Abstract
To address the question of the role of phytohormones in the growth responses induced by P availability, we compared the effects of low P on the growth of barley plants, and the contents of auxin, cytokinins and abscisic acid (ABA). Comparative study of the changes in growth and hormones’ levels in response to P-starvation showed that relative activation of root growth may be related to the decline in shoot cytokinin content and ABA accumulation in the roots of P-starved (P−) barley plants. The decline in shoot cytokinins is likely to result from the inhibition of the transport of these hormones from roots, and in turn, may contribute to increased distribution of auxins in favor of roots. Reduced root branching detected in our experiments, despite maintenance of root auxins, may be related to an elevated level of either cytokinins or ABA in roots of P− barley plants. Thus, interactions between auxins, cytokinins and ABA are likely to be responsible for the changes in root architecture in P− plants.
Similar content being viewed by others
References
Aibara I, Miwa K (2014) Strategies for optimization of mineral nutrient transport in plants: multilevel regulation of nutrient-dependent dynamics of root architecture and transporter activity. Plant Cell Physiol 55:2027–2036
Arkhipova TN, Veselov SU, Melentiev AI, Martynenko EV, Kudoyarova GR (2005) Ability of bacterium Bacillus subtilis to produce cytokinins and to influence the growth and endogenous hormone content of lettuce plants. Plant Soil 27:201–209
Arkhipova TN, Prinsen E, Veselov SU, Martineko EV, Melentiev AI, Kudoyarova GR (2007) Cytokinin producing bacteria enhances plant growth in drying soil. Plant Soil 292:305–315
Casimiro I, Beeckman T, Graham N, Bhalerao R, Zhang H, Casero P, Sandberg G, Bennett MJ (2003) Dissecting Arabidopsis lateral root development. Trends Plant Sci 8:165–171
Drew MC (1975) Comparison of the effects of a localized supply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot of barley. New Phytol 75:479–490
Hachiya T, Sugiura D, Kojima M, Sato S, Yanagisawa S, Sakakibara H, Terashima I, Noguchi K (2014) High CO2 triggers preferential root growth of Arabidopsis thaliana via two distinct systems under low pH and low N stresses. Plant Cell Physiol 55:269–280
Hammond JP, White PJ (2008) Sucrose transport in the phloem: integrating root responses to phosphorus starvation. J Exp Bot 59:93–109
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
Kudoyarova GR, Korobova AV, Akhiyarova GR, Arkhipova TN, Zaytsev DY, Prinsen E, Egutkin NL, Medvedev SS, Veselov SY (2014) Accumulation of cytokinins in roots and their export to the shoots of durum wheat plants treated with the protonophore carbonyl cyanide m-chlorophenylhydrazone (CCCP). J Exp Bot 65:2287–2294
Kudoyarova GR, Dodd IC, Veselov DS, Rothwell SA, Veselov SY (2015) Common and specific responses to availability of mineral nutrients and water. J Exp Bot 66:2133–2144
Lopez-Bucio J, Hernández-Abreu E, Sánchez-Calderón L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L (2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129:244–256
Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol 156:1041–1049
Martin AC, Del Pozo JC, Iglesias J, Rubio V, Solano R, de la Pena A, Leyva A, Paz-Ares J (2000) Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. Plant J 24:559–568
Moubayidin L, Di Mambro R, Sabatini S (2009) Cytokinin-auxin crosstalk. Trends Plant Sci 14:557–562
Niu YF, Chai RS, Jin GL, Wang H, Tang CX, Zhang YS (2013) Responses of root architecture development to low phosphorous availability: a review. Ann Bot 112:391–408
Park MR, So-Hyeon Baek S-H, Reyes BG, Yun SJ, Hasenstein KH (2012) Transcriptome profiling characterizes phosphate deficiency effects on carbohydrate metabolism in rice leaves. J Plant Physiol 169:193–205
Perez-Torres CA, Lopez-Bucio J, Cruz-Ramırez A, Ibarra-Laclette E, Dharmasiri S, Estelle M, Herrera-Estrella L (2008) Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell 20:3258–3272
Puig J, Pauluzzi G, Guiderdoni E, Gantet P (2012) Regulation of shoot and root development through mutual signalling. Mol Plant 5:974–983
Ribot C, Wang Y, Poirier Y (2008) Expression analyses of three members of the AtPHO1 family reveal differential interactions between signaling pathways involved in phosphate deficiency and the responses to auxin, cytokinin, and abscisic acid. Planta 227:1025–1036
Rubio V, Bustos R, Irigoyen ML, Cardona-Lopez X, Rojas-Triana M, Paz-Ares J (2009) Plant hormones and nutrient signaling. Plant Mol Biol 69:361–373
Saab IN, Sharp RE, Pritchard J, Voetberg GS (1990) Increased endogenous abscisic acid maintains primary root growth and inhibits shoot growth of maize seedlings at low water potentials. Plant Physiol 93:1329–1336
Sanchez-Calderon L, Lopez-Bucio J, Chacon-Lopez A, Cruz-Ramırez A, Nieto-Jacobo F, Dubrovsky JG, Herrera-Estrella L (2005) Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant Cell Physiol 46:174–184
Shen C, Yue R, Yang Y, Zhang L, Sun T et al (2014) OsARF16 is involved in cytokinin-mediated inhibition of phosphate transport and phosphate signaling in rice (Oryza sativa L.). PLoS One 9(11):e112906. doi:10.1371/journal.pone.0112906
Shkolnik-Inbar D, Bar-Zvi D (2010) ABI4 mediates abscisic acid and cytokinin inhibition of lateral root formation by reducing polar auxin transport in Arabidopsis. Plant Cell 22:3560–3573
Talboys PJ, Healey JR, Withers PJA, Jones DL (2014) Phosphate depletion modulates auxin transport in Triticum aestivum leading to altered root branching. J Exp Bot 65:5023–5032
Taussky HH, Shorr E (1953) A microcolorimetric method for the determination of inorganic phosphorus. J Biol Chem 202:675–685
Veselov SU, Kudoyarova GR, Egutkin NL, Gyuli-Zade VG, Mustafina AR, Kof EK (1992) Modified solvent partitioning scheme providing increased specificity and rapidity of immunoassay for indole 3-acetic acid. Physiol Plantar 86:93–96
Veselov SU, Valcke R, Van Onckelen H, Kudoyarova G (1999) Cytokinin content and location in the leaves of the wild-type and transgenic tobacco plants. Russ J Plant Physiol 46:26–33
Vysotskaya LB, Korobova AV, Kudoyarova GR (2008) Abscisic acid accumulation in the roots of nutrient-limited plants: its impact on the differential growth of roots and shoots. J Plant Physiol 165:1274–1279
Vysotskaya LB, Korobova AV, Veselov SY, Dodd IC, Kudoyarova GR (2009) ABA mediation of shoot cytokinin oxidase activity: assessing its impacts on cytokinin status and biomass allocation of nutrient deprived durum wheat. Func Plant Biol 36:66–72
Wang SK, Zhang AN, Sun CD, Xu YX, Chen Y, Yu CL, Qian Q, Jiang D-A, Qi YH (2014) Auxin response factor (OsARF12), a novel regulator for phosphate homeostasis in rice (Oryza sativa). New Phytol 201:91–103
Wang Y-L, Almvik M, Clarke N, Eich-Greatorex S, Ogaard AF, Krogstad T, Lambers H, Clarke JL (2015) Contrasting responses of root morphology and root-exuded organic acids to low phosphorus availability in three important food crops with divergent root traits. AoB Plants 7:plv097
Wilkinson S, Kudoyarova GR, Veselov DS, Arkhipova TN, Davies WJ (2012) Plant hormone interactions: innovative targets for crop breeding and management. J Exp Bot 63:3499–3509
Zhang C, Bousquet A, Harris JM (2014) Abscisic acid and lateral root organ defective/numerous infections and polyphenolics modulate root elongation via reactive oxygen species in Medicago truncatula. Plant Physiol 166:644–658
Acknowledgements
The work was partially supported by the Russian Foundation for Basic Research Grant No. 15-04-04750.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by NA Anjum.
Rights and permissions
About this article
Cite this article
Vysotskaya, L.B., Trekozova, A.W. & Kudoyarova, G.R. Effect of phosphorus starvation on hormone content and growth of barley plants. Acta Physiol Plant 38, 108 (2016). https://doi.org/10.1007/s11738-016-2127-5
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-016-2127-5