Abstract
White lupin (Lupinus albus) exhibits strong root morphological and physiological responses to phosphorus (P) deficiency and auxin treatments, but the interactive effects of P and auxin in regulating root morphological and physiological traits are not fully understood. This study aimed to assess white lupin root traits as influenced by P (0 or 250 μmol L−1) and auxin (10−8 mol L−1 NAA) in nutrient solution. Both P deficiency and auxin treatments significantly altered root morphological traits, as evidenced by reduced taproot length, increased number and density of first-order lateral roots, and enhanced cluster-root formation. Changes in root physiological traits were also observed, i.e., increased proton, citrate, and acid phosphatase exudation. Exogenous auxin enhanced root responses and sensitivity to P deficiency. A significant interplay exists between P and auxin in the regulation of root morphological and physiological traits. Principal component analysis showed that P availability explained 64.8% and auxin addition 21.3% of the total variation in root trait parameters, indicating that P availability is much more important than auxin in modifying root responses of white lupin. This suggests that white lupin can coordinate root morphological and physiological responses to enhance acquisition of P resources, with an optimal trade-off between root morphological and physiological traits regulated by external stimuli such as P availability and auxin.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Holford I C R. Soil phosphorus: its measurement, and its uptake by plant. Aust J Soil Res, 1997, 35: 227–239
Lin W Y, Lin S I, Chiou T J. Molecular regulators of phosphate homeostasis in plants. J Exp Bot, 2009, 60: 1427–1438
Schachtman D P, Reid R J, Ayling S M. Phosphorus uptake by plants: from soil to cell. Plant Physiol, 1998, 116: 447–453
Marschner H. Mineral Nutrition of Higher Plants, 2nd ed. London: Academic Press, 1995
Ligaba A, Shen H, Shibata K, et al. The role of phosphorus in aluminium-induced citrate and malate exudation from rape (Brassica napus). Physiol Plantarum, 2004, 120: 575–584
Vance C P, Uhde-Stone C, Allan D L. Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol, 2003, 157: 423–447
Fransen B, Blijjenberg J, de Kroon H. Root morphological and physiological plasticity of perennial grass species and the exploitation of spatial and temporal heterogeneous nutrient patches. Plant Soil, 1999, 211: 179–189
Ericsson T. Growth and shoot-root ratio of seedlings in relation to nutrient availability. Plant Soil, 1995, 168: 205–214
Hermans C, Hammond J P, White P J, et al. How do plants respond to nutrient shortage by biomass allocation? Trends Plant Sci, 2006, 11: 610–617
Lynch J P, Ho M D. Rhizoeconomics: carbon costs of phosphorus acquisition. Plant Soil, 2005, 269: 45–56
Nielsen K L, Eshel A, Lynch J P. The effect of phosphorus availability on the carbon economy of contrasting common bean (Phaseolus vulgaris L.) genotypes. J Exp Bot, 2001, 52: 329–339
Pang J Y, Ryan M H, Tibbett M, et al. Variation in morphological and physiological parameters in herbaceous perennial legumes in response to phosphorus supply. Plant Soil, 2010, 331: 241–255
Bates T R, Lynch J P. Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ, 1996, 19: 529–538
Zhu J M, Zhang C C, Lynch J P. The utility of phenotypic plasticity of root hair length for phosphorus acquisition. Funct Plant Biol, 2010, 37: 313–322
López-Bucio J, Hernandez-Abreu E, Sanchez-Calderon L, et al. Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol, 2002, 129: 244–256
Casper B B, Jackson R B. Plant competition underground. Annu Rev Ecol Syst, 1997, 28: 545–570
He Y, Liao H, Yan X L. Localized supply of phosphorus induces root morphological and architectural changes of rice in split and stratified soil cultures. Plant Soil, 2003, 248: 247–256
Jing J, Rui Y, Zhang F, et al. Localized application of phosphorus and ammonium improves growth of maize seedlings by stimulating root proliferation and rhizosphere acidification. Field Crop Res, 2010, 119: 355–364
Li H G, Shen J B, Zhang F S, et al. 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-London, 2010, 105: 585–593
Hodge A. The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol, 2004, 162: 9–24
Jackson R B, Manwaring J H, Caldwell M M. Rapid physiological adjustment of roots to localized soil enrichment. Nature, 1990, 344: 58–60
Neumann G, Martinoia E. Cluster roots-an underground adaptation for survival in extreme environments. Trends Plant Sci, 2002, 7: 162–167
Shen H, Chen J H, Wang Z Y, et al. Root plasma membrane H+-ATPase is involved in the adaptation of soybean to phosphorus starvation. J Exp Bot, 2006, 57: 1353–1362
Kouas S, Debez A, Slatni T, et al. Root proliferation, proton efflux, and acid phosphatase activity in common bean (Phaseolus vulgaris) under phosphorus shortage. J Plant Biol, 2009, 52: 395–402
Lamont B B. Structure, ecology and physiology of root clusters-a review. Plant Soil, 2003, 248: 1–19
Hocking P J, Jeffery S. Cluster-root production and organic anion exudation in a group of old-world lupins and a new-world lupin. Plant Soil, 2004, 258: 135–150
Shen J, Li H, Neumann G, et al. 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, 2005, 168: 837–845
Lambers H, Shane M W, Cramer M D, et al. Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot-London, 2006, 98: 693–713
Wang B L, Tang X Y, Cheng L Y, et al. Nitric oxide is involved in phosphorus deficiency-induced cluster-root development and citrate exudation in white lupin. New Phytol, 2010, 187: 1112–1123
Neumann G, Römheld V. Root excretion of carboxylic acids and protons in phosphorus-deficient plants. Plant Soil, 1999, 211: 121–130
Neumann G, Massonneau A, Martinoia E, et al. Physiological adaptations to phosphorus deficiency during proteoid root development in white lupin. Planta, 1999, 208: 373–382
Tomasi N, Kretzschmar T, Espen L, et al. Plasma membrane H+-ATPase-dependent citrate exudation from cluster roots of phosphate-deficient white lupin. Plant Cell Environ, 2009, 32: 465–475
Dinkelaker B, Hengeler C, Marschner H. Distribution and function of proteoid roots and other root clusters. Bot Acta, 1995, 108: 183–200
Pérez-Torres C A, López-Bucio J, Cruz-Ramírez A, et al. Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell, 2008, 20: 3258–3272
Gilbert G A, Knight J D, Vance C P, et al. Proteoid root development of phosphorus deficient lupin is mimicked by auxin and phosphonate. Ann Bot-London, 2000, 85: 921–928
Meng Z B, You X D, Suo D, et al. Root-derived auxin contributes to the phosphorus-deficiency-induced cluster-root formation in white lupin (Lupinus albus). Physiol Plantarum, 2012, doi: 10.1111/j.1399-3054.2012.01715.x
Neumann G, Massonneau A, Langlade N, et al. Physiological aspects of cluster root function and development in phosphorus-deficient white lupin (Lupinus albus L.). Ann Bot-London, 2000, 85: 909–919
Hou X L, Wu P, Jiao F C, et al. Regulation of the expression of OsIPS1 and OsIPS2 in rice via systemic and local Pi signalling and hormones. Plant Cell Environ, 2005, 28: 353–364
Shen C, Wang S, Zhang S, et al. OsARF16, a transcription factor, is required for auxin and phosphate starvation response in rice (Oryza sativa L.). Plant Cell Environ, 2012, 36: 607–620
Rober-Kleber N, Albrechtova J T P, Fleig S, et al. Plasma membrane H+-ATPase is involved in auxin-mediated cell elongation during wheat embryo development. Plant Physiol, 2003, 131: 1302–1312
Hager A. Role of the plasma membrane H+-ATPase in auxin-induced elongation growth: historical and new aspects. J Plant Res, 2003, 116: 483–505
Skene K R. Cluster roots: model experimental tools for key biological problems. J Exp Bot, 2001, 52: 479–485
Johnson J F, Vance C P, Allan D L. Phosphorus deficiency in Lupinus albus-altered lateral root development and enhanced expression of phosphoenolpyruvate carboxylase. Plant Physiol, 1996, 112: 31–41
Tang C, Barton L, Raphael C. Pasture legume species differ in their capacity to acidify soil. Aust J Agr Res, 1998, 49: 53–58
Westerman R L. Soil Testing and Plant Analysis. 3rd ed. Madison: Soil Science Society of America, 1990
Neumann G. 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, 2006
Malamy J E, Ryan K S. Environmental regulation of lateral root initiation in Arabidopsis. Plant Physiol, 2001, 127: 899–909
Williamson L C, Ribrioux S P C P, Fitter A H, et al. Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol, 2001, 126: 875–882
Nacry P, Canivenc G, Muller B, et al. A role for auxin redistribution in the responses of the root system architecture to phosphate starvation in Arabidopsis. Plant Physiol, 2005, 138: 2061–2074
Casimiro I, Marchant A, Bhalerao R P, et al. Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell, 2001, 13: 843–852
Reed R C, Brady S R, Muday G K. Inhibition of auxin movement from the shoot into the root inhibits lateral root development in Arabidopsis. Plant Physiol, 1998, 118: 1369–1378
Katekar G F, Geissler A E. Auxin transport inhibitors. 4. evidence of a common-mode of action for a proposed class of auxin transport inhibitors-the phytotropins. Plant Physiol, 1980, 66: 1190–1195
Gaume A, Machler F, De Leon C, et al. Low-P tolerance by maize (Zea mays L.) genotypes: significance of root growth, and organic acids and acid phosphatase root exudation. Plant Soil, 2001, 228: 253–264
Gilbert G A, Knight J D, Vance C P, et al. Acid phosphatase activity in phosphorus-deficient white lupin roots. Plant Cell Environ, 1999, 22: 801–810
Tang C, Han X Z, Qiao Y F, et al. Phosphorus deficiency does not enhance proton release by roots of soybean [Glycine max (L.) Murr.]. Environ Exp Bot, 2009, 67: 228–234
Tang C, Qiao Y F, Han X Z, et al. Genotypic variation in phosphorus utilisation of soybean [Glycine max (L.) Murr.] grown in various sparingly soluble P sources. Aust J Agr Res, 2007, 58: 443–451
Yang Z M, Sivaguru M, Horst W J, et al. Aluminium tolerance is achieved by exudation of citric acid from roots of soybean (Glycine max). Physiol Plantarum, 2000, 110: 72–77
Ligaba A, Yamaguchi M, Shen H, et al. Phosphorus deficiency enhances plasma membrane H+-ATPase activity and citrate exudation in greater purple lupin (Lupinus pilosus). Funct Plant Biol, 2004, 31: 1075–1083
Yan F, Zhu Y Y, Müller C, et al. Adaptation of H+-pumping and plasma membrane H+-ATPase activity in proteoid roots of white lupin under phosphate deficiency. Plant Physiol, 2002, 129: 50–63
Zandonadi D B, Santos M P, Dobbss L B, et al. Nitric oxide mediates humic acids-induced root development and plasma membrane H+-ATPase activation. Planta, 2010, 231: 1025–1036
Zhu Y Y, Yan F, Zorb C, et al. A link between citrate and proton release by proteoid roots of white lupin (Lupinus albus L.) grown under phosphorus-deficient conditions? Plant Cell Physiol, 2005, 46: 892–901
Zhang W H, Ryan P R, Tyerman S D. Citrate-permeable channels in the plasma membrane of cluster roots from white lupin. Plant Physiol, 2004, 136: 3771–3783
Wang B, Shen J, Zhang W, et al. Citrate exudation from white lupin induced by phosphorus deficiency differs from that induced by aluminum. New Phytol, 2007, 176: 581–589
Thomine S, Lelièvre F, Boufflet M, et al. Anion-channel blockers interfere with auxin responses in dark-grown Arabidopsis hypocotyls. Plant Physiol, 1997, 115: 533–542
Diatloff E, Roberts M, Sanders D, et al. Characterization of anion channels in the plasma membrane of Arabidopsis epidermal root cells and the identification of a citrate-permeable channel induced by phosphate starvation. Plant Physiol, 2004, 136: 4136–4149
Sas L, Rengel Z, Tang C. Excess cation uptake, and extrusion of protons and organic acid anions by Lupinus albus under phosphorus deficiency. Plant Sci, 2001, 160: 1191–1198
Tadano T, Ozawa K, Sakai H, et al. Secretion of acid-phosphatase by the roots of crop plants under phosphorus-deficient conditions and some properties of the enzyme secreted by lupin roots. Plant Soil, 1993, 155: 95–98
Hayes J E, Richardson A E, Simpson R J. Phytase and acid phosphatase activities in extracts from roots of temperate pasture grass and legume seedlings. Aust J Plant Physiol, 1999, 26: 801–809
Novoplansky A. Picking battles wisely: plant behaviour under competition. Plant Cell Environ, 2009, 32: 726–741
Yano K, Kume T. Root morphological plasticity for heterogeneous phosphorus supply in Zea mays L. Plant Prod Sci, 2005, 8: 427–432
Semchenko M, John E A, Hutchings M J. Effects of physical connection and genetic identity of neighbouring ramets on root-placement patterns in two clonal species. New Phytol, 2007, 176: 644–654
Cahill J F, McNickle G G, Haag J J, et al. Plants integrate information about nutrients and neighbors. Science, 2010, 328: 1657–1657
Schwinning S, Weiner J. Mechanisms determining the degree of size asymmetry in competition among plants. Oecologia, 1998, 113: 447–455
Grams T E E, Andersen C P. Competition for resources in trees: physiological versus morphological plasticity. In: Esser K, Lüttge U, Beyschlag E, eds. Progress in Botany. Heidelberg: Springer-Verlag, 2007
Author information
Authors and Affiliations
Corresponding author
Additional information
This article is published with open access at Springerlink.com
Rights and permissions
Open Access This article is distributed under the terms of the Creative Commons Attribution 2.0 International License (https://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
About this article
Cite this article
Tang, H., Shen, J., Zhang, F. et al. Interactive effects of phosphorus deficiency and exogenous auxin on root morphological and physiological traits in white lupin (Lupinus albus L.). Sci. China Life Sci. 56, 313–323 (2013). https://doi.org/10.1007/s11427-013-4461-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11427-013-4461-9