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Oryzalin bodies: in addition to its anti-microtubule properties, the dinitroaniline herbicide oryzalin causes nodulation of the endoplasmic reticulum

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Abstract

Oryzalin is a much-used pre-emergence herbicide which causes microtubules (Mt) to depolymerize. Here, we document that this dinitroaniline herbicide also leads to characteristic changes in the morphology of the endoplasmic reticulum (ER) and Golgi apparatus. These effects, which are reversible upon washing out the herbicide, are already elicited at low concentrations (2 μM) and become most pronounced at 20 μM. For our studies, we have employed roots of Arabidopsis thaliana, tobacco leaf epidermal cells, and BY-2 suspension cultures, all expressing the luminal ER marker GFP::HDEL. In all cell types, the typical cortical network of the ER assumed a pronounced nodulated morphology with increasing oryzalin concentrations. This effect was enhanced through subsequent application of brefeldin A (BFA). Thin sections of Arabidopsis roots observed in the electron microscope revealed the nodules to consist of a mass of anastomosing ER tubules. Oryzalin also caused the cisternae in Golgi stacks to increase in number but reduced their diameter. Oryzalin retarded ER mobility but did not prevent latrunculin B-induced clustering of Golgi stacks on islands of cisternal ER. While the mechanism underlying these changes in endomembranes remains unknown, it is specific for oryzalin since these effects were not elicited with other Mt-depolymerizing herbicides, e.g., trifluralin, amiprophosmethyl, or colchicine.

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Abbreviations

BFA:

brefeldin A

CLSM:

confocal laser scanning microscope

ER:

endoplasmic reticulum

ST-RFP:

sialyl transferase-RFP

TGN:

trans Golgi network

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Acknowledgements

We thank Steffi Gold for technical help in the electron microscopy preparations. We also thank Dr. Christophe Ritzenthaler (IPMB, Strasbourg, France) for supplying us with N. benthamiana plants stably expressing HDEL-GFP, and Drs. John Runions and Chris Hawes (Oxford Brookes University, Oxford, UK) for supplying us with Arabidopsis plants double transformed with ST::mRFP/GFP::HDEL. Financial support of the German Research Council (DFG Grant number Ro440/11-3) is gratefully acknowledged.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Dept. Cell Biology, Heidelberg Institute for Plant Sciences, University of Heidelberg, Heidelberg, Germany

    Markus Langhans, Silke Niemes, Peter Pimpl & David G. Robinson

  2. HIP-Cell Biology, Univ. Heidelberg, Im Neuenheimer Feld 230, 69120, Heidelberg, Germany

    Markus Langhans, Silke Niemes, Peter Pimpl & David G. Robinson

Authors
  1. Markus Langhans
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  2. Silke Niemes
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  3. Peter Pimpl
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  4. David G. Robinson
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Corresponding author

Correspondence to David G. Robinson.

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Fig. S1

Recovery after 1 h oryzalin (10 μM) in N. benthamiana leaf epidermal cells stably expressing GFP-HDEL. A: control, normal ER pattern; B: after oryzalin treatment; C: recovery after 1 h washing out (placing the leaf disk twice onto fresh Murashige-Skoog medium), ER nodules are absent and a typical ER pattern is seen. (GIF 84 kb)

High resolution image file (TIFF 17.4 mb)

S2

Movie sequence corresponding to frames in Fig. 5a (AVI 31.2 mb)

S3

Movie sequence corresponding to frames in Fig. 5b (AVI 15.6 mb)

S4

Movie sequence corresponding to frames in Fig. 5c (AVI 14.4 mb)

S5

Movie sequence corresponding to frames in Fig. 5d (AVI 7.8 mb)

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Langhans, M., Niemes, S., Pimpl, P. et al. Oryzalin bodies: in addition to its anti-microtubule properties, the dinitroaniline herbicide oryzalin causes nodulation of the endoplasmic reticulum. Protoplasma 236, 73–84 (2009). https://doi.org/10.1007/s00709-009-0059-2

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  • DOI: https://doi.org/10.1007/s00709-009-0059-2

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