Table 1.
Comparison of the effects of microcystins (MCs) and cylindrospermopsin (CYN) on plants at the subcellular level.
| Cell Compartment/Phenomenon | Effects of MCs Including MC Type and Concentration | Effects of CYNs Including CYN Concentration | Mechanisms |
|---|---|---|---|
| Plastids | 5 nM MC-LR a + 30.26 µM ANA/14 d MC-LR containing Microcystis aeruginosa cultures: accumulation of osmiophilic granules in chloroplasts of Vallisneria natans [19,20] | n.d. | Generation of ROS by MC-LR |
| 100 µM MC-LR a isolated chloroplasts of pea, inhibition of vesicle traffic in plastids [21] | PP1/PP2A inhibition | ||
| Cytoskeleton |
MTs: CMT—0.01–40 µM MC-LR a—disruption in Phragmites australis, reorientation in Ceratophyllum demersum PPB—45 µM MC-LR a, short-term exposure—PPB disruption in rice root meristem spindle—0.05–40 µM MC-LR a—disruptions, deformations in Sinapis alba, Vicia faba, P. australis phragmoplast—0.5–40 µM MC-LR a—disruptions in roots of P. australis, V. faba [22,23,24,25,26] |
MTs: CMT—12–96 µM CYN a—reorientation, decrease in their density in P. australis PPB—2.4–24 µM CYN a—double and split PPBs in roots of P. australis, V. faba spindle—2.4–12 µM CYN a—disruptions, deformations of metaphase and anaphase spindle in roots of S. alba and P. australis phragmoplast—1.2–12 µM CYN a—disruptions in roots of P. australis [24,27] |
PP1/PP2A inhibition for MCs; protein synthesis inhibition for CYN |
| MFs—45 µM MC-LR a and MCs short-term treatment: misorientation of cortical MFs in rice roots [28] | MFs: n.d. | PP1/PP2A inhibition? | |
| Mitotic chromatin, mitotic index | 0.5–40 µM MC-LR a-mis-segregation of sister chromatids including lagging chromosomes in telophase/cytokinesis, micronucleus: S. alba, V. faba, P. australis 0.001–0.002 µM MC-LR a and MCs c: chromosome aberrations and micronuclei in Allium cepa roots 1–10 µM MC-LR a: alterations in the timing of metaphase–anaphase transition MCs b—blocking of cells in early mitosis, rice roots [22,23,25,26,29,30,31,32] |
1.2–12 µM CYN a—lagging chromosomes in root tips of P. australis
2.4, 6 µM CYN a—blocking of cells in early mitosis in P. australis roots 12 µM CYN a—delay of mitosis in synchronized V. faba roots 0.24–12 µM CYN a—chromosome breaks in roots of V. faba [24,27,33] |
disruptions in the mitotic MT cytoskeleton; for MCs, hyperphosphorylation of histone H3 related to PP1 (PP2A) inhibition For CYN, inhibition of protein synthesis? |
| MC-LR a—inhibition of mitosis: S. alba (≥10 μM), P. australis (≥0.5 μM); stimulation of mitosis at lower concentrations (1 µM): S. alba, V. faba MC b: stimulation of mitosis, A. cepa roots [23,24,34] |
0.024–0.24 µM CYN a—stimulation and 6–48 µM CYN a—inhibition of mitosis in roots of V. faba [24,29] | probably related to the direct biochemical targets of cyanotoxins | |
| Cell wall | 5–40 µM MC-LR—lignification of cell walls in root cortex and stele of S. alba and P. australis [29,35] | 24–48 µM CYN a—lignification of endodermis and pericycle cells of S. alba roots [24] | non-specific stress reactions? |
| Vacuoles and other endomembranes | MCs b, aggregations of ER and Golgi membranes in rice root cells 1 µM MC-LR a, short-term exposure: vacuole fragmentation, engulfment of plastids in tonoplast-coated vesicles in Arabidopsis hypocotyl cells [8,17] |
n.d. | n.d. for ER/Golgi; PP2A/PP1 inhibition for vacuole fragmentation [28,36] |
| Cell death | 5–100 µM MC-LR a: cotyledon, leaf and/or root necrosis, in Phaseolus vulgaris, S. alba, Brassica napus, P. australis, Ceratophyllum submersum −5–10 µM/2–20 d: CMT reorganization caused crown root formation and radial expansion of cells 1 µM: plasmolysis, swollen chloroplasts and mitochondria with destroyed inner membrane structures in V. natans [23,29,35,37,38,39,40,41,42] |
-root necrosis in P. australis (≥24 μM CYN) and V. faba (2.4–48 μM CYN, but not in S. alba
−12–24 µM/2–20 d: swelling of cells and formation of a callus-like tissue S. alba, P. australis without early formation of aerenchyma [27,29,33] |
generation of ROS induced by MCs and CYN; alterations in nuclease (ssDNase and dsDNase) and protease activities [37,38,39,40,41] |
|
apoptosis/AL-PCD: MC-RR a 60 μM/5 d and ≥1 μM/8 d: TobaccoBY-2 cells, 5 µM/4 d S. alba seedlings: perinuclear chromatin margination, condensation of nuclear chromatin, shrinking, blebbing, fragmentation of nucleus, formation of apoptotic-like bodies, the loss of mitochondrial membrane potential (DWm) 1–2 μM MC-LR a/72 h, autophagosome formation in Arabidopsis hypocotyl cells [24,36,43,44,45] |
In V. faba 12–48 µM/3–6 d CYN a induced nucleus fragmentation, blebbing and chromosomal breaks, and increased the ratio of TUNEL-positive cells in 1.2–48 µM/10 d CYN a treated P. australis and in 0.024–24 µM/4 d CYN a treated S. alba roots, in P. australis chromatin fragmentation was detected as well [24,27,41] |
||
| 50 μM MC-LR a/72–144 h reduced cell viability of TobaccoBY-2 cells (Evans blue, PI, staining) Significantly higher cell death index compared with control meristematic A. cepa root tip cells [31,42,43] |
Abbreviations: CMT—cortical microtubule; MF—microfilament; MT—microtubule; n.d.- no data; PI—propidium-iodide; PPB—preprophase band; ROS—reactive oxygen species. Type of toxin preparations: a commercial; b cyanobacterial extract containing multiple MCs; c MC containing freshwater samples and cyanobacterial extracts.