Advertisement

Plant Growth Regulation

, Volume 59, Issue 1, pp 27–36 | Cite as

Reactive oxygen species localization in roots of Arabidopsis thaliana seedlings grown under phosphate deficiency

  • Jarosław Tyburski
  • Kamila Dunajska
  • Andrzej Tretyn
Original Paper

Abstract

Arabidopsis plants responding to phosphorus (P) deficiency increase lateral root formation and reduce primary root elongation. In addition the number and length of root hairs increases in response to P deficiency. Here we studied the patterns of radical oxygen species (ROS) in the roots of Arabidopsis seedlings cultured on media supplemented with high or low P concentration. We found that P availability affected ROS distribution in the apical part of roots. If plants were grown on high P medium, ROS were located in the root elongation zone and quiescent centre. At low P ROS were absent in the elongation zone, however, their synthesis was detected in the primary root meristem. The proximal part of roots was characterized by ROS production in the lateral root primordia and in elongation zones of young lateral roots irrespective of P concentration in the medium. On the other hand, plants grown at high or low P differed in the pattern of ROS distribution in older lateral roots. At high P, the elongation zone was the primary site of ROS production. At low P, ROS were not detected in the elongation zone. However, they were present in the proximal part of the lateral root meristem. These results suggest that P deficiency affects ROS distribution in distal parts of Arabidopsis roots. Under P-sufficiency ROS maximum was observed in the elongation zone, under low P, ROS were not synthesized in this segment of the root, however, they were detected in the apical root meristem.

Keywords

Hydrogen peroxide Lateral roots Phosphate availability Superoxide Root growth Root system architecture 

Abbreviations

DCF

2′,7′-Dichlorofluorescein

DCFH

2′,7′-Dichlorodihydrofluorescein

NBT

Nitroblue tetrazolium

QC

Quiescent centre

ROS

Radical oxygen species

Notes

Acknowledgments

This work was financially supported by the Grant of the Rector of Nicolaus Copernicus University (Grant No. 525-B).

References

  1. Bielski BHJ, Shine GG, Bajuk S (1980) Reduction of nitro blue tetrazolium by CO2 and O2 radicals. J Phys Chem 84:830–833. doi: 10.1021/j100445a006 CrossRefGoogle Scholar
  2. Correa-Aragunde N, Graziano M, Chevalier C, Lamattina L (2006) Nitric oxide modulates the expression of cell cycle regulatory genes during lateral root formation in tomato. J Exp Bot 57:581–588. doi: 10.1093/jxb/erj045 PubMedCrossRefGoogle Scholar
  3. Dunand C, Crèvecoeur M, Penel C (2007) Distribution of superoxide and hydrogen peroxide in Arabidopsis thaliana roots and their influence on root development: possible interactions with peroxidases. New Phytol 174:332–341. doi: 10.1111/j.1469-8137.2007.01995.x PubMedCrossRefGoogle Scholar
  4. Foreman J, Demidchik V, Bothwell JHF, Mylona P, Mledema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JDG, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446. doi: 10.1038/nature01485 PubMedCrossRefGoogle Scholar
  5. Fry SC (1998) Oxidative scission of plant cell wall polysaccharides by ascorbate-induced hydroxyl radicals. Biochem J 332:507–515PubMedGoogle Scholar
  6. Gadea J, Conejero V, Vera P (1999) Developmental regulation of a cytosolic ascorbate peroxidases gene from tomato plants. Mol Gen Genet 262:212–219. doi: 10.1007/s004380051077 PubMedCrossRefGoogle Scholar
  7. Green MA, Fry SC (2005) Apoplastic degradation of ascorbate: Novel enzymes and metabolites permeating the cell wall. Plant Biosyst 139:2–7. doi: 10.1080/11263500500056849 Google Scholar
  8. Hammond JP, Broadley MR, White PJ (2004) Genetic responses to phosphorus deficiency. Ann Bot (Lond) 94:323–332. doi: 10.1093/aob/mch156 CrossRefGoogle Scholar
  9. Jiang K, Meng YL, Feldman LJ (2003) Quiescent center formation in maize roots is associated with an auxin-regulated oxidizing environment. Development 130:1429–1438. doi: 10.1242/dev.00359 PubMedCrossRefGoogle Scholar
  10. Joo JH, Bae YS, Lee JS (2001) Role of auxin-induced reactive oxygen species in root gravotropism. Plant Physiol 126:1055–1060. doi: 10.1104/pp.126.3.1055 PubMedCrossRefGoogle Scholar
  11. Lai F, Thacker J, Li Y, Doerner P (2007) Cell division activity determines the magnitude of phosphate starvation responses in Arabidopsis. Plant J 50:545–556. doi: 10.1111/j.1365-313X.2007.03070.x PubMedCrossRefGoogle Scholar
  12. Linkohr BI, Williamson LC, Fitter AH, Leyser HMO (2002) Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. Plant J 29:751–760. doi: 10.1046/j.1365-313X.2002.01251.x PubMedCrossRefGoogle Scholar
  13. Liszkay A, Kenk B, Schopfer P (2003) Evidence for the involvement of cell wall peroxidases in the generation of hydroxyl radicals mediating extension growth. Planta 217:658–667. doi: 10.1007/s00425-003-1028-1 PubMedCrossRefGoogle Scholar
  14. Liszkay A, van der Yalm E, Schopfer P (2004) Production of reactive oxygen intermediates (O2 , H2O2 and OH) by maize roots and their role in wall loosening and elongation growth. Plant Physiol 135:3114–3123. doi: 10.1104/pp.104.044784 CrossRefGoogle Scholar
  15. Lopéz-Bucio J, Hernandez-Abreu E, Sanchez-Calderon L, Nieto-Jacopo 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. doi: 10.1104/pp.010934 PubMedCrossRefGoogle Scholar
  16. López-Bucio J, Hernandez-Abreu E, Sanchez-Calderon L, Perez-Torres A, Rampey RA, Bartel B, Herrera-Estrella L (2005) An auxin transport independent pathway is involved in phosphate stress-induced root architectural alterations in Arabidopsis. Identification of BIG as a mediator of auxin in pericycle cell activation. Plant Physiol 137:681–691. doi: 10.1104/pp.104.049577 Google Scholar
  17. Mellersh DG, Foulds IV, Higgins VJ, Heath MC (2002) H2O2 plays different roles in determining penetration failure in three diverse plant-fungal interactions. Plant J 29:257–268. doi: 10.1046/j.0960-7412.2001.01215.x PubMedCrossRefGoogle Scholar
  18. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15:437–497. doi: 10.1111/j.1399-3054.1962.tb08052.x CrossRefGoogle Scholar
  19. Nacry P, Canivenc G, Muller B, Azmi A, Van Oncelen H, Rossignol M, Doumas P (2005) A role for auxin redistribution in the responses of the root system architecture to phosphate starvation in Arabidopsis. Plant Physiol 138:2061–2074. doi: 10.1104/pp.105.060061 PubMedCrossRefGoogle Scholar
  20. Rodriguez AA, Grunberg KA, Taleisnik EL (2002) Reactive oxygen species in the elongation zone of maize leaves are necessary for leaf extension. Plant Physiol 129:1627–1632. doi: 10.1104/pp.001222 PubMedCrossRefGoogle Scholar
  21. Sánchez-Calderón L, López-Bucio J, Chacón-López A, Gutiérrez-Ortega A, Hernández-Abreu E, Herrera-Estrella L (2005) Characterization of low phosphorus insensitive mutants reveals a crosstalk between low phosphorus-induced determinate root development and the activation of genes involved in the adaptation of Arabidopsis to phosphorus deficiency. Plant Physiol 140:879–889. doi: 10.1104/pp.105.073825 CrossRefGoogle Scholar
  22. Schopfer P, Plachy C, Frahry G (2001) Release of reactive oxygen intermediates (superoxide radicals, hydrogen peroxide and hydroxyl radicals) and peroxidase in germinating radish seeds controlled by light, gibberelin and abscisic acid. Plant Physiol 125:1591–1602. doi: 10.1104/pp.125.4.1591 PubMedCrossRefGoogle Scholar
  23. Shin R, Schachtman DP (2004) Hydrogen peroxide mediates plat root cell response to nutrient deprivation. Proc Natl Acad Sci USA 101:8827–8832. doi: 10.1073/pnas.0401707101 PubMedCrossRefGoogle Scholar
  24. Shin R, Berg RH, Schachtman DP (2005) Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency. Plant Cell Physiol 46:1350–1357. doi: 10.1093/pcp/pci145 PubMedCrossRefGoogle Scholar
  25. Williamson LC, Ribrioux SPCP, Fitter AH, Leyser HMO (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126:875–882. doi: 10.1104/pp.126.2.875 PubMedCrossRefGoogle Scholar
  26. Zhang X, Zhang L, Dong F, Gao J, Galbraith DW, Song C-P (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126:1438–1448. doi: 10.1104/pp.126.4.1438 PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Jarosław Tyburski
    • 1
  • Kamila Dunajska
    • 1
  • Andrzej Tretyn
    • 1
  1. 1.Department of Biotechnology, Institute of General and Molecular BiologyNicolaus Copernicus UniversityToruńPoland

Personalised recommendations