Microcystin-LR, a cyanotoxin, modulates division of higher plant chloroplasts through protein phosphatase inhibition and affects cyanobacterial division

Csaba Máthé; Károly Bóka; Zoltán Kónya; Ferenc Erdődi; Gábor Vasas; Csongor Freytag; Tamás Garda

doi:10.1016/j.chemosphere.2024.142125

Microcystin-LR, a cyanotoxin, modulates division of higher plant chloroplasts through protein phosphatase inhibition and affects cyanobacterial division

Chemosphere. 2024 Apr 24:358:142125. doi: 10.1016/j.chemosphere.2024.142125. Online ahead of print.

Authors

Csaba Máthé¹, Károly Bóka², Zoltán Kónya³, Ferenc Erdődi³, Gábor Vasas⁴, Csongor Freytag⁵, Tamás Garda⁶

Affiliations

¹ Plant Cell and Developmental Biology Research Group, Department of Botany, Institute of Biology and Ecology, Faculty of Science and Technology, University of Debrecen, Egyetem ter 1, H-4032, Debrecen, Hungary. Electronic address: mathe.csaba@science.unideb.hu.
² Department of Plant Anatomy, Institute of Biology, Faculty of Science, ELTE Eötvös Loránd University, Pázmány P. s. 1/c, Budapest, H-1117, Hungary.
³ Department of Medical Chemistry, Faculty of Medicine, University of Debrecen, Egyetem ter 1, H-4032, Debrecen, Hungary.
⁴ Plant and Algal Natural Product Research Group, Department of Botany, Institute of Biology and Ecology, Faculty of Science and Technology, University of Debrecen, Egyetem ter 1, H-4032, Debrecen, Hungary; Balaton Limnological Research Institute- HUN-REN, Klebelsberg str. 3, H-8237, Tihany, Hungary.
⁵ Plant Cell and Developmental Biology Research Group, Department of Botany, Institute of Biology and Ecology, Faculty of Science and Technology, University of Debrecen, Egyetem ter 1, H-4032, Debrecen, Hungary; One Health Institute, Faculty of Health Sciences, University of Debrecen, Nagyerdei krt. 98, H-4032, Debrecen, Hungary.
⁶ Plant Cell and Developmental Biology Research Group, Department of Botany, Institute of Biology and Ecology, Faculty of Science and Technology, University of Debrecen, Egyetem ter 1, H-4032, Debrecen, Hungary.

PMID: 38670509
DOI: 10.1016/j.chemosphere.2024.142125

Abstract

Microcystin-LR (MC-LR) is a harmful cyanotoxin that inhibits 1 and 2A serine-threonine protein phosphatases. This study examines the influence of MC-LR on chloroplast division and the underlying mechanisms and consequences in Arabidopsis. MC-LR increased the frequency of dividing chloroplasts in hypocotyls in a time range of 1-96 h. At short-term exposures to MC-LR, small-sized chloroplasts (longitudinal diameters ≤6 μm) were more sensitive to these stimulatory effects, while both small and large chloroplasts showed stimulations at long-term exposure. After 48 h, the cyanotoxin increased the frequency of small-sized chloroplasts, indicating the stimulation of division. MC-LR inhibited protein phosphatases in whole hypocotyls and isolated chloroplasts, while it did not induce oxidative stress. We show for the first time that total cellular phosphatases play important roles in chloroplast division and that particular chloroplast phosphatases may be involved in these processes. Interestingly, MC-LR has a protective effect on cyanobacterial division during methyl-viologen (MV) treatments in Synechococcus PCC6301. MC-LR production has harmful effects on ecosystems and it may have an ancient cell division regulatory role in stressed cyanobacterial cells, the evolutionary ancestors of chloroplasts. We propose that cytoplasmic (eukaryotic) factors also contribute to the relevant effects of MC-LR in plants.

Keywords: Arabidopsis; Chloroplast division/fission; Cyanobacterial division; Microcystin-LR; Protein phosphatase.