Abstract
Cytoplasmic male sterility (CMS)-C is one of the most attractive sources of male sterility in the production of hybrid maize. However, the abortion mechanism of CMS-C is currently unknown. The major aim of this work was to characterize the expression of genes and proteins during pollen abortion. The materials assayed included CMS-C line C48-2, its maintainer line N48-2, and fertile F1 (C48-2 × 18 white). A total of 20 unique genes and 25 proteins were identified by suppression subtractive hybridization and 2-D electrophoresis, respectively. Most of the genes and proteins identified are closely related to energy metabolism, stress responses, molecular chaperones, and cell death, which are generally considered to be essential to pollen development. Based on the function of these identified genes and proteins, reactive oxygen species in isolated mitochondria and DNA fragments were analyzed. The results from this study indicate that the oxidative stress which was associated with the specific expression patterns of some genes may be the physiological cause for the abortion of premature microspores in the maize CMS-C line.
Similar content being viewed by others
References
Abu-Hamad S, Sivan S, Shoshan-Barmatz V (2006) The expression level of the voltage-dependent anion channel controls life and death of the cell. Proc Natl Acad Sci USA 103:5787–5792
Allen J, Fauron C, Minx P, Roark L, Oddiraju S, Lin G, Meyer L, Sun H, Kim K, Wang C (2007) Comparisons among two fertile and three male-sterile mitochondrial genomes of maize. Genetics 177:1173–1192
Arrigo A, Virot S, Chaufour S, Firdaus W, Kretz-Remy C, Diaz-Latoud C (2005) Hsp27 consolidates intracellular redox homeostasis by upholding glutathione in its reduced form and by decreasing iron intracellular levels. Antioxid Redox Signal 7:414–422
Balk J, Leaver C (2001) The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release. Plant Cell 13:1803
Banzet N, Richaud C, Deveaux Y, Kazmaier M, Gagnon J, Triantaphylidès C (1998) Accumulation of small heat shock proteins, including mitochondrial HSP22, induced by oxidative stress and adaptive response in tomato cells. Plant J 13:519–527
Beckett J (1971) Classification of male-sterile cytoplasms in maize (Zea mays L.). Crop Sci 11:724–726
Bradford M (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
Brandt U, Kerscher S, Dröse S, Zwicker K, Zickermann V (2003) Proton pumping by NADH: ubiquinone oxidoreductase. A redox driven conformational change mechanism? FEBS Lett 545:9–17
Carroll J, Fearnley I, Skehel J, Shannon R, Hirst J, Walker J (2006) Bovine complex I is a complex of forty-five different subunits. J Biol Chem 281:32724–32727
Chan E, Fraser S, Yin S, Yeo G, Kwek K, Fairclough R, Smith R (2002) Human myometrial genes are differentially expressed in labor: a suppression subtractive hybridization study. J Clin Endocrinol Metab 87:2435
Crompton M (1999) The mitochondrial permeability transition pore and its role in cell death. Biochem J 341:233
Dewey R, Timothy D, Levings C (1991) Chimeric mitochondrial genes expressed in the C male-sterile cytoplasm of maize. Curr Genet 20:475–482
Diatchenko L, Lau Y, Campbell A, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov E (1996) Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 93:6025
Duan J, Zhang M, Liang C (1996) The relationship between membrane lipid peroxidation and cytoplasmic male sterility in maize. Plant Phys Commun 32:331–334
Fecke W, Sled V, Ohnishi T, Weiss H (1994) Disruption of the gene encoding the NADH-binding subunit of NADH: ubiquinone oxidoreductase in Neurospora crassa. Eur J Biochem 220:551–558
Forde B, Oliver R, Leaver C (1978) Variation in mitochondrial translation products associated with male-sterile cytoplasms in maize. Proc Natl Acad Sci USA 75:3841
Franklin-Tong V, Gourlay C (2008) A role for actin in regulating apoptosis/programmed cell death: evidence spanning yeast, plants and animals. Biochem J 413:389–404
Green D, Kroemer G (2004) The pathophysiology of mitochondrial cell death. Science 305:626
Gutierres S, Sabar M, Lelandais C, Chetrit P, Diolez P, Degand H, Boutry M, Vedel F, De Kouchkovsky Y, De Paepe R (1997) Lack of mitochondrial and nuclear-encoded subunits of complex I and alteration of the respiratory chain in Nicotiana sylvestris mitochondrial deletion mutants. Proc Natl Acad Sci USA 94:3436
Hanson M, Bentolila S (2004) Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16:S154–S169
Heazlewood JL, Howell KA, Whelan J, Millar AH (2003) Towards an analysis of the rice mitochondrial proteome. Plant Physiol 132:230–241
Hochholdinger F, Guo L, Schnable P (2004) Cytoplasmic regulation of the accumulation of nuclear-encoded proteins in the mitochondrial proteome of maize. Plant J 37:199–208
Horner H, Hall VL, Vargas-Olvera M (1993) Isolation, sorting, and characterization of uni-and binucleate tapetal protoplasts from anthers of normal and Texas cytoplasmic male-sterile Zea mays L. Protoplasma 173:48–57
Jiang PD, Zhang X, Zhu Y, Zhu W, Xie H, Wang X (2007) Metabolism of reactive oxygen species in cotton cytoplasmic male sterility and its restoration. Plant Cell Rep 26:1627–1634
Lemasters J (2005) Dying a thousand deaths: redundant pathways from different organelles to apoptosis and necrosis. Gastroenterology 129:351–360
Li S, Wan C, Kong J, Zhang Z, Li Y, Zhu Y (2004) Programmed cell death during microgenesis in a Honglian CMS line of rice is correlated with oxidative stress in mitochondria. Funct Plant Biol 31:369–376
Lu Y, Liu Y, Wang J, Cao M, Rong T (2010) Variation and patterns of DNA methylation in maize C-type CMS lines and their maintainers. J Plant Biochem Biotechnol 19:43–50
Mignouna H, Virmani S, Briquet M (1987) Mitochondrial DNA modifications associated with cytoplasmic male sterility in rice. Theor Appl Genet 74:666–669
Millar A, Mittova V, Kiddle G, Heazlewood J, Bartoli C, Theodoulou F, Foyer C (2003) Control of ascorbate synthesis by respiration and its implications for stress responses. Plant Physiol 133:443
Møller I (2003) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52:561
Nakamoto H, Vigh L (2007) The small heat shock proteins and their clients. Cell Mol Life Sci 64:294–306
Newton K (1989) Molecular correlates of cytoplasmic types. Maize Genet Crop Newsl 63:197
Pla M, Mathieu C, De Paepe R, Chétrit P, Vedel F (1995) Deletion of the last two exons of the mitochondrial nad7 gene results in lack of the NAD7 polypeptide in a Nicotiana sylvestris CMS mutant. MGG 248:79–88
Porubleva L, Vander Velden K, Kothari S, Oliver D, Chitnis P (2001) The proteome of maize leaves: use of gene sequences and expressed sequence tag data for identification of proteins with peptide mass fingerprints. Electrophoresis 22:1724–1738
Samuel M, Ellis B (2002) Double jeopardy: both overexpression and suppression of a redox-activated plant mitogen-activated protein kinase render tobacco plants ozone sensitive. Plant Cell 14:2059
Shen Y, Zhang Z, Lin H, Liu H, Chen J, Peng H, Cao M, Rong T, Pan G (2011) Cytoplasmic male sterility-regulated novel microRNAs from maize. Funct Integr Genomics 11:179–191
Sofi P, Rather A, Wani S (2007) Genetic and molecular basis of cytoplasmic male sterility in maize. Commun Biomet Crop Sci 2:49–60
Takada K, Ishimaru K, Kamada H, Ezura H (2006) Anther-specific expression of mutated melon ethylene receptor gene Cm-ERS1/H70A affected tapetum degeneration and pollen grain production in transgenic tobacco plants. Plant Cell Rep 25:936–941
Thomas S, Huang S, Li S, Staiger C, Franklin-Tong V (2006) Actin depolymerization is sufficient to induce programmed cell death in self-incompatible pollen. J Cell Biol 174:221
Wang J, Cao M, Pan G, Lu Y, Rong T (2009) RNA editing of mitochondrial functional genes atp6 and cox2 in maize (Zea mays L.). Mitochondrion 9:364–369
Xia T, Liu JL (1994) Cytochrome oxidase activity and ATP content of male-sterile cytoplasm in maize (Zea mays L.). Acta Agriculturae Boreali Sinica 9:33–37
Xu K, Cao M, Zhu Y (2008) Analysis of differential expression of mitochondrial proteins between C- type cytoplasmic male sterility line C48-2 and maintainer in maize. Acta Agronomica Sinica 34:232–237
Yan P, Zhang Y, Tang C, Su A, Sun N (2006) Comparative proteomic analysis provides new insights into chilling stress responses in rice. Mol Cell Proteomics 5:484
Yang J, Zhang M, Yu J (2009) Mitochondrial nad2 gene is co-transcripted with CMS-associated orfB gene in cytoplasmic male-sterile stem mustard (Brassica juncea). Mol Biol Rep 36(2):345–351
Zizi M, Forte M, Blachly-Dyson E, Colombini M (1994) NADH regulates the gating of VDAC, the mitochondrial outer membrane channel. J Biol Chem 269:1614
Zou J, Lin W, Luo H, Sun L, Liu C (2009) Comparison the activities of peroxidase, catalase, superoxide dismutase and peroxidase zymogram in C-cytoplasmic male sterility line on maize. J Maize Sci 17:45–49
Acknowledgments
This work was financed by the National Natural Science Foundation of China (no. 30971794) and the Scientific Research Foundation of Sichuan Education Department, China.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Liwen Jiang
Rights and permissions
About this article
Cite this article
Huang, L., Xiang, J., Liu, J. et al. Expression characterization of genes for CMS-C in maize. Protoplasma 249, 1119–1127 (2012). https://doi.org/10.1007/s00709-011-0358-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00709-011-0358-2