Effects of Phytotoxic Nonenolides, Stagonolide A and Herbarumin I, on Physiological and Biochemical Processes in Leaves and Roots of Sensitive Plants

Phytotoxic macrolides attract attention as prototypes of new herbicides. However, their mechanisms of action (MOA) on plants have not yet been elucidated. This study addresses the effects of two ten-membered lactones, stagonolide A (STA) and herbarumin I (HBI) produced by the fungus Stagonospora cir...

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Autores principales: Tyutereva, Elena V., Dalinova, Anna A., Demchenko, Kirill N., Dmitrieva, Valeriya A., Dubovik, Vsevolod R., Lukinskiy, Yuriy V., Mitina, Galina V., Voitsekhovskaja, Olga V., Berestetskiy, Alexander
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10145764/
https://www.ncbi.nlm.nih.gov/pubmed/37104172
http://dx.doi.org/10.3390/toxins15040234
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author Tyutereva, Elena V.
Dalinova, Anna A.
Demchenko, Kirill N.
Dmitrieva, Valeriya A.
Dubovik, Vsevolod R.
Lukinskiy, Yuriy V.
Mitina, Galina V.
Voitsekhovskaja, Olga V.
Berestetskiy, Alexander
author_facet Tyutereva, Elena V.
Dalinova, Anna A.
Demchenko, Kirill N.
Dmitrieva, Valeriya A.
Dubovik, Vsevolod R.
Lukinskiy, Yuriy V.
Mitina, Galina V.
Voitsekhovskaja, Olga V.
Berestetskiy, Alexander
author_sort Tyutereva, Elena V.
collection PubMed
description Phytotoxic macrolides attract attention as prototypes of new herbicides. However, their mechanisms of action (MOA) on plants have not yet been elucidated. This study addresses the effects of two ten-membered lactones, stagonolide A (STA) and herbarumin I (HBI) produced by the fungus Stagonospora cirsii, on Cirsium arvense, Arabidopsis thaliana and Allium cepa. Bioassay of STA and HBI on punctured leaf discs of C. arvense and A. thaliana was conducted at a concentration of 2 mg/mL to evaluate phenotypic responses, the content of pigments, electrolyte leakage from leaf discs, the level of reactive oxygen species, Hill reaction rate, and the relative rise in chlorophyll a fluorescence. The toxin treatments resulted in necrotic and bleached leaf lesions in the dark and in the light, respectively. In the light, HBI treatment caused the drop of carotenoids content in leaves on both plants. The electrolyte leakage caused by HBI was light-dependent, in contrast with that caused by STA. Both compounds induced light-independent peroxide generation in leaf cells but did not affect photosynthesis 6 h after treatment. STA (10 µg/mL) caused strong disorders in root cells of A. thaliana leading to the complete dissipation of the mitochondrial membrane potential one hour post treatment, as well as DNA fragmentation and disappearance of acidic vesicles in the division zone after 8 h; the effects of HBI (50 µg/mL) were much milder. Furthermore, STA was found to inhibit mitosis but did not affect the cytoskeleton in cells of root tips of A. cepa and C. arvense, respectively. Finally, STA was supposed to inhibit the intracellular vesicular traffic from the endoplasmic reticulum to the Golgi apparatus, thus interfering with mitosis. HBI is likely to have another main MOA, probably inhibiting the biosynthesis of carotenoids.
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spelling pubmed-101457642023-04-29 Effects of Phytotoxic Nonenolides, Stagonolide A and Herbarumin I, on Physiological and Biochemical Processes in Leaves and Roots of Sensitive Plants Tyutereva, Elena V. Dalinova, Anna A. Demchenko, Kirill N. Dmitrieva, Valeriya A. Dubovik, Vsevolod R. Lukinskiy, Yuriy V. Mitina, Galina V. Voitsekhovskaja, Olga V. Berestetskiy, Alexander Toxins (Basel) Article Phytotoxic macrolides attract attention as prototypes of new herbicides. However, their mechanisms of action (MOA) on plants have not yet been elucidated. This study addresses the effects of two ten-membered lactones, stagonolide A (STA) and herbarumin I (HBI) produced by the fungus Stagonospora cirsii, on Cirsium arvense, Arabidopsis thaliana and Allium cepa. Bioassay of STA and HBI on punctured leaf discs of C. arvense and A. thaliana was conducted at a concentration of 2 mg/mL to evaluate phenotypic responses, the content of pigments, electrolyte leakage from leaf discs, the level of reactive oxygen species, Hill reaction rate, and the relative rise in chlorophyll a fluorescence. The toxin treatments resulted in necrotic and bleached leaf lesions in the dark and in the light, respectively. In the light, HBI treatment caused the drop of carotenoids content in leaves on both plants. The electrolyte leakage caused by HBI was light-dependent, in contrast with that caused by STA. Both compounds induced light-independent peroxide generation in leaf cells but did not affect photosynthesis 6 h after treatment. STA (10 µg/mL) caused strong disorders in root cells of A. thaliana leading to the complete dissipation of the mitochondrial membrane potential one hour post treatment, as well as DNA fragmentation and disappearance of acidic vesicles in the division zone after 8 h; the effects of HBI (50 µg/mL) were much milder. Furthermore, STA was found to inhibit mitosis but did not affect the cytoskeleton in cells of root tips of A. cepa and C. arvense, respectively. Finally, STA was supposed to inhibit the intracellular vesicular traffic from the endoplasmic reticulum to the Golgi apparatus, thus interfering with mitosis. HBI is likely to have another main MOA, probably inhibiting the biosynthesis of carotenoids. MDPI 2023-03-23 /pmc/articles/PMC10145764/ /pubmed/37104172 http://dx.doi.org/10.3390/toxins15040234 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Tyutereva, Elena V.
Dalinova, Anna A.
Demchenko, Kirill N.
Dmitrieva, Valeriya A.
Dubovik, Vsevolod R.
Lukinskiy, Yuriy V.
Mitina, Galina V.
Voitsekhovskaja, Olga V.
Berestetskiy, Alexander
Effects of Phytotoxic Nonenolides, Stagonolide A and Herbarumin I, on Physiological and Biochemical Processes in Leaves and Roots of Sensitive Plants
title Effects of Phytotoxic Nonenolides, Stagonolide A and Herbarumin I, on Physiological and Biochemical Processes in Leaves and Roots of Sensitive Plants
title_full Effects of Phytotoxic Nonenolides, Stagonolide A and Herbarumin I, on Physiological and Biochemical Processes in Leaves and Roots of Sensitive Plants
title_fullStr Effects of Phytotoxic Nonenolides, Stagonolide A and Herbarumin I, on Physiological and Biochemical Processes in Leaves and Roots of Sensitive Plants
title_full_unstemmed Effects of Phytotoxic Nonenolides, Stagonolide A and Herbarumin I, on Physiological and Biochemical Processes in Leaves and Roots of Sensitive Plants
title_short Effects of Phytotoxic Nonenolides, Stagonolide A and Herbarumin I, on Physiological and Biochemical Processes in Leaves and Roots of Sensitive Plants
title_sort effects of phytotoxic nonenolides, stagonolide a and herbarumin i, on physiological and biochemical processes in leaves and roots of sensitive plants
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10145764/
https://www.ncbi.nlm.nih.gov/pubmed/37104172
http://dx.doi.org/10.3390/toxins15040234
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