Skip to main content
Log in

Alterations in the porphyrin biosynthesis and antioxidant responses to chilling and heat stresses in Oryza sativa

  • Original Papers
  • Published:
Biologia Plantarum

Abstract

Roles of an altered porphyrin biosynthesis and antioxidants in protection against chilling and heat stresses were evaluated in rice (Oryza sativa L.). When exposed to the same exposure time (6 or 30 h), heat-stressed (45 °C) plants exhibited a less oxidative stress as indicated by a lower dehydration, ion leakage, and H2O2 production compared to chilling-stressed (4 °C) plants. Malondialdehyde production also increased after a mild chilling stress, whereas it increased only after a long-term heat stress. The content of protoporphyrin IX, Mg-protoporphyrin IX and its methyl ester, and protochlorophyllide drastically declined under both the stresses, particularly under the long-term heat stress. Greater increases in catalase and peroxidase activities in heat-stressed plants indicate more cofactors supplied for hemoproteins compared to those of chilling-stressed and untreated control plants. Intermediates of carotenoid biosynthesis, zeaxanthin and antheraxanthin, also increased under the chilling and heat stresses. In comparison to chilling-stressed plants, heat-stressed plants were more efficient in porphyrin scavenging and antioxidant enzyme responses, which may play crucial roles in plant protection under temperature stress, thereby suffering less from oxidative stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ALA:

5-aminolevulinic acid

APX:

ascorbate peroxidase

CAT:

catalase

DAB:

3,3-diaminobenzidine

MDA:

malondialdehyde

MgProto IX:

Mg-protoporphyrin IX

MgProto IX ME:

Mg-protoporphyrin IX methyl ester

Pchlide:

protochlorophyllide

POD:

peroxidase

Proto IX:

protoporphyrin IX

ROS:

reactive oxygen species

RWC:

relative water content

SOD:

superoxide dismutase

References

  • Abdelkader, A.F., Aronsson, H., Sundqvist, C.: High salt stress in wheat leaves causes retardation of chlorophyll accumulation due to a limited rate of protochlorophyllide formation. — Physiol. Plant. 130: 157–166, 2007.

    Article  CAS  Google Scholar 

  • Almeselmani, M., Deshmukh, P.S., Sairam, P.K., Kushwaha, S.R., Singh, T.P.: Protective role of antioxidant enzymes under high temperature stress. — Plant Sci. 171: 382–388, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Alscher, R.G., Hess, J.L. (ed.): Antioxidants in Higher Plants. — CRC Press, Boca Raton 1993.

    Google Scholar 

  • Asada, K.: The role of ascorbate peroxidase and monodehydroascorbte reductase in H2O2 scavenging in plants. — In: Scandalios, J.G. (ed.): Oxidative Stress and the Molecular Biology of Antioxidant Defenses. Pp. 715–735. CSHL Press, Cold Spring Harbor 1997.

    Google Scholar 

  • Back, K., Jung, S.: The lack of plastidal transit sequence cannot override the targeting capacity of Bradyrhizobium japonicum δ-aminolevulinic acid synthase in transgenic rice. — Biol. Plant. 54: 279–284, 2010.

    Article  CAS  Google Scholar 

  • Beale, S.I., Weinstein, J.D.: Tetrapyrrole metabolism in photosynthetic organisms. — In: Daily, H.A. (ed.): Biosynthesis of Heme and Chlorophyll. Pp. 287–391. McGraw-Hill, New York 1990.

    Google Scholar 

  • Berry, J.A., Björkman, O.: Photosynthetic response and adaptation to temperature in higher plants. — Annu. Rev. Plant Physiol. 31: 491–543, 1980.

    Article  Google Scholar 

  • Buege, T.A., Aust, S.D.: Microsomal lipid peroxidation. — Methods Enzymol. 52: 302–310, 1978.

    Article  CAS  PubMed  Google Scholar 

  • Dalal, V.K., Tripathy, B.C.: Modulation of chlorophyll biosynthesis by water stress in rice seedlings during chloroplast biogenesis. — Plant Cell Environ. 35: 1685–1703, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Duke, S.O., Lydon, J., Becerril, J.M., Sherman, T.D., Lehnen, L.P., Matsumoto, H.: Protoporphyrinogen oxidaseinhibiting herbicides. — Weed Sci. 39: 465–473, 1991.

    CAS  Google Scholar 

  • Dutta, S., Mohanty, S., Tripathy, B.C.: Role of temperature stress on chloroplast biogenesis and protein import in pea. — Plant Physiol. 150: 1050–1061, 2009.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • Feierabend, J., Mikus, M.: Occurrence of a high temperature sensitivity of chloroplast ribosome formation in several higher plants. — Plant Physiol. 59: 863–867, 1976.

    Article  Google Scholar 

  • Foyer, C.H., Shigeoka, S.: Understanding oxidative stress and antioxidant functions to enhance photosynthesis. — Plant Physiol. 155: 93–100, 2011.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gill, S.S., Tuteja, N.: Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. — Plant Physiol. Biochem. 48: 909–930, 2010.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gilmore, A.M., Yamamoto, H.Y.: Linear models relating xanthophylls and lumen acidity to non-photochemical fluorescence quenching. Evidence that antheraxanthin explains zeaxanthin-independent quenching. — Photosynth. Res. 35: 67–78, 1993.

    Article  CAS  PubMed  Google Scholar 

  • Guy, C.L.: Cold acclimation and freezing stress tolerance. — Annu. Rev. Plant Physiol. Plant mol. Biol. 41: 187–223, 1990.

    Article  CAS  Google Scholar 

  • Holt, N.E., Zigmantas, D., Valkunas, L., Li, X.-P., Niyogi, K.K., Fleming, G.R.: Carotenoid cation formation and the regulation of photosynthetic light harvesting. — Science 307: 433–435, 2005.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Jung, S., Steffen, K.L.: Influence of photosynthetic photon flux densities before and during long-term chilling on xanthophyll cycle and chlorophyll fluorescence quenching in leaves of tomato (Lycopersicon hirsutum). — Physiol. Plant. 100: 958–966, 1997.

    Article  CAS  Google Scholar 

  • Kaplan, F., Kopka, J., Haskell, D.W., Zhao, W., Schiller, K.C., Gatzke, N., Sung, D.Y., Guy, C.L.: Exploring the temperature-stress metabolome of Arabidopsis. — Plant Physiol. 136: 4159–4168, 2004.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • King, M.M., Ludford, P.M.: Chilling injury and electrolyte leakage in fruit of different tomato cultivars. — J. amer. Soc. hort. Sci. 108: 74–77, 1983.

    Google Scholar 

  • Ledford, H.K., Niyogi, K.K.: Singlet oxygen and photooxidative stress management in plants and algae. — Plant Cell Environ. 28: 1037–1045, 2005.

    Article  CAS  Google Scholar 

  • Lee, G., Carrow, V., Duncan, A.: Growth and water relation responses to salinity stress in halophytic sea shore Paspalum ecotypes. — Sci. Hort. 104: 221–236, 2005.

    Article  Google Scholar 

  • Lee, D.H., Lee, C.B.: Chilling stress-induced changes of antioxidant enzymes in the leaves of cucumber: in gel enzyme activity assays. — Plant Sci. 159: 75–85, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Lermontova, I., Grimm, B.: Overexpression of plastidic protoporphyrinogen IX oxidase leads to resistance to the diphenylether herbicide acifluorfen. — Plant Physiol. 122: 75–83, 2000.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lichtenthaler, H.K.: Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. — Methods Enzymol. 148: 350–382, 1987.

    Article  CAS  Google Scholar 

  • Mazorra, L.M., Nunez, M., Echerarria, E., Coll, F., Sánchez-Blanco, M.J.: Influence of brassinosteroids and antioxidant enzymes activity in tomato under different temperatures. — Plant Biol. 45: 593–596, 2002.

    Article  CAS  Google Scholar 

  • Mittler, R., Finka, A., Goloubinoff, P.: How do plants feel the heat? — Trends biochem. Sci. 37: 118–125, 2012.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • Miura, K., Furumoto, T.: Cold signaling and cold response in plants. — Int. J. mol. Sci. 14: 5312–5337, 2013.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mohanty S., Grimm B., Tripathy B.C.: Light and dark modulation of chlorophyll biosynthetic genes in response to temperature. — Planta 224: 692–699, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Niyogi, K.K.: Photoprotection revisited: genetic and molecular approaches. — Annu. Rev. Plant Physiol. Plant mol. Biol. 50: 333–359, 1999.

    Article  CAS  PubMed  Google Scholar 

  • Olson, P.D., Varner, J.E.: Hydrogen peroxide and lignification. — Plant J. 4: 887–892, 1993.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Prasad, T.K., Anderson, M.D., Martin, B.A., Stewart, C.R.: Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. — Plant Cell 6: 65–74, 1994.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Qu, A.-L., Ding, Y.-F., Jiang, Q., Zhu, C.: Molecular mechanisms of the plant heat stress response. — Biochem. biophys. Res. Commun. 432: 203–207, 2013.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Reinbothe, S., Reinbothe, C.: The regulation of enzymes involved in chlorophyll biosynthesis. — Eur. J. Biochem. 237: 323–343, 1996.

    Article  CAS  PubMed  Google Scholar 

  • Reinbothe, S., Reinbothe, C., Apel, K., Lebedev, N.: Evolution of chlorophyll biosynthesis — the challenge to survive photooxidation. — Cell 86: 703–705, 1996.

    Article  CAS  PubMed  Google Scholar 

  • Sanghera, G.S., Wani, S.H., Hussain, W., Singh, N.B.: Engineering cold stress tolerance in crop plants. — Curr. Genomics 2: 30–43, 2011.

    Article  Google Scholar 

  • Shinozaki, K., Yamaguchi-Shinozaki, K., Seki, M.: Regulatory network of gene expression in the drought and cold stress responses. — Curr. Opin. Plant Biol. 6: 410–417, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Sung, D.-Y., Kaplan, F., Lee, K.-J., Guy, C.L.: Acquired tolerance to temperature extremes. — Trends Plant Sci. 8: 179–187, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Suzuki, N., Koussevitzky, S., Mittler, R., Miller, G.: ROS and redox signaling in the response of plants to abiotic stress. — Plant Cell Environ. 35: 259–270, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Tanaka, A., Tanaka, R.: Chlorophyll metabolism. — Curr. Opin. Plant Biol. 9: 248–255, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Tewari, A.K., Tripathy, B.C. Temperature-stress-induced impairment of chlorophyll biosynthetic reactions in cucumber and wheat. — Plant Physiol. 117: 851–858, 1998.

    Article  CAS  Google Scholar 

  • Tewari, A.K., Tripathy, B.C.: Acclimation of chlorophyll biosynthetic reactions to temperature stress in cucumber (Cucumis sativus L.). — Planta 208: 431–437, 1999.

    Article  CAS  Google Scholar 

  • Thordal-Christensen, H., Zhang, Z., Wei, Y., Collinge, D.B.: Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. — Plant J. 11: 1187–1194, 1997.

    Article  CAS  Google Scholar 

  • Tripathy, B.C., Dalal, V.: Modulation of chlorophyll biosynthesis by environmental cues. — In: Biswal, B., Krupinska, K., Biswal, U.C. (ed.): Plastid Development in Leaves During Growth and Senescence. Advances in Photosynthesis and Respiration Vol. 36. Pp. 601–639. Springer, Dordrecht 2013.

    Chapter  Google Scholar 

  • Valenzeno, D.: Photomodification of biological membranes with emphasis on singlet oxygen mechanisms. — Photochem. Photobiol. 46: 146–160, 1987.

    Google Scholar 

  • Wagner, D., Przybyla, D., Op den Camp, R., Kim, C., Landgraf, F., Lee, K.P., Würsch, M., Laloi, C., Nater, M., Hideg, E., Apel, K.: The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. — Science 306: 1183–1185, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Wahid, A., Gelani, S., Ashraf, M., Foolad, M.R.: Heat tolerance in plants: an overview. — Environ. exp. Bot. 61: 199–223, 2007.

    Article  Google Scholar 

  • Wilson, K.E., Sieger, S.M., Huner, N.P.A.: The temperature-dependent accumulation of Mg-protoporphyrin IX and reactive oxygen species in Chlorella vulgaris. — Physiol. Plant. 119: 126–136, 2003.

    Article  CAS  Google Scholar 

  • Woodbury, W., Spencer, A.K., Stahman, M.A.: An improved procedure for using ferricyanide for detecting catalase isozymes. — Anal. Biochem. 44: 301–305, 1971.

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki, K., Shinozaki, K.: Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. — Annu. Rev. Plant Biol. 57: 781–803, 2006.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. Jung.

Additional information

Acknowledgements: This work was supported by the National Research Foundation of Korea Grant funded by the Ministry of Education, Science and Technology (NRF-2009-0076123 and NRF-2010-0005635).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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 (2015). https://doi.org/10.1007/s10535-015-0505-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10535-015-0505-2

Additional key words

Navigation