Abstract
We compared the defense against photoinhibitions and oxidative stress in transgenic rice expressing a modified Myxococcus xanthus protoporphyrinogen oxidase (MxProtox) gene and in wild-type (WT) rice. Although the MxProtox transgenic lines had higher content of protoporphyrin IX (Proto IX) than the untreated controls, they did not exhibit a drastic accumulation of Proto IX as in the WT after 2 d of 50 μM oxyfluorfen (OF) treatment. In the transgenic lines S4 and S11, the transcriptions of OsProtox and modified MxProtox genes were almost sustained in response to OF, although transcription of OsProtox was greatly down-regulated in the WT. The excess Proto IX in the WT plants treated with OF generated a severe stress mediated by singlet oxygen (1O2), leading to a prominent increases in electrolyte leakage and malondialdehyde production. This stress in the WT necessitated not only a substantial accumulation of zeaxanthin and antheraxanthin, but also strong increases in activities of superoxide dismutase, catalase, and peroxidase as well as transcriptions of CatalaseB, Ascorbate Peroxidase, and Heme Oxygenase2 genes. By contrast, the transgenic plants did not result in any noticeable increase in these parameters. Our results demonstrate that the transgenic rice expressing modified MxProtox efficiently prevented accumulation of photosensitizing Proto IX through sustaining higher transcriptions of porphyrin biosynthetic genes, thereby reducing the stress imposed by OF.
Similar content being viewed by others
Abbreviations
- APX:
-
ascorbate peroxidase
- CAT:
-
catalase
- MDA:
-
malondialdehyde
- MxProtox:
-
Myxococcus xanthus protoporphyrinogen oxidase
- OF:
-
oxyfluorofen
- POD:
-
peroxidase
- Proto IX:
-
protoporphyrin IX
- Protox:
-
protoporphyrinogen oxidase
- ROS:
-
reactive oxygen species
- SOD:
-
superoxide dismutase
- WT:
-
wild-type
References
Beale, S.I., Weinstein, J.D.: Biochemistry and regulation of photosynthetic pigment formation in plants and algae. — In: Jordan, P.M., (ed.): Biosynthesis of Tetrapyrroles. Pp. 155–235. Elsevier, Amsterdam 1991.
Buege, J.A., Aust, S.D.: Microsomal lipid peroxidation. — Methods Enzymol. 52: 302–310, 1978.
Demmig-Adams, B., Adams III, W.W., Barker, D.H., Logan, B.A., Bowling, D.R., Verhoeven, A.S.: Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. — Physiol. Plant. 98: 253–264, 1996.
Feierabend, J.: Catalases in plants: molecular and functional properties and role in stress defence. — In: Smirnoff, N. (ed.): Antioxidants and Reactive Oxygen Species in Plants. Pp. 101–140. Blackwell Publishing, Oxford 2005.
Foyer, C.H., Noctor, G.: Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. — Antioxid. Redox Signal. 11: 861–905, 2009.
Gallie, D.R.: The role of L-ascorbic acid recycling in responding to environmental stress and in promoting plant growth. — J. exp. Bot. 64: 433–443, 2013.
Gilmore, A.M., Yamamoto, H.Y.: Zeaxanthin formation and energy-dependent fluorescence quenching in pea chloroplasts under artificially-mediated linear and cyclic electron transport. — Plant Physiol. 96: 635–643, 1991.
Jacobs, J.M., Jacobs, N.J., Sherman, T.D., Duke, S.O.: Effects of diphenyl ether herbicides on oxidation of protoporphyrinogen to protoporphyrin in organellar and plasma membrane enriched fractions of barley. — Plant Physiol. 97: 197–203, 1991.
Jahns, P., Holzwarth, A.R.: The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. — Biochim. biophys. Acta 1817: 182–193, 2012.
Jia, H., Förster, B., Chow, W.S., Pogson, B.J., Osmond, B.: Decreased photochemical efficiency of photosystem II following sunlight exposure of shade-grown leaves of avocado: because of, or in spite of, two kinetically distinct xanthophyll cycles? — Plant Physiol. 161: 836–852, 2013.
Jung, S., Lee, Y., Yang, K., Lee, S.B., Jang, S.M., Ha, S.B., Back, K.: Dual targeting of Myxococcus xanthus protoporphyrinogen oxidase into chloroplasts and mitochondria and high level oxyfluorfen resistance. — Plant Cell Environ. 27: 1436–1446, 2004.
Kim, J.-G., Back, K., Lee, H.Y., Lee, H.-J., Phung, T.-H., Grimm, B., Jung, S.: Increased expression of Fe-chelatase leads to increased metabolic flux into heme and confers protection against photodynamically induced oxidative stress. — Plant mol. Biol. 86: 271–287, 2014.
Lee, H.J., Duke, M.V., Birk, J.H., Yamamoto, M., Duke, S.O.: Biochemical and physiological effects of benzheterocycles and related compounds. — J. agr. Food Chem. 43: 2722–2727, 1995.
Lermontova, I., Grimm, B.: Overexpression of plastidic protoporphyrinogen IX oxidaseleads to resistance to the diphenyl-ether herbicide acifluorfen. — Plant Physiol. 122: 75–83, 2000.
Lichtenthaler, H.K.: Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. — Methods Enzymol. 148: 350–382, 1987.
Mittler, R., Poulos, T.L.: Ascorbate peroxidase. — In: Smirnoff, N. (ed.): Antioxidants and Reactive Oxygen Species in Plants. Pp. 87–100. Blackwell Publishing, Oxford 2005.
Mock, H.-P., Heller, W., Molina, A., Neubohn, B., Sandermann, H., Jr., Grimm, B.: Expression of uroporphyrinogen decarboxylase or coproporphyrinogen oxidase antisense RNA in tobacco induces pathogen defense responses conferring increased resistance to tobacco mosaic virus. — J. biol. Chem. 274: 4231–4238, 1999.
Molina, A., Volrath, A., Guyer, D., Maleck, K., Ryals, J., Ward, E.: Inhibition of protoporphyrinogen oxidase expression in Arabidopsis causes a lesion-mimic phenotype that induces systemic acquired resistance. — Plant J. 17: 667–678, 1999.
Muramoto, T., Tsurui, N., Terry, M.J., Yokota, A., Kohchi, T.: Expression and biochemical properties of a ferredoxindependent heme oxygenase required for phytochrome chromophore synthesis. — Plant Physiol. 130: 1958–1966, 2002.
Nandihalli, U.B., Duke, M.V., Duke, S.O.: Relationships between molecular properties and biological activities of O-phenyl pyrrolidino- and piperidino-carbamate herbicides. — J. agr. Food Chem. 40: 1993–2000, 1992.
Noctor, G., Mhamdi, A., Foyer, C.H.: The roles of reactive oxygen metabolism in drought: not so cut and dried. — Plant Physiol. 164, 1636–1648, 2014.
Noriega, G.O., Balestrasse, K.B., Batlle, A., Tomaro, M.L.: Heme oxygenase exerts a protective role against oxidative stress in soybean leaves. — Biochem. biophys. Res. Commun. 323: 1003–1008, 2004.
Papenbrock, J., Grimm, B.: Regulatory network of tetrapyrrole biosynthesis - studies of intracellular signaling involved in metabolic and developmental control of plastids. — Planta 213: 667–681, 2001.
Pham, N.-T., Kim, J.-G., Jung, S.: Differential antioxidant responses and perturbed porphyrin biosynthesis after exposure to oxyfluorfen and methyl viologen in Oryza sativa. — Int. J. mol. Sci. 16: 16529–16544, 2015.
Phung, T.-H., Jung, S.: Differential antioxidant defense and detoxification mechanisms in photodynamically stressed rice plants treated with the deregulators of porphyrin biosynthesis, 5-aminolevulinic acid and oxyfluorfen. — Biochem. biophys. Res. Commun. 459: 346–351, 2015a.
Phung, T.-H., Jung, S.: Alterations in the porphyrin biosynthesis and antioxidant responses to chilling and heat stresses in Oryza sativa. — Biol. Plant. 59: 341–349, 2015b.
Phung, T.-H., Jung, H.-I., Park, J.-H., Kim, J.-G., Back, K., Jung, S.: Porphyrin biosynthesis control under water stress: sustained porphyrin status correlates with drought tolerance in transgenic rice. — Plant Physiol. 157: 1746–1764, 2011.
Rao, M.V., Paliyath, G., Ormrod, D.P.: Ultraviolet-B- and ozone-induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana. — Plant Physiol. 110: 125–136, 1996.
Reinbothe, S., Reinbothe, C., Apel, K., Lebedev, N.: Evolution of chlorophyll biosynthesis - the challenge to survive photooxidation. — Cell 86: 703–705, 1996.
Suzuki, N., Koussevitzky, S., Mittler, R., Miller, G.: ROS and redox signalling in the response of plants to abiotic stress. — Plant Cell Environ. 35: 259–270, 2012.
Tanaka, R., Tanaka, A.: Tetrapyrrole biosynthesis in higher plants. — Annu. Rev. Plant Biol. 58: 321–346, 2007.
Tripathy, B.C., Oemüller, R.: Reactive oxygen species generation and signaling in plants. — Plant Signal. Behav. 7: 1621–1633, 2012.
Von Wettstein, D., Gough, S., Kannangara, C.G.: Chlorophyll biosynthesis. — Plant Cell 7: 1039–1057, 1995.
Woodbury, W., Spencer, A.K, Stahman, M.A.: An improved procedure for using ferricyanide for detecting catalase isozymes. — Anal. Biochem. 44: 301–305, 1971.
Yang, K., Jung, S., Lee, Y., Back, K.: Modifying Myxococcus xanthus protoporphyrinogen oxidase to plant codon usage and high level of oxyfluorfen resistance in transgenic rice. — Pestic. Biochem. Physiol. 86: 186–194, 2006.
Author information
Authors and Affiliations
Corresponding author
Additional information
Acknowledgements: This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2015R1D1A3A01020365).
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Park, J., Tran, L.H. & Jung, S. A protoporphyrinogen oxidase gene expression influences responses of transgenic rice to oxyfluorfen. Biol Plant 61, 659–666 (2017). https://doi.org/10.1007/s10535-017-0732-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10535-017-0732-9