaeppler SM (2001) Induction of maize acid phosphatase activities under phosphorus starvation. Plant Soil 237:109–115
Zhang H, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279:407–409
Zhang H, Huang Y, Ye X, Shi L, Xu F (2009) Genotypic differences in phosphorus acquisition and the rhizosphere properties of Brassica napus in response to low phosphorus stress. Plant Soil 320:91–102
Zhang Y, Yu P, Peng Y, Li X, Chen F, Li C (2012) Fine root patterning and balanced inorganic phosphorus distribution in the soil indicate distinctive adaptation of maize plants to phosphorus deficiency. Pedosphere 22:870–877
Zhou LL, Cao J, Zhang FS, Li L (2009) Rhizosphere acidification of faba bean, soybean and maize. Sci Total Environ 407:4356–4362
Zhu J, Lynch JP (2004) The contribution of lateral rooting to phosphorus acquisition efficiency in maize (Zea mays) seedlings. Funct Plant Biol 31:949–958
Zhu J, Kaeppler SM, Lynch JP (2005) Topsoil foraging and phosphorus acquisition efficiency in maize (Zea mays). Funct Plant Biol 32:749
Zhu J, Zhang C, Lynch JP (2010) The utility of phenotypic plasticity of root hair length for phosphorus acquisition. Funct Plant Biol 37:313–322
Zia M, Amin R, Aslam M (1988) Plant tissue concentration and uptake of phosphorus by maize as affected by levels of fertilization. Pak J Agric Res 9:335–338
Zobel RW, Kinraide TB, Baligar VC (2007) Fine root diameters can change in response to changes in nutrient concentrations. Plant Soil 297:243–254
Acknowledgments
This study was supported by the National Natural Science Foundation of China (NSFC) (31330070 and 31210103906), the Innovative Group Grant of the National Natural Science Foundation of China (31421092), and National key research and development program (2016YFE0101100). Support was also provided by Australian Research Council (DP160104434).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Ellis Hoffland.
Rights and permissions
About this article
Cite this article
Wen, Z., Li, H., Shen, J. et al. Maize responds to low shoot P concentration by altering root morphology rather than increasing root exudation. Plant Soil 416, 377–389 (2017). https://doi.org/10.1007/s11104-017-3214-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-017-3214-0