Reactive nitrogen species act as the enhancers of glutathione pool in embryonic axes of apple seeds subjected to accelerated ageing.
Glutathione peroxidase-like
Glutathione reductase
Nitric oxide derivatives
Reactive oxygen species
Redox potential
Journal
Planta
ISSN: 1432-2048
Titre abrégé: Planta
Pays: Germany
ID NLM: 1250576
Informations de publication
Date de publication:
12 Jul 2024
12 Jul 2024
Historique:
received:
21
12
2023
accepted:
22
06
2024
medline:
12
7
2024
pubmed:
12
7
2024
entrez:
12
7
2024
Statut:
epublish
Résumé
Reactive nitrogen species mitigate the deteriorative effect of accelerated seed ageing by affecting the glutathione concentration and activities of GR and GPX-like. The treatment of apple (Malus domestica Borkh.) embryos isolated from accelerated aged seeds with nitric oxide-derived compounds increases their vigour and is linked to the alleviation of the negative effect of excessive oxidation processes. Reduced form of glutathione (GSH) is involved in the maintenance of redox potential. Glutathione peroxidase-like (GPX-like) uses GSH and converts it to oxidised form (GSSG), while glutathione reductase (GR) reduces GSSG into GSH. The aim of this work was to investigate the impact of the short-time NOx treatment of embryos isolated from apple seeds subjected to accelerated ageing on glutathione-related parameters. Apple seeds were subjected to accelerated ageing for 7, 14 or 21 days. Isolated embryos were shortly treated with NOx and cultured for 48 h. During ageing, in the axes of apple embryos, GSH and GSSG levels as well as half-cell reduction potential remained stable, while GR and GPX-like activities decreased. However, the positive effect of NOx in the vigour preservation of embryos isolated from prolonged aged seeds is linked to the increased total glutathione pool, and above all, higher GSH content. Moreover, NOx increased the level of transcripts encoding GPX-like and stimulated enzymatic activity. The obtained results indicate that high seed vigour related to the mode of action of NO and its derivatives is closely linked to the maintenance of higher GSH levels.
Identifiants
pubmed: 38995415
doi: 10.1007/s00425-024-04472-5
pii: 10.1007/s00425-024-04472-5
doi:
Substances chimiques
Glutathione
GAN16C9B8O
Reactive Nitrogen Species
0
Glutathione Reductase
EC 1.8.1.7
Glutathione Peroxidase
EC 1.11.1.9
Nitric Oxide
31C4KY9ESH
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
51Subventions
Organisme : Narodowe Centrum Nauki
ID : 2016/23/B/NZ9/03462
Informations de copyright
© 2024. The Author(s).
Références
Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Suarez S, Doctorovich F, Sobieszczuk-Nowicka E, Bruce King S, Milczarek G, Rębiś T, Gajewska J, Jagodzik P, Żywicki M (2022) Discovery of endogenous nitroxyl as a new redox player in Arabidopsis thaliana. Nat Plants 9:36–44. https://doi.org/10.1038/s41477-022-01301-z
doi: 10.1038/s41477-022-01301-z
pubmed: 36564632
pmcid: 9873566
Bai X, Yang L, Tian M, Chen J, Shi J, Yang Y, Hu X (2011) Nitric oxide enhances desiccation tolerance of recalcitrant Antiaris toxicaria seeds via protein S-nitrosylation and carbonylation. PLoS ONE. https://doi.org/10.1371/journal.pone.0020714
doi: 10.1371/journal.pone.0020714
pubmed: 22216234
pmcid: 3247246
Bailly C (2019) The signalling role of ROS in the regulation of seed germination and dormancy. Biochem J 476:3019–3032. https://doi.org/10.1042/BCJ20190159
doi: 10.1042/BCJ20190159
pubmed: 31657442
Bela K, Horváth E, Gallé Á, Szabados L, Tari I, Csiszár J (2015) Plant glutathione peroxidases: Emerging role of the antioxidant enzymes in plant development and stress responses. J Plant Physiol 176:192–201. https://doi.org/10.1016/j.jplph.2014.12.014
doi: 10.1016/j.jplph.2014.12.014
pubmed: 25638402
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
doi: 10.1016/0003-2697(76)90527-3
pubmed: 942051
Cairns NG, Pasternak M, Wachter A, Cobbett CS, Meyer AJ (2006) Maturation of Arabidopsis seeds is dependent on glutathione biosynthesis within the embryo. Plant Physiol 141:446–455. https://doi.org/10.1104/pp.106.077982
doi: 10.1104/pp.106.077982
pubmed: 16531482
pmcid: 1475471
Chu F (1994) The human glutathione peroxidase genes GPX2, GPX3, and GPX4 map to chromosomes 14, 5, and 19, respectively. Cytogenet Genome Res 66:96–98. https://doi.org/10.1159/000133675
doi: 10.1159/000133675
Ciacka K, Krasuska U, Otulak-Kozieł K, Gniazdowska A (2019) Dormancy removal by cold stratification increases glutathione and S-nitrosoglutathione content in apple seeds. Plant Physiol Biochem 138:112–120. https://doi.org/10.1016/j.plaphy.2019.02.026
doi: 10.1016/j.plaphy.2019.02.026
pubmed: 30861401
Ciacka K, Tymiński M, Gniazdowska A, Krasuska U (2020) Carbonylation of proteins—an element of plant ageing. Planta 252:12. https://doi.org/10.1007/s00425-020-03414-1
doi: 10.1007/s00425-020-03414-1
pubmed: 32613330
pmcid: 7329788
Ciacka K, Tyminski M, Gniazdowska A, Krasuska U (2022a) Cold stratification-induced dormancy removal in apple (Malus domestica Borkh.) seeds is accompanied by an increased glutathione pool in embryonic axes. J Plant Physiol 274:153736. https://doi.org/10.1016/j.jplph.2022.153736
doi: 10.1016/j.jplph.2022.153736
pubmed: 35661472
Ciacka K, Tyminski M, Gniazdowska A, Krasuska U (2022b) Nitric oxide as a remedy against oxidative damages in apple seeds undergoing accelerated ageing. Antioxidants 11:70. https://doi.org/10.3390/antiox11010070
doi: 10.3390/antiox11010070
Ciacka K, Tyminski M, Wal A, Gniazdowska A, Krasuska U (2022c) Nitric oxide–an antidote to seed aging modifies meta-tyrosine content and expression of aging-linked genes in apple embryos. Front Plant Sci 13:2677. https://doi.org/10.3389/FPLS.2022.929245/BIBTEX
doi: 10.3389/FPLS.2022.929245/BIBTEX
Considine MJ, Foyer CH (2021) Oxygen and reactive oxygen species-dependent regulation of plant growth and development. Plant Physiol 186:79–92. https://doi.org/10.1093/plphys/kiaa077
doi: 10.1093/plphys/kiaa077
pubmed: 33793863
Corpas FJ, Alché JD, Barroso JB (2013) Current overview of S-nitrosoglutathione (GSNO) in higher plants. Front Plant Sci 4:126. https://doi.org/10.3389/fpls.2013.00126
doi: 10.3389/fpls.2013.00126
pubmed: 23658557
pmcid: 3647110
Corpas FJ, González-Gordo S, Rodríguez-Ruiz M, Muñoz-Vargas MA, Palma JM (2022) Thiol-based oxidative posttranslational modifications (OxiPTMs) of plant proteins. Plant Cell Physiol 63:889–900. https://doi.org/10.1093/pcp/pcac036
doi: 10.1093/pcp/pcac036
pubmed: 35323963
pmcid: 9282725
Couto N, Wood J, Barber J (2016) The role of glutathione reductase and related enzymes on cellular redox homoeostasis network. Free Radic Biol Med 95:27–42. https://doi.org/10.1016/j.freeradbiomed.2016.02.028
doi: 10.1016/j.freeradbiomed.2016.02.028
pubmed: 26923386
De Vos CHR, Kraak HL, Bino RJ (1994) Ageing of tomato seeds involves glutathione oxidation. Physiol Plant 92:131–139. https://doi.org/10.1111/j.1399-3054.1994.tb06664.x
doi: 10.1111/j.1399-3054.1994.tb06664.x
Dębska K, Krasuska U, Budnicka K, Bogatek R, Gniazdowska A (2013) Dormancy removal of apple seeds by cold stratification is associated with fluctuation in H
doi: 10.1016/j.jplph.2012.11.018
pubmed: 23347818
Diaz-Vivancos P, de Simone A, Kiddle G, Foyer CH (2015) Glutathione: linking cell proliferation to oxidative stress. Free Radic Biol Med 89:1154–1164. https://doi.org/10.1016/j.freeradbiomed.2015.09.023
doi: 10.1016/j.freeradbiomed.2015.09.023
pubmed: 26546102
Drevet J (2000) Glutathione peroxidases expression in the mammalian epididymis and vas deferens. In: Francavilla F, Francavilla S, Forti G (eds) Proceedings of the 1st european congress of andrology. Andrology 2000, Aquila, Italy, pp 427–461
Esterbauer H, Grill D (1978) Seasonal variation of glutathione and glutathione reductase in needles of Picea abies. Plant Physiol 61:119–121. https://doi.org/10.1104/pp.61.1.119
doi: 10.1104/pp.61.1.119
pubmed: 16660223
pmcid: 1091810
Flohé L, Günzler WA (1984) Assays of glutathione peroxidase. Methods Enzymol 105:114–120. https://doi.org/10.1016/S0076-6879(84)05015-1
doi: 10.1016/S0076-6879(84)05015-1
pubmed: 6727659
Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18. https://doi.org/10.1104/pp.110.167569
doi: 10.1104/pp.110.167569
pubmed: 21205630
pmcid: 3075780
Fu LH, Wang XF, Eyal Y, She YM, Donald LJ, Standing KG, Ben-Hayyim G (2002) A selenoprotein in the plant kingdom. J Biol Chem 277:25983–25991. https://doi.org/10.1074/jbc.M202912200
doi: 10.1074/jbc.M202912200
pubmed: 11973339
Gill SS, Anjum NA, Hasanuzzaman M, Gill R, Trivedi DK, Ahmad I, Pereira E, Tuteja N (2013) Glutathione and glutathione reductase: a boon in disguise for plant abiotic stress defense operations. Plant Physiol Biochem 70:204–212. https://doi.org/10.1016/j.plaphy.2013.05.032
doi: 10.1016/j.plaphy.2013.05.032
pubmed: 23792825
Gniazdowska A, Krasuska U, Dębska K, Andryka P, Bogatek R (2010) The beneficial effect of small toxic molecules on dormancy alleviation and germination of apple embryos is due to NO formation. Planta 232:999–1005. https://doi.org/10.1007/s00425-010-1214-x
doi: 10.1007/s00425-010-1214-x
pubmed: 20628761
He Y, Xue H, Li Y, Wang X (2018) Nitric oxide alleviates cell death through protein S-nitrosylation and transcriptional regulation during the ageing of elm seeds. J Exp Bot 69:5141–5155. https://doi.org/10.1093/jxb/ery270
doi: 10.1093/jxb/ery270
pubmed: 30053069
pmcid: 6184755
Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J (2007) QBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8:1–14. https://doi.org/10.1186/GB-2007-8-2-R19
doi: 10.1186/GB-2007-8-2-R19
Herbette S, Lenne C, Leblanc N, Julien J-L, Drevet JR, Roeckel-Drevet P (2002) Two GPX-like proteins from Lycopersicon esculentum and Helianthus annuus are antioxidant enzymes with phospholipid hydroperoxide glutathione peroxidase and thioredoxin peroxidase activities. Eur J Biochem 269:2414–2420. https://doi.org/10.1046/j.1432-1033.2002.02905.x
doi: 10.1046/j.1432-1033.2002.02905.x
pubmed: 11985625
Hughes MN (2008) Chemistry of nitric oxide and related species. In: Poole R (ed) Methods in enzymology. Academic Press, London, pp 3–19
Kranner I (1998) Determination of glutathione, glutathione disulphide and two related enzymes, glutathione reductase and glucose-6-phosphate dehydrogenase, in fungal and plant cells. In: Varma A (ed) Mycorrhiza manual. Springer, Berlin, Heidelberg, pp 227–241
doi: 10.1007/978-3-642-60268-9_15
Kranner I, Birtić S, Anderson KM, Pritchard HW (2006) Glutathione half-cell reduction potential: a universal stress marker and modulator of programmed cell death? Free Radic Biol Med 40:2155–2165. https://doi.org/10.1016/j.freeradbiomed.2006.02.013
doi: 10.1016/j.freeradbiomed.2006.02.013
pubmed: 16785029
Krasuska U, Gniazdowska A (2012) Nitric oxide and hydrogen cyanide as regulating factors of enzymatic antioxidant system in germinating apple embryos. Acta Physiol Plant 34:683–692. https://doi.org/10.1007/s11738-011-0868-8
doi: 10.1007/s11738-011-0868-8
Krasuska U, Ciacka K, Andryka-Dudek P, Bogatek R, Gniazdowska A (2015) “Nitrosative Door” in seed dormancy alleviation and germination. In: Gupta KJ, Igamberdiev AU (eds) Reactive oxygen and nitrogen species signaling and communication in plants, 1st edn. Springer, Cham, pp 215–237
doi: 10.1007/978-3-319-10079-1_11
Krasuska U, Ciacka K, Staszek P, Tyminski M, Wal A, Gniazdowska A (2023) Hormetic action of cyanide: plant gasotransmitter and poison. Phytochem Rev. https://doi.org/10.1007/s11101-023-09904-w
doi: 10.1007/s11101-023-09904-w
Kurek K, Plitta-Michalak B, Ratajczak E (2019) Reactive oxygen species as potential drivers of the seed aging process. Plants 8:174. https://doi.org/10.3390/plants8060174
doi: 10.3390/plants8060174
pubmed: 31207940
pmcid: 6630744
Lewak S (2011) Metabolic control of embryonic dormancy in apple seed: seven decades of research. Acta Physiol Plant 33:1–24. https://doi.org/10.1007/s11738-010-0524-8
doi: 10.1007/s11738-010-0524-8
Mao C, Zhu Y, Cheng H, Yan H, Zhao L, Tang J, Ma X, Mao P (2018) Nitric oxide regulates seedling growth and mitochondrial responses in aged oat seeds. Int J Mol Sci 19:1052. https://doi.org/10.3390/ijms19041052
doi: 10.3390/ijms19041052
pubmed: 29614792
pmcid: 5979601
Mittler R (2017) ROS are good. Trends Plant Sci 22:11–19. https://doi.org/10.1016/j.tplants.2016.08.002
doi: 10.1016/j.tplants.2016.08.002
pubmed: 27666517
Möller MN, Rios N, Trujillo M, Radi R, Denicola A, Alvarez B (2019) Detection and quantification of nitric oxide–derived oxidants in biological systems. J Biol Chem 294:14776–14802. https://doi.org/10.1074/jbc.REV119.006136
doi: 10.1074/jbc.REV119.006136
pubmed: 31409645
pmcid: 6779446
Morscher F, Kranner I, Arc E, Bailly C, Roach T (2015) Glutathione redox state, tocochromanols, fatty acids, antioxidant enzymes and protein carbonylation in sunflower seed embryos associated with after-ripening and ageing. Ann Bot 116:669–678. https://doi.org/10.1093/aob/mcv108
doi: 10.1093/aob/mcv108
pubmed: 26346716
pmcid: 4578002
Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer C (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484. https://doi.org/10.1111/j.1365-3040.2011.02400.x
doi: 10.1111/j.1365-3040.2011.02400.x
pubmed: 21777251
Pei J, Pan X, Wei G, Hua Y (2023) Research progress of glutathione peroxidase family (GPX) in redoxidation. Front Pharmacol 14:1147414. https://doi.org/10.3389/fphar.2023.1147414
doi: 10.3389/fphar.2023.1147414
pubmed: 36937839
pmcid: 10017475
Roach T, Nagel M, Börner A, Eberle C, Kranner I (2018) Changes in tocochromanols and glutathione reveal differences in the mechanisms of seed ageing under seedbank conditions and controlled deterioration in barley. Environ Exp Bot 156:8–15. https://doi.org/10.1016/j.envexpbot.2018.08.027
doi: 10.1016/j.envexpbot.2018.08.027
Rodriguez Milla M, Maurer A, Huete AR, Gustafson JP (2003) Glutathione peroxidase genes in Arabidopsis are ubiquitous and regulated by abiotic stresses through diverse signaling pathways. Plant J 36:602–615. https://doi.org/10.1046/j.1365-313X.2003.01901.x
doi: 10.1046/j.1365-313X.2003.01901.x
pubmed: 14617062
Stamler J, Singel D, Loscalzo J (1992) Biochemistry of nitric oxide and its redox-activated forms. Science (80-) 258:1898–1902. https://doi.org/10.1126/science.1281928
doi: 10.1126/science.1281928
Sun M, Sun S, Mao C, Zhang H, Ou C, Jia Z, Wang Y, Ma W, Li M, Jia S, Mao P (2022) Dynamic responses of antioxidant and glyoxalase systems to seed aging based on full-length transcriptome in oat (Avena sativa L.). Antioxidants 11:395. https://doi.org/10.3390/antiox11020395
doi: 10.3390/antiox11020395
pubmed: 35204277
pmcid: 8869221
Tommasi F, Paciolla C, Arrigoni O (1999) The ascorbate system in recalcitrant and orthodox seeds. Physiol Plant 105:193–198. https://doi.org/10.1034/j.1399-3054.1999.105202.x
doi: 10.1034/j.1399-3054.1999.105202.x
Ursini F, Maiorino M, Brigelius-Flohé R, Aumann KD, Roveri A, Schomburg D, Flohé L (1995) Diversity of glutathione peroxidases. Methods Enzymol 252:38–53. https://doi.org/10.1016/0076-6879(95)52007-4
doi: 10.1016/0076-6879(95)52007-4
pubmed: 7476373
Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:1–12. https://doi.org/10.1186/GB-2002-3-7-RESEARCH0034
doi: 10.1186/GB-2002-3-7-RESEARCH0034
Xia F, Cheng H, Chen L, Zhu H, Mao P, Wang M (2020) Influence of exogenous ascorbic acid and glutathione priming on mitochondrial structural and functional systems to alleviate aging damage in oat seeds. BMC Plant Biol 20:104. https://doi.org/10.1186/s12870-020-2321-x
doi: 10.1186/s12870-020-2321-x
pubmed: 32138669
pmcid: 7059392
Yamasaki H (2000) Nitrite-dependent nitric oxide production pathway: implications for involvement of active nitrogen species in photoinhibition in vivo. Philos Trans R Soc B Biol Sci 355:1477–1488. https://doi.org/10.1098/rstb.2000.0708
doi: 10.1098/rstb.2000.0708
Yan HF, Mao CL, Zhu YQ, Cheng H, Mao PS (2017) Exogenous glutathione pre-treatment improves germination and resistance of Elymus sibiricus seeds subjected to different ageing conditions. Seed Sci Technol 45:607–621. https://doi.org/10.15258/sst.2017.45.3.01
doi: 10.15258/sst.2017.45.3.01
Yao Z, Liu L, Gao F, Rampitsch C, Reinecke DM, Ozga JA, Ayele BT (2012) Developmental and seed aging mediated regulation of antioxidative genes and differential expression of proteins during pre- and post-germinative phases in pea. J Plant Physiol 169:1477–1488. https://doi.org/10.1016/j.jplph.2012.06.001
doi: 10.1016/j.jplph.2012.06.001
pubmed: 22742946