Skip to main content
Log in

Damage of oxidative stress on mitochondria during microspores development in Honglian CMS line of rice

  • Biotic and Abiotic Stress
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

One of the cytoplasmic male sterility (CMS) types used for hybrid rice (Oryza sativa L.) production in China is the Honglian (HL)-CMS. Previous studies suggested that pollen abortion of the sterile plants was resulted from a special programmed cell death (PCD) program started at meiosis in the microspores. To elucidate the molecular basis of the pollen abortion, we compared the biochemical and physiological properties such as content of reactive oxygen species (ROS), ATP, NADH, total glutathione and ascorbate acid, the activities of dehydroascrbate reductase, glutathione reductase, ascorbate peroxides and superoxide dismutase, and the integrity of mitochondrial genome DNA isolated from an HL-CMS line, Yuetai A and its maintainer line, Yuetai B. Our results indicated that the mitochondria of the HL-CMS line suffered from a serious oxidative stress during microspores development. Oxidative stress induced by abnormal increased ROS at meiosis stage resulted in the depletion of ATP and NADH, and the degradation of mitochondrial genomic DNA. This suggests that the presence of redox signal originated in mitochondria affects the rest of the cell. Therefore, it is possible that the abortion of premature microspores in HL-CMS line is induced by the chronic oxidative stress in mitochondria in the early stage of pollen development.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Alscher R, Donahue JL, Cramer CL (1997) Reactive oxygen species and antioxidants: relation ships in green cells. J Plant Physiol 100:224–233

    Article  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–99

    Article  PubMed  CAS  Google Scholar 

  • Balk J, Leaver CJ (2001) The PET1-CMS mitochondrial mutation sunflower is associated with premature programmed cell death and cytochrome c release. Plant Cell 13:1803–1818

    Article  PubMed  CAS  Google Scholar 

  • Balk J, Leaver CJ, McCabe PF (1999) Translocation of cytochrome c from the mitochondria to the cytosol occurs during heat induced programmed cell death in cucumber plants. FEBS Lett 463:151–154

    Article  PubMed  CAS  Google Scholar 

  • Bartoli CG, Pastori GM, Foyer CH (2000) Ascorbate biosynthesis in mitochondria is linked to the electron transport chain between complexes III and IV. Plant Physiol 123:335–344

    Google Scholar 

  • Bartoli CG, Gomez F, Mart DE, Mirtinez FG, Guiamet JJ (2004) Mitochondria are the main target for oxidative damage in leaves of wheat. J Exp Bot 55:1663–1669

    Article  PubMed  CAS  Google Scholar 

  • Bartosz G (1997) Oxidative stress in plants. Acta Physiol Plantarum 19:47–64

    CAS  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assay and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  PubMed  CAS  Google Scholar 

  • Bergman A, Gardeström P, Ericson I (1980) Method to obtain a chlorophyll-free preparation of intact mitochondria from spinach leaves. Plant Physiol 66:442–445

    Article  PubMed  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analyt Biochem 72:248–254

    Google Scholar 

  • Bray TM, Taylor CG (1993) Tissue glutathione, nutrition, and oxidative stress. Can J Physiol Pharm 71:746–751

    CAS  Google Scholar 

  • Brennicke A, Marchfelde A, Binder S (1999) RNA editing. FEMS Microbiol Rev 23:297–316

    Article  PubMed  CAS  Google Scholar 

  • Ducos E, Touzet P, Boutry M (2001) The male sterile G cytoplasm of wild beet displays modified mitochondrial respiratory complexes. Plant J 26:171–180

    Article  PubMed  CAS  Google Scholar 

  • Dutilleu C, Garmier M, Noctor G, Mathieu C, Cherit P (2003) Leaf mitochondrial modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. Plant Cell 15:1212–1226

    Article  CAS  Google Scholar 

  • Esposito LA, Melov S, Panov A, Cottrell BA, Wallace DC (1999) Mitochondrial disease in mouse results in increased oxidative stress. Proc Natl Acad Sci USA 96:4820–4825

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Noctor G (2000) Oxygen processing in photosynthesis: regulation and signaling. New Phytol 146:359–388

    Article  CAS  Google Scholar 

  • Foyer CH, Rowell J, Walker D (1983) Measurements of the ascorbate content of spinach leaf protoplasts and chloroplasts during illumination. Planta 157:239–244

    Article  CAS  Google Scholar 

  • Friedberg EC, Walker GC, Siede W (1995) DNA repair and mutagenesis. Am Soc Microbiol, Washington, DC

  • Garmie M, Dutilleu C, Mathieu C, Chetrit P, Boccara M, Paepe RD (2002) Changes in antioxidant erpression and harpin-induced hyoersensitive response in a Nicotiana sylvestris mitochondrial mutant. Plant Physiol Biochem 40:561–566

    Article  Google Scholar 

  • Gueguen V, Macherel D, Jaquinod M, Douce R, Bourguignon J (2000) Fatty acid and lipoic acid biosynthesis in higher plant mitochondria. J Biol Chem 275:5016–5025

    Google Scholar 

  • Kingston-Smith AH, Foyer CH (2000) Over expression of Mn-superoxide dismutase in maize leaves leads to increased monodehydroascorbate reducatase, dehydroascorbate reductase and glutathion reductase activities. J Exp Bot 51:1867–1877

    Article  PubMed  CAS  Google Scholar 

  • Li SQ, Wan CX, Kong J, Zhang ZJ, Li YS, Zhu YG (2004) Programmed cell death during microgenesis in Honglian CMS line of rice is correlated with oxidative stress in mitochondria. Funct Plant Biol 31:369–376

    Article  CAS  Google Scholar 

  • Liu XQ, Xu X, Tan YP, Li SQ, Hu J, Huang JY, Yang DC, Li YS, Zhu YG (2004) Inheritance and molecular mapping of two fertility-restoring loci for Honglian gametophytic cytoplasmic male sterility in rice (Oryza sativa L.). Mol Genet Genom 271:586–594

    Article  CAS  Google Scholar 

  • Mehlhorn H, Lelandais M, Korth HG, Foyer CH (1996) Ascorbate is the natural substrate for plant peroxidases. FEBS Lett 378:203–206

    Article  PubMed  CAS  Google Scholar 

  • Mittler R, Zilinskas BA (1993) Detection of ascorbate peroxidase activity in native gels by inhibition of the ascorbate-dependent reduction of nitroblue tetrazolium. Anal Biochem 212:540–546

    Article  PubMed  CAS  Google Scholar 

  • Møller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52:561–591

    Article  PubMed  Google Scholar 

  • Nijs D, Kelley PM (1991) Vitamins C and E donate single hydrogen atoms in vivo. FEBS Lett 284:147–151

    Article  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  PubMed  CAS  Google Scholar 

  • Notsu Y, Masood S, Nishikawa T, Kubo N, Akiduki G, Nakazono M, Hirai A, Kadowaki K (2002) The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol Genet Genom 268:434–445

    Article  CAS  Google Scholar 

  • Rebeille F, Macherel D, Mouillon JM, Garin J, Douce R (1997) Folate biosynthesis in higher plants: Purification and molecular cloning of bifunctional 6-hydroxymethyl-7,8-dihydropterin pyrophosphokinase-7,8-dihydropteroate synthase localized in mitochondria. EMBO J 16:947–957

    Google Scholar 

  • Richter C, Park JW, Ames B (1988) Normal oxidative damage to mitochondrial and nuclear DNA is extensive. Proc Natl Acad Sci USA 85:6465–6467

    Article  PubMed  CAS  Google Scholar 

  • Schnable P, Wise RP (1998) The molecular basis of cytoblasmic male sterility and fertility restoration. Trends Plant Sci 3:175–180

    Article  Google Scholar 

  • Singh KK (2004) Mitochondria damage checkpoint in apoptosis and genome stability. FEMS Yeast Res 5:127–132

    Article  PubMed  CAS  Google Scholar 

  • St. John JB (1970) Determination of ATP in Chlorella with the luciferin–luciferase enzyme system. Anal Biochem 37:409–416

    Article  PubMed  CAS  Google Scholar 

  • Sweetlove LJ, Heazlewood JL, Herald V, Holtzapffel R, Day DA, Leaver CJ, Milla AH (2002) The impact of oxidative stress on Arabidopsis mitochondria. Plant J 32:891–904

    Article  PubMed  CAS  Google Scholar 

  • Taylor NL, Day DA, Millar AH (2002) Environmental stress causes oxidative damage to plant mitochondria leading to inhibition of glycine decarboxylase. J Biol Chem 277:42663–42668

    Article  PubMed  CAS  Google Scholar 

  • Teixeira RT, Knorpp C, Glimelius K (2005) Modified sucrose, starch, and ATP levels in two alloplasmic male-sterile lines of B. napus. J Exp Bot 56:1245–1253

    Article  PubMed  CAS  Google Scholar 

  • Tiwari BS, Belengh B, Levine A (2002) Oxidative stress increased respiration and generation of reactive oxygen species, resulting in ATP depletion, opening of mitochondrial permeability transition, and programmed cell death. Plant Physiol 128:1271–1281

    Article  PubMed  CAS  Google Scholar 

  • Tretter L, Adam-Vizi V (2000) Inhibition of Krebs cycle enzymes by hydrogen peroxide: a key role of a-ketoglutarate dehydrogenase in limiting NADH production under oxidative stress. J Neurosci 20:8972–8979

    PubMed  CAS  Google Scholar 

  • Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C (1997) Catalase is a sink for H2O2 and is indispensable for stress defense in C3 plants. EMBO J 14:4806–4816

    Article  Google Scholar 

  • Yakes FM, Houten BV (1997) Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc Natl Acad Sci USA 94:514–519

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Dr. Daichang Yang for his critical review of the manuscript. The work was supported by National Natural Science Foundation of China (30270149) and National 973 Program of China (Grant no. 2001CB108806).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yingguo Zhu.

Additional information

Communicated by W.-H. Wu

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wan, C., Li, S., Wen, L. et al. Damage of oxidative stress on mitochondria during microspores development in Honglian CMS line of rice. Plant Cell Rep 26, 373–382 (2007). https://doi.org/10.1007/s00299-006-0234-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-006-0234-2

Keywords

Navigation