The effects of microcystin-LR in Oryza sativa root cells: F-actin as a new target of cyanobacterial toxicity

Plant Biol (Stuttg). 2020 Sep;22(5):839-849. doi: 10.1111/plb.13120. Epub 2020 Jun 17.

Abstract

Microcystins are toxins produced by cyanobacteria, notorious for negatively affecting a wide range of living organisms, among which several plant species. Although microtubules are a well-established target of microcystin toxicity, its effect on filamentous actin (F-actin) in plant cells has not yet been studied. Τhe effects of microcystin-LR (MC-LR) and an extract of a microcystin-producing freshwater cyanobacterial strain (Microcystis flos-aquae TAU-MAC 1510) on the cytoskeleton (F-actin and microtubules) of Oryza sativa (rice) root cells were studied with light, confocal, and transmission electron microscopy. Considering the role of F-actin in endomembrane system distribution, the endoplasmic reticulum and the Golgi apparatus in extract-treated cells were also examined. F-actin in both MC-LR- and extract-treated meristematic and differentiating root cells exhibited time-dependent alterations, ranging from disorientation and bundling to the formation of ring-like structures, eventually resulting in a collapse of the F-actin network after longer treatments. Disorganization and eventual depolymerization of microtubules, as well as abnormal chromatin condensation were observed following treatment with the extract, effects which could be attributed to microcystins and other bioactive compounds. Moreover, cell cycle progression was inhibited in extract-treated roots, specifically affecting the mitotic events. As a consequence of F-actin network disorganization, endoplasmic reticulum elements appeared stacked and diminished, while Golgi dictyosomes appeared aggregated. These results support that F-actin is a prominent target of MC-LR, both in pure form and as an extract ingredient. Endomembrane system alterations can also be attributed to the effects of cyanobacterial bioactive compounds (including microcystins) on the F-actin cytoskeleton.

Keywords: Microcystis; Actin filaments; Golgi apparatus; cell cycle; endoplasmic reticulum; rice.

MeSH terms

  • Actins* / metabolism
  • Marine Toxins* / toxicity
  • Microcystins* / toxicity
  • Microcystis / chemistry
  • Oryza* / drug effects
  • Plant Roots / drug effects

Substances

  • Actins
  • Marine Toxins
  • Microcystins
  • cyanoginosin LR

Supplementary concepts

  • Microcystis flos-aquae