Abstract
The localization of salt-induced H2O2 accumulation in the leaves of rice was examined using 3,3-diaminobenzidine and CeCl3 staining at ultrastructure level. When the 3-week-old rice plants were affected by 100 mM NaCl for 14 days, the swelling of thylakoids and the destruction of thylakoid membranes were observed. H2O2 accumulation was also observed in the chloroplast of the leaf treated with NaCl. The electron dense products of 3,3-diaminobenzidine and CeCl3 were mainly observed especially around the swelling of thylakoids. H2O2 accumulation and any ultrastructural changes were not observed in the chloroplasts under dark condition. Furthermore, treatment with ascorbic acid suppressed both H2O2 accumulation and the changes in chloroplast ultrastructure. These results suggest that light-induced production of excess H2O2 under salinity is responsible for the changes in chloroplast ultrastructure. H2O2 accumulation was also observed in the mitochondria, peroxisomes, plasma membrane, and cell walls under light but not dark, suggesting that these organelles are also the source of H2O2 and the production is light dependent under salinity.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Ann Rev Plant Mol 55:373–399
Bestwick CS, Brown IR, Bennett MHR, Mansfield JW (1997) Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolocola. Plant Cell 9:209–221
Blokhina OB, Chirkova TV, Fagertstedt KV (2001) Anoxic stress leads to hydrogen peroxide formation in plant cells. J Exp Bot 52:1179–1190
Corpas FJ, Gómez M, Hernández JA, del Rio LA (1993) Metabolism of activated oxygen in peroxisomes from two Pisum sativum L. cultivars with different sensitivity to sodium chloride. J Plant Physiol 141:160–165
Dat J, Vandenabeele S, Vranová E, Van Montagu M, Inzé D (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795
Foyer CH (2004) The contribution of photosynthetic oxygen metabolism to oxidative stress in plants. In: Inzé D, Van Montagu M (eds) Oxidative stress in plants. Taylor & Francis, San Diego, pp 51–83
Frederich SE, Newcomb EH (1969) Cytochemical localization of catalase in leaf microbodies (peroxisomes). J Cell Biol 49:343–353
Fridovich I (1986) Biological effects of the superoxide radical. Arch Biochem Biophys 247:1–11
Heineke D, Riens B, Grosse H, Hoferichter P, Peter U, Flügge U-I, Heldt HW (1991) Redox transfer across the inner chloroplast envelope membrane. Plant Physiol 95:1131–1137
Hernández JA, Olmos E, Corpas FJ, Servilla F, del Rio LA (1995) Salt-induced oxidative stress in chloroplast of pea plants. Plant Sci 105:151–167
Hernandez M, Fernandez-Garcia N, Diaz-Vivancos P, Olmos E (2010) A different role for hydrogen peroxide and the antioxidative system under short and long salt stress in Brassica oleracea roots. J Exp Bot 61:521–535
Hu X, Zhang A, Zhamg J, Jiang M (2006) Abscisic acid is key inducer of hydrogen peroxide production in leaves of maize plants exposed to water stress. Plant Cell Physiol 47:1484–1495
Kinoshita H, Nagasaki J, Yoshikawa N, Yamamoto A, Takito S, Kawasaki M, Sugiyama T, Miyake H, Weber APM, Taniguchi M (2011) The chloroplastic 2-oxoglutarate/malate transporter has dual function as the malate valve and in carbon/nitrogen metabolism. Plant J 65:15–26
Michalecka AM, Svensson AS, Johansson FI, Agius SC, Johanson U, Brennicke A, Binder S, Rasmusson AG (2003) Arabidopsis genes encoding mitochondrial type II NAD(P)H dehydrogenases have different evolutionary origin and show distinct responses to light. Plant Physiol 133:642–652
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signaling during drought and salinity stresses. Plant Cell Environ 33:453–467
Mitsuya S, Takeoka Y, Miyake H (2000) Effects of sodium chloride on foliar ultrastructure of sweet potato (Ipomoea batatas Lam.) plantlets grown under light and dark conditions in vitro. J Plant Physiol 157:661–667
Mitsuya S, Kawasaki M, Taniguchi M, Miyake H (2003) Light dependency of salinity-induced chloroplast degradation. Plant Prod Sci 6:219–223
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Mittova V, Guy M, Tal M, Volokita M (2004) Salinity up-regulates the antioxidative system in root mitochondria and peroxisomes of the wild salt-tolerant tomato species Lycopersicon pennellii. J Exp Bot 55:1105–1113
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681
Neill SJ, Desikan R, Hancock JT (2002) Hydrogen peroxide signaling. Curr Opin Plant Biol 5:388–395
Noctor G, Veljovic-Jovanovic S, Driscoll S, Novistskaya L, Foyer CH (2002) Drought and oxidative load in the leaves of C3 plants: a predominant role for photorespiration? Ann Bot 89:841–850
Novikoff AB, Goldfischer S (1969) Visualization of peroxisomes (microbodies) and mitochondria with diaminobenzidine. J Histochem Cytochem 17:675–680
Pellinen R, Palva T, Kangasjärvi J (1999) Subcellular localization of ozone-induced hydrogen peroxide production in birch (Betula pendula) leaf cells. Plant J 20:349–356
Rhoads DM, Umbach AL, Subbaiah CC, Siedow JN (2006) Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling. Plant Physiol 141:357–366
Romero-Puertas MC, Rodrígues-Serrano M, Corpas FJ, Gómez M, del Río LA, Sandalio LM (2004) Cadmium-induced subcellular accumulation of O −2 and H2O2 in pea leaves. Plant Cell Environ 27:1122–1134
Shalata A, Tal M (1998) The effect of salt stress on lipid peroxidation and antioxidants in the leaf of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii. Physiol Plant 104:169–174
Shi Q, Ding F, Wang X, Wei M (2007) Exogenous nitric oxide protect cucumber roots against oxidative stress induced by salt stress. Plant Physiol Biochem 45:542–550
Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11:1187–1194
Ueda R, Konno N, Nakatani M, Katagiri T (2003) Production of hydrogen peroxide in situ in cardiac myocytes during hypoxia-reoxygenation as assessed with cerium. Med Electron Microsc 36:41–46
Vaidyanathan H, Sivakumar P, Chakrabarty R, Thomas G (2003) Scavenging of reactive oxygen species in NaCl-stressed rice (Oryza sativa L.) differential response in salt-tolerant and sensitive varieties. Plant Sci 165:1411–1418
Yamane K, Rahman MS, Kawasaki M, Taniguchi M, Miyake H (2004) Pretreatment with antioxidants decreases the effects of salt stress on chloroplast ultrastructure in rice leaf segments (Oryza sativa L.). Plant Prod Sci 7:292–300
Yamane K, Mitsuya S, Taniguchi M, Miyake H (2009) Antioxidant capacity and damages caused by salinity stress in apical and basal regions of rice leaf. Plant Prod Sci 12:319–326
Acknowledgments
We are grateful to Mr. Shinya Mizuno of the University Farm for harvesting the rice seeds used in this investigation. This work was supported by a Grant-in-Aid for Scientific Research (no. 22658005) from the Ministry of Education, Culture, Sports, Science and Technology, Japan.
Conflicts of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Adrienne R. Hardham
Rights and permissions
About this article
Cite this article
Yamane, K., Taniguchi, M. & Miyake, H. Salinity-induced subcellular accumulation of H2O2 in leaves of rice. Protoplasma 249, 301–308 (2012). https://doi.org/10.1007/s00709-011-0280-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00709-011-0280-7