Abstract
Microcystins (MCs) are cyanobacterial toxins and potent inhibitors of protein phosphatases 1 (PP1) and 2A (PP2A), which are involved in plant cytoskeleton (microtubules and F-actin) organization. Therefore, studies on the toxicity of cyanobacterial products on plant cells have so far been focused on MCs. In this study, we investigated the effects of extracts from 16 (4 MC-producing and 12 non-MC-producing) cyanobacterial strains from several habitats, on various enzymes (PP1, trypsin, elastase), on the plant cytoskeleton and H2O2 levels in Oryza sativa (rice) root cells. Seedling roots were treated for various time periods (1, 12, and 24 h) with aqueous cyanobacterial extracts and underwent either immunostaining for α-tubulin or staining of F-actin with fluorescent phalloidin. 2,7-dichlorofluorescein diacetate (DCF-DA) staining was performed for H2O2 imaging. The enzyme assays confirmed the bioactivity of the extracts of not only MC-rich (MC+), but also MC-devoid (MC−) extracts, which induced major time-dependent alterations on both components of the plant cytoskeleton. These findings suggest that a broad spectrum of bioactive cyanobacterial compounds, apart from MCs or other known cyanotoxins (such as cylindrospermopsin), can affect plants by disrupting the cytoskeleton.
Highlights
Cyanobacteria are an ancient group of oxygenic photosynthetic prokaryotes, thriving in both aquatic and terrestrial habitats, even under the harshest conditions [1]
In order to preliminarily assess the inhibitory potential of the cyanobacterial extracts used in this study, we examined the inhibition of three enzymes, phosphatases 1 (PP1), trypsin, and elastase, typically included in tests for cyanobacterial toxicity [28,36] (Table 1)
MC+ extracts, and MC− extracts from various non-MC-producing cyanobacterial strains were able to induce alterations in both plant cytoskeletal components, i.e., F-actin and microtubules, in Oryza sativa root cells (Table 2). This is the first report of cyanobacterial extracts, not containing any known cyanotoxins, affecting the plant cytoskeleton
Summary
Cyanobacteria are an ancient group of oxygenic photosynthetic prokaryotes, thriving in both aquatic and terrestrial habitats, even under the harshest conditions [1]. Anabaenopeptins have been experimentally shown to inhibit PP1 activity in vitro [28], raising questions over their ability to induce disruption of the cytoskeleton In her recent review, Janssen [26] underlines the significance of using extracts from cyanobacterial strains as reference, in order to simulate field exposure to cyanopeptides. Rice (Oryza sativa) is an ideal experimental material for such research, due to its importance for food production [33] and the fact that it is usually cultivated in fields flooded with water, potentially containing cyanobacteria and their metabolic products In this context, we carried out an extensive screening of the toxic effects of a variety of MC-rich (MC+) and MC-devoid (MC−) cyanobacterial extracts on rice roots, in order to broaden the data concerning the potential adverse toxic effects of cyanobacteria on plant cells. These observations reveal that cyanobacteria could negatively affect plants through a broad “arsenal” of bioactive compounds
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