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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

The levels of peroxisomal catalase protein and activity modulate the onset of cell death in tobacco BY-2 cells via reactive oxygen species levels and autophagy

Elena V. Tyutereva A , Ksenia S. Dobryakova A , Andreas Schiermeyer B , Maria F. Shishova C , Katharina Pawlowski D , Vadim Demidchik A E , Sigrun Reumann F G H and Olga V. Voitsekhovskaja A F I
+ Author Affiliations
- Author Affiliations

A Laboratory of Molecular and Ecological Physiology, Komarov Botanical Institute, Russian Academy of Sciences, ul. Professora Popova 2, 197376 Saint Petersburg, Russia.

B Fraunhofer Institute for Molecular Biology and Applied Ecology IME, Department of Plant Biotechnology, Forckenbeckstrasse 6, D-52074 Aachen, Germany.

C Department of Physiology and Biochemistry of Plants, Saint Petersburg State University, Universitetskaya em., 7/9, 199034 Saint Petersburg, Russia.

D Department of Ecology, Environment and Plant Sciences, Stockholm University, 106 91 Stockholm, Sweden.

E Department of Plant Cell Biology and Bioengineering, Belarusian State University, Independence Avenue 4, 220030 Minsk, Belarus.

F Department of Plant Biochemistry, Albrecht-von-Haller-Institute for Plant Sciences, Georg-August-University of Goettingen, Justus-von-Liebig Weg 11, D-37077, Goettingen, Germany.

G Faculty of Science and Technology, Centre for Organelle Research (CORE), University of Stavanger, N-4036 Stavanger, Norway.

H Plant Biochemistry and Infection Biology, Universität Hamburg, D-22609 Hamburg, Germany.

I Corresponding author. Email: ovoitse@binran.ru

This paper originates from a presentation at the Fourth International Symposium on Plant Signaling and Behavior, Komarov Botanical Institute RAS/Russian Science Foundation, Saint Petersburg, Russia, 1923 June 2016.

Functional Plant Biology 45(2) 247-258 https://doi.org/10.1071/FP16418
Submitted: 28 November 2016  Accepted: 3 April 2017   Published: 17 May 2017

Abstract

In plant cells, peroxisomes participate in the metabolism of reactive oxygen species (ROS). One of the major regulators of cellular ROS levels – catalase (CAT) – occurs exclusively in peroxisomes. CAT activity is required for immunity-triggered autophagic programmed cell death (PCD). Autophagy has been recently demonstrated to represent a route for degradation of peroxisomes in plant cells. In the present study, the dynamics of the cellular peroxisome pool in tobacco BY-2 cell suspension cultures were used to analyse the effects of inhibition of basal autophagy with special attention to CAT activity. Numbers of peroxisomes per cell, levels of CAT protein and activity, cell viability, ROS levels and expression levels of genes encoding components of antioxidant system were analysed upon application of 3-methyladenine (3-MA), an inhibitor of autophagy, and/or aminotriazole (AT), an inhibitor of CAT. When applied separately, 3-MA and AT led to an increase in cell death, but this effect was attenuated by their simultaneous application. The obtained data suggest that both the levels of CAT protein in peroxisomes as well as CAT activity modulate the onset of cell death in tobacco BY-2 cells via ROS levels and autophagy.

Additional keywords: aminotriazole; 3-methyladenine.


References

Bergmeyer HU (1974) ‘Methods of enzymatic analysis.’ (Verlag Chemie Weinheim Academic Press Inc.: New York)

Busch M, Seuter A, Hain R (2002) Functional analysis of the early steps of carotenoid biosynthesis in tobacco. Plant Physiology 128, 439–453.
Functional analysis of the early steps of carotenoid biosynthesis in tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhsVSrurc%3D&md5=472bfcc32b7baa0a707c614f8c3f8c6fCAS |

Carletti G, Nervo G, Cattivelli L (2014) Flavonoids and melanins: a common strategy across two kingdoms. International Journal of Biological Sciences 10, 1159–1170.
Flavonoids and melanins: a common strategy across two kingdoms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhslKjuro%3D&md5=ad93a464b82940e030d19b82a17f3dd5CAS |

del Río LA (2015) ROS and RNS in plant physiology: an overview. Journal of Experimental Botany 66, 2827–2837.
ROS and RNS in plant physiology: an overview.Crossref | GoogleScholarGoogle Scholar |

Demidchik V (2015) Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. Environmental and Experimental Botany 109, 212–228.
Mechanisms of oxidative stress in plants: from classical chemistry to cell biology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlaiur%2FM&md5=f8db8a141307c54edb23849b86ec517bCAS |

Deosaran E, Larsen KB, Hua R, Sargent G, Wang Y, Kim S, Lamark T, Jauregui M, Law K, Lippincott-Schwartz J, Brech A, Johansen T, Kim PK (2013) NBR1 acts as an autophagy receptor for peroxisomes. Journal of Cell Science 126, 939–952.
NBR1 acts as an autophagy receptor for peroxisomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXotFaitbg%3D&md5=0dc5d1bb3795b53ab81b5bb06eb8c6c7CAS |

Farmer LM, Rinaldi MA, Young PG, Danan CH, Burkhart SE, Bartel B (2013) Disrupting autophagy restores peroxisome function to an Arabidopsis lon2 mutant and reveals a role for the LON2 protease in peroxisomal matrix protein degradation. The Plant Cell 25, 4085–4100.
Disrupting autophagy restores peroxisome function to an Arabidopsis lon2 mutant and reveals a role for the LON2 protease in peroxisomal matrix protein degradation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvFOrtrjO&md5=1e98bbed334b64f46ff6caf2c9fd1170CAS |

Goto-Yamada S, Mano S, Nakamori C, Kondo M, Yamawaki R, Kato A, Nishimura M (2014) Chaperone and protease functions of LON protease 2 modulate the peroxisomal transition and degradation with autophagy. Plant & Cell Physiology 55, 482–496.
Chaperone and protease functions of LON protease 2 modulate the peroxisomal transition and degradation with autophagy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXktlKmu74%3D&md5=f87481a50edb94d1af8593a1aa9e33b6CAS |

Hackenberg T, Juul T, Auzina A, Gwiżdż S, Małolepszy A, Van Der Kelen K, Dam S, Bressendorff S, Lorentzen A, Roepstorff P, Nielsen KL, Jørgensen J-E, Hofius D, Van Breusegem F, Petersen M, Andersen SU (2013) Catalase and NO CATALASE ACTIVITY1 promote autophagy-dependent cell death in Arabidopsis. The Plant Cell 25, 4616–4626.
Catalase and NO CATALASE ACTIVITY1 promote autophagy-dependent cell death in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitVOqsrw%3D&md5=995f0228916a0b5ca8014d6fec5612acCAS |

Hu J, Baker A, Bartel B, Linka N, Mullen RT, Reumann S, Zolmanh BK (2012) Plant peroxisomes: biogenesis and function. The Plant Cell 24, 2279–2303.
Plant peroxisomes: biogenesis and function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1Wjs7bJ&md5=c04d66987b2d22acbb8c45e8db862281CAS |

Kim J, Lee H, Lee HN, Kim SH, Shin KD, Chung T (2013) Autophagy-related proteins are required for degradation of peroxisomes in Arabidopsis hypocotyls during seedling growth. The Plant Cell 25, 4956–4966.
Autophagy-related proteins are required for degradation of peroxisomes in Arabidopsis hypocotyls during seedling growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXisFars7s%3D&md5=8d9a2c408f5769bd686d06235aa0c706CAS |

Kliebenstein DJ, Monde RA, Last RL (1998) Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiology 118, 637–650.
Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmslyqtb0%3D&md5=04077bab884c127d97c8ab5c2bfb92f2CAS |

Lichtenthaler HK, Wellburn AR (1983) Determination of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemical Society Transactions 11, 591–592.
Determination of total carotenoids and chlorophylls a and b of leaf extracts in different solvents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXhslSquro%3D&md5=2fef4c1e3267be1d91649785407f4169CAS |

Liu Y, Bassham DC (2012) Autophagy: pathways for self-eating in plant cells. Annual Review of Plant Biology 63, 215–237.
Autophagy: pathways for self-eating in plant cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xos1ams7g%3D&md5=ddbd4b444e0d81bf166c5ea3120372c6CAS |

MacRae E (2007) Extraction of plant RNA. Methods in Molecular Biology 353, 15–24.

Madhusudhan R, Ishikawa T, Sawa Y, Shigeoka S, Shibata H (2003) Characterization of an ascorbate peroxidase in plastids of tobacco BY-2 cells. Physiologia Plantarum 117, 550–557.
Characterization of an ascorbate peroxidase in plastids of tobacco BY-2 cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtlOltbg%3D&md5=ce6dbc7e862e270b2f3b2bce2b03f0bbCAS |

Middelkoop E, Strijland A, Tager JM (1991) Does aminotriazole inhibit import of CAT into peroxisomes by retarding unfolding? FEBS Letters 279, 79–82.
Does aminotriazole inhibit import of CAT into peroxisomes by retarding unfolding?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXhtFOltL4%3D&md5=f8165270657007ffd7e65d5da7703973CAS |

Mizuno M, Tada Y, Uchii K, Kawakami S, Mayama S (2005) CAT and alternative oxidase cooperatively regulate programmed cell death induced by β-glucan elicitor in potato suspension cultures. Planta 220, 849–853.
CAT and alternative oxidase cooperatively regulate programmed cell death induced by β-glucan elicitor in potato suspension cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtl2ltb4%3D&md5=6c2d0b76f0dafd9c4f92a91031126e47CAS |

Petiot A, Ogier-Denis E, Blommaart EF, Meijer AJ, Codogno P (2000) Distinct classes of phosphatidylinositol 3ʹ-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. Journal of Biological Chemistry 275, 992–998.
Distinct classes of phosphatidylinositol 3ʹ-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXntleisQ%3D%3D&md5=41dd0ee012389a4135543a071248598fCAS |

Petrov V, Hille J, Mueller-Roeber B, Gechev TS (2015) ROS-mediated abiotic stress-induced programmed cell death in plants. Frontiers in Plant Science 6, 69
ROS-mediated abiotic stress-induced programmed cell death in plants.Crossref | GoogleScholarGoogle Scholar |

Reumann S, Bartel B (2016) Plant peroxisomes: recent discoveries in functional complexity, organelle homeostasis, and morphological dynamics. Current Opinion in Plant Biology 34, 17–26.
Plant peroxisomes: recent discoveries in functional complexity, organelle homeostasis, and morphological dynamics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xht12jt73I&md5=d11d827dc3c3e71049b63d0fa2ec792eCAS |

Reumann S, Babujee L, Ma C, Wienkoop S, Siemsen T, Antonicelli GE, Rasche N, Lüder F, Weckwerth W, Jahn O (2007) Proteome analysis of Arabidopsis leaf peroxisomes reveals novel targeting peptides, metabolic pathways, and defense mechanisms. The Plant Cell 19, 3170–3193.
Proteome analysis of Arabidopsis leaf peroxisomes reveals novel targeting peptides, metabolic pathways, and defense mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVersLbN&md5=1c2878b5125f65ac02e710306993cb48CAS |

Reumann S, Quan S, Aung K, Yang PF, Manandhar-Shrestha K, Holbrook D, Linka N, Switzenberg R, Wilkerson CG, Weber APM, Olsen LJ, Hu J (2009) In-depth proteome analysis of Arabidopsis leaf peroxisomes combined with in vivo subcellular targeting verification indicates novel metabolic and regulatory functions of peroxisomes. Plant Physiology 150, 125–143.
In-depth proteome analysis of Arabidopsis leaf peroxisomes combined with in vivo subcellular targeting verification indicates novel metabolic and regulatory functions of peroxisomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvFahsro%3D&md5=0227bcb89cbe4de9d1141c8161608a1cCAS |

Sandalio LM, Romero-Puertas MC (2015) Peroxisomes sense and respond to environmental cues by regulating ROS and RNS signalling networks. Annals of Botany 116, 475–485.
Peroxisomes sense and respond to environmental cues by regulating ROS and RNS signalling networks.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2MbivFeqsQ%3D%3D&md5=d7bf1b5fb7176fa1d54972ae1478ae64CAS |

Shibata M, Oikawa K, Yoshimoto K, Kondo M, Mano S, Yamada K, Hayashi M, Sakamoto W, Ohsumi Y, Nishimura M (2013) Highly oxidized peroxisomes are selectively degraded via autophagy in Arabidopsis. The Plant Cell 25, 4967–4983.
Highly oxidized peroxisomes are selectively degraded via autophagy in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXisFars7g%3D&md5=cd0ac4ffd328aba24a15e3f67e58007dCAS |

Suttangkakul A, Li F, Chung T, Vierstra RD (2011) The ATG1/ATG13 protein kinase complex is both a regulator and a target of autophagic recycling in Arabidopsis. The Plant Cell 23, 3761–3779.
The ATG1/ATG13 protein kinase complex is both a regulator and a target of autophagic recycling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1eku7rE&md5=3eeb3277af47c34a5ed6a04450b877bcCAS |

Tada M, Kohno M, Niwano Y (2010) Scavenging or quenching effect of melanin on superoxide anion and singlet oxygen. Journal of Clinical Biochemistry and Nutrition 46, 224–228.
Scavenging or quenching effect of melanin on superoxide anion and singlet oxygen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXovVGjsrY%3D&md5=74ff86f11a0259193429ca69da219119CAS |

Takatsuka C, Inoue Y, Matsuoka K, Moriyasu Y (2004) 3-methyladenine inhibits autophagy in tobacco culture cells under sucrose starvation conditions. Plant & Cell Physiology 45, 265–274.
3-methyladenine inhibits autophagy in tobacco culture cells under sucrose starvation conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXivVChtL4%3D&md5=5dce4e0b7c1fd195cc7828b469805125CAS |

Tolbert N (1980) Microbodies – peroxisomes and glyoxisomes. In ‘The biochemistry of plants’. (Eds PF Stumpf, EE Con). pp. 488–521. (Academic Press: New York)

Ueno N, Nihei S, Miyakawa N, Hirasawa T, Kanekatsu M, Marubashi W, van Doorn WG, Yamada T (2016) Time course of programmed cell death, which included autophagic features, in hybrid tobacco cells expressing hybrid lethality. Plant Cell Reports 35, 2475–2488.
Time course of programmed cell death, which included autophagic features, in hybrid tobacco cells expressing hybrid lethality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsVCmsbrL&md5=1b0ee6eb401c9657a4df1bb621dd97caCAS |

Vanlerberghe GC (2013) Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants. International Journal of Molecular Sciences 14, 6805–6847.
Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlslCnurk%3D&md5=1cd0ebecad875b85af4b034b3ed4942bCAS |

Vanlerberghe GC, McIntosh L (1994) Mitochondrial electron transport regulation of nuclear gene expression. Studies with the alternative oxidase gene of tobacco. Plant Physiology 105, 867–874.
Mitochondrial electron transport regulation of nuclear gene expression. Studies with the alternative oxidase gene of tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlsFSgtbk%3D&md5=ae3b78789f80d6fa231321752ec275e4CAS |

Voitsekhovskaja OV, Schiermeyer A, Reumann S (2014) Plant peroxisomes are degraded by starvation-induced and constitutive autophagy in tobacco BY-2 suspension-cultured cells. Frontiers in Plant Science 5, 629
Plant peroxisomes are degraded by starvation-induced and constitutive autophagy in tobacco BY-2 suspension-cultured cells.Crossref | GoogleScholarGoogle Scholar |

Williams C, Aksam EB, Gunkel K, Veenhuis M, van der Klei IJ (2012) The relevance of the non-canonical PTS1 of peroxisomal CAT. Biochimica et Biophysica Acta 1823, 1133–1141.
The relevance of the non-canonical PTS1 of peroxisomal CAT.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xot12htr0%3D&md5=bcf2d179edc4a305d517246e0f8c2cd3CAS |

Yoshimoto K, Shibata M, Kondo M, Oikawa K, Sato M, Toyooka K, Shirasu K, Nishimura M, Ohsumi Y (2014) Organ-specific quality control of plant peroxisomes is mediated by autophagy. Journal of Cell Science 127, 1161–1168.
Organ-specific quality control of plant peroxisomes is mediated by autophagy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmvFSgtrc%3D&md5=c93d0a9b78df2900dd4344bf29742c3aCAS |

Yu L, Wan F, Dutta S, Welsh S, Liu Z-H, Freundt E, Baehrecke EH, Lenardo M (2006) Autophagic programmed cell death by selective CAT degradation. Proceedings of the National Academy of Sciences of the United States of America 103, 4952–4957.
Autophagic programmed cell death by selective CAT degradation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjsVGls7k%3D&md5=47c4f54203eb23a58f0bd1063ebc0675CAS |

Zhou J, Zhang Y, Qi J, Chi Y, Fan B, Yu J-Q, Chen Z (2014) E3 ubiquitin ligase CHIP and NBR1-mediated selective autophagy protect additively against proteotoxicity in plant stress responses. PLoS Genetics 10, e1004116
E3 ubiquitin ligase CHIP and NBR1-mediated selective autophagy protect additively against proteotoxicity in plant stress responses.Crossref | GoogleScholarGoogle Scholar |

Zientara-Rytter K, Łukomska J, Moniuszko G, Gwozdecki R, Surowiecki P, Lewandowska M, Liszewska F, Wawrzyńska A, Sirko A (2011) Identification and functional analysis of Joka2, a tobacco member of the family of selective autophagy cargo receptors. Autophagy 7, 1145–1158.
Identification and functional analysis of Joka2, a tobacco member of the family of selective autophagy cargo receptors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XisFSnt78%3D&md5=d5e11e5a7d703c35ea29af6183186e25CAS |