Subcellular Alterations Induced by Cyanotoxins in Vascular Plants-A Review

Abstract

Phytotoxicity of cyanobacterial toxins has been confirmed at the subcellular level with consequences on whole plant physiological parameters and thus growth and productivity. Most of the data are available for two groups of these toxins: microcystins (MCs) and cylindrospermopsins (CYNs). Thus, in this review we present a timely survey of subcellular cyanotoxin effects with the main focus on these two cyanotoxins. We provide comparative insights into how peculiar plant cellular structures are affected. We review structural changes and their physiological consequences induced in the plastid system, peculiar plant cytoskeletal organization and chromatin structure, the plant cell wall, the vacuolar system, and in general, endomembrane structures. The cyanotoxins have characteristic dose-and plant genotype-dependent effects on all these structures. Alterations in chloroplast structure will influence the efficiency of photosynthesis and thus plant productivity. Changing of cell wall composition, disruption of the vacuolar membrane (tonoplast) and cytoskeleton, and alterations of chromatin structure (including DNA strand breaks) can ultimately lead to cell death. Finally, we present an integrated view of subcellular alterations. Knowledge on these changes will certainly contribute to a better understanding of cyanotoxin-plant interactions.

Keywords: cell death; cell wall; chromatin; cyanotoxin; cylindrospermopsin; cytoskeleton; microcystin; plastid; vacuole.

Figure 1

The chemical structure of MC-LR (a) and CYN (b).

Figure 2

Characteristic subcellular alterations induced by MC-LR and CYN. Panels (a–c) etc. refer to distinct subcellular features; toxin treatments are presented alongside with controls (ctr). (a) Phragmites australis roots, control cells present normal cortical microtubules (CMTs), while two day-treatments with 20 µM MC-LR induce depolymerization of CMTs and radial swelling of cells. (b) 10 µM CYN induces the formation of double preprophase bands (PPBs) in P. australis roots. (c) Long-term treatments with high (≥5 µM) concentrations of both MC-LR and CYN induce the formation of lagging chromosomes during cytokinesis and in general, mis-segregation of sister chromatids (arrowheads) in roots of Vicia faba. (d) 40 µM MC-LR induces chromatin condensation in roots of P. australis (upper image), and 10 µM MC-LR induces the formation of numerous nuclear fragments in roots of V. faba. Control nuclei are from roots of P. australis. (e) Phloroglucinol-HCl labels lignin purple. Only walls of xylem cells are labeled in control Sinapis alba roots, while 5 µM MC-LR induces uniform labeling of endodermal cell walls (arrowheads), and 10 µM CYN induces cell wall lignification in the whole stele. The inhibition of xylem differentiation by MC-LR and cell swelling in pith tissue by CYN are noteworthy. (f) Vacuolar systems of young Arabidopsis hypocotyl cells shown by tonoplast labeling with the fluorescent dye CACAIN and chloroplast autofluorescence (pink pseudo-coloring). Controls show vacuoles of different sizes, while 4-h treatment with 5 µM MC-LR induces strong fragmentation of vacuoles. (g) TEM images of young Arabidopsis hypocotyl cells. 24-h treatment with 2 µM MC-LR induces the formation of osmiophilic granules (og) in chloroplasts (cp) and the formation of autophagosome-like structures (ap). This latter structure is boxed and shown in detail (image on the right) to show its double-membrane envelope and many membrane vesicles inside. vac-vacuole. Scalebars: 50 µm (a,e), 10 µm (b,d,f), 5 µm (c,g). Microscopic images collected by L. Székvölgyi (a/ctr), J. Roszik (b), C. Máthé (a/MC-LR, c,d), M. M-Hamvas (e), Gy. Vereb (f), and K. Bóka (g). These micrographs were not published previously, and all authors agreed to their publication here.

Figure 3

A summary of subcellular effects for microcystins (MCs) and cylindrospermopsin (CYN). Physiological alterations such as the detailed mechanisms of oxidative damage or inhibition of chloroplast photosynthetic activity are not shown here. CW—cell wall, Cyp450—cytochrome monooxygenase P450, MF—microfilament, mit—mitochondria, MT—microtubule, px—peroxisome, vac—vacuole. Image created with BioRender.com.