Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

ABA mediation of shoot cytokinin oxidase activity: assessing its impacts on cytokinin status and biomass allocation of nutrient-deprived durum wheat

Lidia B. Vysotskaya A , Alla V. Korobova A , Stanislav Y. Veselov B , Ian C. Dodd C D and Guzel R. Kudoyarova A

A Institute of Biology, Ufa Research Centre, Russian Academy of Sciences, 450054 Ufa, Russian Federation.

B Department of Biology, Bashkirian State University, Russian Federation.

C The Lancaster Environment Centre, Lancaster University, LA1 4YQ, UK.

D Corresponding author. Email: i.dodd@lancaster.ac.uk

Functional Plant Biology 36(1) 66-72 http://dx.doi.org/10.1071/FP08187
Submitted: 3 July 2008  Accepted: 4 October 2008   Published: 7 January 2009

Abstract

Although nutrient deprivation alters the concentrations of several plant hormones, the role of each in decreasing shoot-to-root ratio is not clear. A 10-fold dilution of the nutrient concentration supplied to hydroponically-grown 7-day-old durum wheat (Triticum turgidum L. ssp. durum Desf.) plants decreased shoot growth, shoot-to-root ratio and shoot and root cytokinin concentrations, increased shoot ABA concentration and shoot cytokinin oxidase activity, but had no effect on xylem sap ABA and cytokinin concentrations. Nutrient deprivation also increased xylem concentrations of conjugated ABA. The role of ABA in these responses was addressed by adding 11.4 µm ABA to the nutrient solution of well fertilised plants, or 1.2 mm fluridone (an inhibitor of ABA biosynthesis) to the nutrient solution of nutrient-deprived plants. The former induced similar changes in shoot-to-root ratio (by inhibiting shoot growth), shoot ABA concentration, shoot and root cytokinin concentrations and shoot cytokinin oxidase activity as nutrient deprivation. Conversely, fluridone addition to nutrient-deprived plants restored shoot-to-root ratio (by inhibiting root growth), shoot ABA concentration, shoot and root cytokinin concentrations to levels similar to well fertilised plants. Although root growth maintenance during nutrient deprivation depends on a threshold ABA concentration, shoot growth inhibition is independent of shoot ABA status. Although fluridone decreased shoot cytokinin oxidase activity of nutrient-deprived plants, it was still 1.7-fold greater than well fertilised plants, implying that nutrient deprivation could also activate shoot cytokinin oxidase independently of ABA. These data question the root signal basis of cytokinin action, but demonstrate that changes in ABA status can regulate shoot cytokinin concentrations via altering their metabolism.

Additional keywords: growth, nutrient deprivation, root-to-shoot signalling.


References

Aloni R Langhans M Aloni E Dreieicher E Ullrich CI 2005 Root-synthesized cytokinin in Arabidopsis is distributed in the shoot by the transpiration stream. Journal of Experimental Botany 56 1535 1544 doi:10.1093/jxb/eri148

Arkhipova TN Prinsen E Veselov SU Martinenko EV Melentiev AI Kudoyarova GR 2007 Cytokinin producing bacteria enhance plant growth in drying soil. Plant and Soil 292 305 315 doi:10.1007/s11104-007-9233-5

Beck EH 1996 Regulation of shoot/root ratio by cytokinins from roots in Urtica dioica: opinion. Plant and Soil 185 1 12 doi:10.1007/BF02257560

Brugiere N Jiao SP Hantke S Zinselmeier C Roessler JA Niu XM Jones RJ Habben JE 2003 Cytokinin oxidase gene expression in maize is localized to the vasculature, and is induced by cytokinins, abscisic acid, and abiotic stress. Plant Physiology 132 1228 1240 doi:10.1104/pp.102.017707

Chapin FS III (1990) Effects of nutrient deficiency on plant growth: evidence for a centralised stress-response system. In ‘Importance of root to shoot communication in the responses to environmental stress’. (Eds WI Davies, B Jeffcoat) pp. 135–148. (British Society for Plant Growth Regulation: Bristol)

Chen C-C Ertl JR Lesiner SM Chang C-C 1985 Localisation of cytokinin biosynthetic sites in pea plants and carrot roots. Plant Physiology 78 510 513

Cherkozianova AV Vysotskaya LB Veselov SY Kudoyarova GR 2005 Hormonal control of the shoot-to-root ratio is not related to water deficiency in wheat plants under mineral deficiency. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 52 629 634
doi:10.1007/s11183-005-0093-7

Davies WJ Kudoyarova G Hartung W 2005 Long-distance ABA signaling and its relation to other signaling pathways in the detection of soil drying and the mediation of the plant’s response to drought. Journal of Plant Growth Regulation 24 285 295 doi:10.1007/s00344-005-0103-1

Dodd IC 2003 Leaf area development of ABA deficient and wild-type peas at two levels of nitrogen supply. Functional Plant Biology 30 777 783 doi:10.1071/FP02227

Dodd IC Munns R Passioura JB 2002 Does shoot water status limit leaf expansion of nitrogen-deprived barley? Journal of Experimental Botany 53 1765 1770 doi:10.1093/jxb/erf030

Dodd IC Tan LP He J 2003 Do increases in xylem sap pH and/or ABA concentration mediate stomatal closure following nitrate deprivation? Journal of Experimental Botany 54 1281 1288 doi:10.1093/jxb/erg122

Dodd IC Ngo C Turnbull CGN Beveridge CA 2004 Effects of nitrogen supply on xylem cytokinin delivery, transpiration and leaf expansion of pea genotypes differing in xylem cytokinin concentration. Functional Plant Biology 31 903 911 doi:10.1071/FP04044

Forde BG 2002 Local and long-range signaling pathways regulating plant responses to nitrate. Annual Review of Plant Biology 53 203 224 doi:10.1146/annurev.arplant.53.100301.135256

Galuszka P Frebortova J Werner T Yamada M Strnad M Schmulling T Frebort I 2004 Cytokinin oxidase/dehydrogenase genes in barley and wheat: cloning and heterologous expression. European Journal of Biochemistry 271 3990 4002 doi:10.1111/j.1432-1033.2004.04334.x

Hare PD van Staden J 1994 Cytokinin oxidase: biochemical features and physiological significance. Physiologia Plantarum 91 128 136 doi:10.1111/j.1399-3054.1994.tb00668.x

Jackson MB 1993 Are plant hormones involved in root to shoot communication? Advances in Botanical Research 19 103 187 doi:10.1016/S0065-2296(08)60204-9

Jackson RB Manwaring JH Caldwell MM 1990 Rapid physiological adjustment of roots to localized soil enrichment. Nature 344 58 60 doi:10.1038/344058a0

Jeschke WD Peuke AD Pate JS Hartung W 1997 Transport, synthesis and catabolism of abscisic acid (ABA) in intact plants of castor bean (Ricinus communis L.) under phosphate deficiency and moderate salinity. Journal of Experimental Botany 48 1737 1747 doi:10.1093/jexbot/48.314.1737

Jiang F Hartung W 2008 Long-distance signalling of abscisic acid (ABA): the factors regulating the intensity of the ABA signal. Journal of Experimental Botany 59 37 43 doi:10.1093/jxb/erm127

Jiang F Veselova S Veselov D Kudoyarova G Jeschke WD Hartung W 2005 Cytokinin flows from Hordeum vulgare to the hemiparasite Rhinanthus minor and the influence of infection on host and parasite cytokinins relations. Functional Plant Biology 32 619 629 doi:10.1071/FP04168

Kudoyarova GR Farhutdinov RG Mitrichenko AN Teplova IR Dedov AV Veselov SU Kulaeva ON 1998 Fast changes in growth rate and cytokinin content of the shoot following rapid cooling of roots of wheat seedling. Plant Growth Regulation 26 105 108 doi:10.1023/A:1006088827358

Kudoyarova GR Vysotskaya LB Cherkozyanova A Dodd IC 2007 Effect of partial rootzone drying on the concentration of zeatin-type cytokinins in tomato (Lycopersicon esculentum Mill.) xylem sap and leaves. Journal of Experimental Botany 58 161 168 doi:10.1093/jxb/erl116

Kuiper D Schuit J Kuiper PJC 1988 Effects of internal and external cytokinin concentrations on root growth and shoot to root ratio of Plantago major ssp. pleiosperma at different nutrient conditions. Plant and Soil 111 231 236 doi:10.1007/BF02139944

Miyawaki K Matsumoto-Kitano M Kakimoto T 2004 Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin and nitrate. The Plant Journal 37 128 138 doi:10.1046/j.1365-313X.2003.01945.x

Munns R Cramer GR 1996 Is coordination of leaf and root growth mediated by abscisic acid? Opinion. Plant and Soil 185 33 40 doi:10.1007/BF02257563

Pierce M Raschke K 1980 Correlation between loss of turgor and accumulation of abscisic acid in detached leaves. Planta 148 174 182 doi:10.1007/BF00386419

Rahayu YS Walch-Liu P Neumann G Romheld V von Wiren N Bangerth F 2005 Root-derived cytokinins as long-distance signals for NO3 - induced stimulation of leaf growth. Journal of Experimental Botany 56 1143 1152 doi:10.1093/jxb/eri107

Sauter A Dietz KJ Hartung W 2002 A possible stress physiological role of abscisic acid conjugates in root-to-shoot signalling. Plant, Cell & Environment 25 223 228 doi:10.1046/j.1365-3040.2002.00747.x

Sharp RE 2002 Interaction with ethylene: changing views on the role of abscisic acid in root and shoot growth responses to water stress. Plant, Cell & Environment 25 211 222 doi:10.1046/j.1365-3040.2002.00798.x

Takei K Sakakibara H Taniguchi M Sugiyama T 2001 Nitrogen-dependent accumulation of cytokinins in root and the translocation to leaf: implication of cytokinin species that induces gene expression of maize response regulator. Plant & Cell Physiology 42 85 93 doi:10.1093/pcp/pce009

Takei K Ueda N Aoki K Kuromori T Hirayama T Shinozaki K Yamaya T Sakakibara H 2004 AtIPT3 is a key determinant of nitrate-dependent cytokinin biosynthesis in Arabidopsis. Plant & Cell Physiology 45 1053 1062 doi:10.1093/pcp/pch119

Vaseva I Todorova D Malbeck J Travnickova A Machackova I 2008 Response of cytokinin pool and cytokinin oxidase/dehydrogenase activity to abscisic acid exhibits organ specificity in peas. Acta Physiologiae Plantarum 30 151 155 doi:10.1007/s11738-007-0103-9

Veselov SYu Kudoyarova GR Egutkin NL Gyuli-Zade VZ Mustafina AR Kof EM 1992 Modified solvent partitioning scheme providing increased specificity and rapidity of immunoassay for indole-3-acetic acid. Physiologia Plantarum 86 93 96 doi:10.1111/j.1399-3054.1992.tb01316.x

Veselov SY Valcke R Van Onckelen H Kudoyarova GR 1999 Cytokinin content and location in the leaves of the wild-type and transgenic tobacco plants. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 46 26 31

Veselova SV Farhutdinov RG Veselov SYu Kudoyarova GR Veselov DS Hartung W 2005 The effect of root cooling on hormone content, leaf conductance and root hydraulic conductivity of durum wheat seedlings (Triticum durum L.). Journal of Plant Physiology 162 21 26
doi:10.1016/j.jplph.2004.06.001

Vysotskaya LB Timergalina LN Simonyan MV Veselov SY Kudoyarova GR 2001 Growth rate, IAA and cytokinin content of wheat seedling after root pruning. Plant Growth Regulation 33 51 57 doi:10.1023/A:1010700617829

Vysotskaya LB Kudoyarova GR Veselov S Jones HG 2004 Unusual stomatal behaviour on partial root excision in wheat seedlings. Plant, Cell & Environment 27 69 77 doi:10.1046/j.0016-8025.2003.01126.x

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. Journal of Plant Physiology 165 1274 1279 doi:10.1016/j.jplph.2007.08.014

Werner T Motyka V Strnad M Schmülling T 2001 Regulation of plant growth by cytokinin. Proceedings of the National Academy of Sciences of the United States of America 98 10487 10492 doi:10.1073/pnas.171304098

Werner T Motyka V Laucou V Smets R Van Onckelen H Schmülling T 2003 Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. The Plant Cell 15 2532 2550 doi:10.1105/tpc.014928



Export Citation Cited By (14)