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Plant Cell Reports

, Volume 35, Issue 10, pp 2181–2195 | Cite as

Nitric oxide–cytokinin interplay influences selenite sensitivity in Arabidopsis

  • Nóra Lehotai
  • Gábor Feigl
  • Ágnes Koós
  • Árpád Molnár
  • Attila Ördög
  • Andrea Pető
  • László Erdei
  • Zsuzsanna Kolbert
Original Article

Abstract

Key message

Selenite oppositely modifies cytokinin and nitric oxide metabolism in Arabidopsis organs. A mutually negative interplay between the molecules exists in selenite-exposed roots; and their overproduction causes selenite insensitivity.

Abstract

Selenium-induced phytotoxicity is accompanied by developmental alterations such as primary root (PR) shortening. Growth changes are provoked by the modulation of hormone status and signalling. Cytokinin (CK) cooperates with the nitric oxide (NO) in many aspects of plant development; however, their interaction under abiotic stress has not been examined. Selenite inhibited the growth of Arabidopsis seedlings and reduced root meristem size through cell division arrest. The CK-dependent pARR5::GUS activity revealed the intensification of CK signalling in the PR tip, which may be partly responsible for the root meristem shortening. The selenite-induced alterations in the in situ expressions of cytokinin oxidases (AtCKX4::GUS, AtCKX5::GUS) are associated with selenite-triggered changes of CK signalling. In wild-type (WT) and NO-deficient nia1nia2 root, selenite led to the diminution of NO content, but CK overproducer ipt-161 and -deficient 35S:CKX2 roots did not show NO decrease. Exogenous NO (S-nitroso-N-acetyl-DL-penicillamine, SNAP) reduced the pARR5::GFP and pTCS::GFP expressions. Roots of the 35S:CKX and cyr1 plants suffered more severe selenite-triggered viability loss than the WT, while in ipt-161 and gsnor1-3 no obvious viability decrease was observed. Exogenous NO ameliorated viability loss, but benzyladenine intensified it. Based on the results, selenite impacts development by oppositely modifying CK signalling and NO level. In the root system, CK signalling intensifies which possibly contributes to the nitrate reductase-independent NO diminution. A mutually negative CK-NO interplay exists in selenite-exposed roots; however, overproduction of both molecules worsens selenite sensing. Hereby, we suggest novel regulatory interplay and role for NO and CK in abiotic stress signalling.

Keywords

Cytokinin Nitric oxide Root growth Selenite 

Notes

Acknowledgments

The NR double mutant nia1nia2 plants were kindly provided by Prof. G. F. E. Scherer (University Hannover, Germany), the gsnor1-3 seeds were donated by Prof. Christian Lindermayr (Helmholtz Zentrum München, Neuherberg, Germany). Seeds of 35S:CKX2 and AtCKX::GUS lines were kindly provided by Prof. Thomas Schmülling and Prof. Thomáš Werner (Freie Universität Berlin, Germany). We thank the SALK Institute for Biological Studies for providing the CYCB1;1::GFP seeds (Dr. Peter Doerner). Special thanks to Dr. Wolfgang Busch for his help and useful advices by carrying out confocal imaging, Bonnie Wohlrab for the valuable technical help, Christian Göschl for the computing work (Gregor Mendel Institute of Molecular Plant Biology, Vienna, Austria) and Dr. Ferhan Ayaydin (Biological Research Centre of the Hungarian Academy of Sciences, Szeged, Hungary) for his support in part of the confocal microscopy work. Prof. Péter Hegyi (I. Department of Internal Medicine, University of Szeged) provided the opportunity for supplemental confocal microscopic experiments and Dr. József Maléth provided excellent technical assistance. Both of their kind help is highly appreciated. Special thanks to Dr. Barnabás Wodala for the proofreading.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Funding

The research was funded by the Hungarian Scientific Research Fund (Grant no. OTKA PD100504) and by the Hungarian Academy of Sciences János Bolyai Fellowship.

Supplementary material

299_2016_2028_MOESM1_ESM.tif (342 kb)
Supplementary Figure 1 Ratios of different microelement (Fe, Mn, B, Cu, Zn, Mo, Ni) concentrations (µg/g dry weight) in the shoot (A and C) and root (B and D) system of control (A and B) and 40 µM selenite-treated (C and D) fourteen-day-old wild-type Arabidopsis. (TIFF 341 kb)
299_2016_2028_MOESM2_ESM.tif (34 kb)
Supplementary Figure 2 Stomatal aperture (µm) on the cotyledons of four-day-old wild-type Arabidopsis treated with 0 or 10 µM sodium selenite. Significant differences according to Student’s t test (total stomatal number = 100, ***P < 0.001) are indicated. (TIFF 33 kb)
299_2016_2028_MOESM3_ESM.tif (713 kb)
Supplementary Figure 3 Primary root tips of four-day-old X-Gluc-stained pARR5::GUS Arabidopsis grown on agar medium supplemented with 0, 0.005, 0.01, 0.05 or 0.1 µM benzyladenine (BA). Bar = 500 µm. (TIFF 713 kb)

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Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of Plant Physiology, Umeå Plant Science CentreUmeå UniversityUmeåSweden
  2. 2.Department of Plant Biology, Faculty of Science and InformaticsUniversity of SzegedSzegedHungary

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