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Fertility restoration mechanisms in S-type cytoplasmic male sterility of maize (Zea mays L.) revealed through expression differences identified by cDNA microarray and suppression subtractive hybridization

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Abstract

Cytoplasmic male sterility (CMS) is thought to be due to an incompatibility of 2 genomes that results in pollen abortion. In CMS-S of maize (Zea mays L.), mitochondrialorf355-orf77 and the nuclear restorer of fertility interact to control fertility of gametophytes. Numerous studies demonstrated thatRf3 can regulate nuclear and mitochondrial gene expression and shows pleiotropic effects on the transcriptional level. Little is known, however, about the alteration of the global expression profile caused byRf3 substitution ofrf3 under S cytoplasm or about molecular fertility restoration mechanisms. In this study, cDNA microarray and suppression subtractive hybridization were used to reveal differentially expressed genes during pollen development by comparing a set ofRf3/rf3 near isogenic lines. A total of 137 tentative unique genes (TUGs) were identified at the transcriptional level. On the basis of functional category analysis, these TUGs were involved in a broad range of cellular and biochemical activities, including metabolism, cell structure, cell defense, and apoptosis, as well as signal transduction pathways. Northern blot analysis using 5 representative clones as probes confirmed differential expression among S-(Rf3) and S-(rf3). Especially in S-(Rf3), the expression patterns of genes associated with electron or H+ conduction and antiapoptosis genes (e.g., VADC2, BI-1, cystatin, 14-3-3) are distinctly different from in S-(rf3). Together with normalization of cellular and biochemical activities in S-(Rf3), we proposed thatRf3 might regulate accumulation of nuclear and mitochondrial gene transcripts directly or indirectly to inhibit multiple programmed cell death pathways in S-type cytoplasm allowing the normal developmental pathways to unfold.

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Abbreviations

AdoMetDC:

adenosylmethionine decarboxylase

BI-1:

Bax-inhibitor

CDPK:

calcium-dependent protein kinase

CMS:

cytoplasmic male sterility

CP:

collapsed pollen

ESTs:

expressed sequence tags

LV:

large-vacuolated microspores

NIL:

near-isogenic line

ORF:

open-reading frame

PCD:

programmed cell death

PCR:

polymerase chain reaction

SF:

starch filling pollen

SSH:

suppression subtractive hybridization

SSR:

single sequence repeat

SV:

small-vacuolated microspores

TUGs:

tentative unique genes

VDAC:

voltage-dependent anion channel protein

References

  • Abe M, Abe K, Domoto C, and Arai S (1995) Two distinct species of corn cystatin in corn kernels. Biosci Biotechnol Biochem 59: 756–758.

    Article  PubMed  CAS  Google Scholar 

  • Anjanasree KN and Bansal KC (2003) Isolation and characterization of ripening-related expansin cDNA from tomato. J Plant Biochem Biotechnol 12: 31–35.

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Bedinger PA and Edgerton MD (1990) Developmental staging of maize microspores reveals a transition in developing microspore proteins. Plant Physiol 92: 474–479.

    Article  PubMed  CAS  Google Scholar 

  • Bentolila S, Alfonso AA, and Hanson MR (2002) A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proc Natl Acad Sci USA 99: 10887–10892.

    Article  PubMed  CAS  Google Scholar 

  • Bitar FA, Roosens N, Smeyers M, Vauterin M, Van Boxtel J, Jacobs M, and Hombl F (2003) Sequence analysis, transcriptional and posttranscriptional regulation of the rice VDAC family. Biochim Biophys Acta 1625: 43–45.

    Article  PubMed  Google Scholar 

  • Buchert JG (1961) The stage of the genome-plasmon interaction in the restoration of fertility to cytoplasmically pollen-sterile maize. Proc Natl Acad Sci USA 47: 1436–1440.

    Article  Google Scholar 

  • Chase CD, Wen L, Gallagher L, Jamoom E, and Ortega V (2001) Programmed cell death in male-sterile maize. Maize Genetics Conference Abstracts 43: T17.

    Google Scholar 

  • Cheng EH, Sheiko TV, Fisher JK, Craigen WJ, and Korsmeyer SJ (2003) VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science 301: 513–517.

    Article  PubMed  CAS  Google Scholar 

  • Chiang C, Kanies C, Kim KW, Fang WB, Parkhurst C, Xie M, Henry T, and Yang E (2003) Protein phosphatase 2A dephosphorylation of phosphoserine 112 plays the gatekeeper role for BAD-mediated apoptosis. Mol Cell Biol 23: 6350–6362.

    Article  PubMed  CAS  Google Scholar 

  • Cosgrove DJ, Bedinger P, and Durachko DM (1997) Group I allergens of grass pollen as cell wall-loosening agents. Proc Natl Acad Sci USA 94: 6559–6564.

    Article  PubMed  CAS  Google Scholar 

  • Cui XQ, Wise RP, and Schnable PS (1996) The rf2 nuclear restore gene of male-sterile-cytoplasm maize. Science 272: 1334–1336.

    Article  PubMed  CAS  Google Scholar 

  • Datta R, Chamusco KC, and Chourey PS (2002) Starch biosynthesis during pollen maturation is associated with altered patterns of gene expression in maize. Plant Physiol 130: 1645–1656.

    Article  PubMed  CAS  Google Scholar 

  • Datta R, Chourey PS, Pring DR, and Tang HV (2001) Gene-expression analysis of sucrose-starch metabolism during pollen maturation in cytoplasmic male-sterile and fertile lines of sorghum. Sex Plant Reprod 14: 127–134.

    Article  CAS  Google Scholar 

  • Dill CJ, Wise RP, and Schnable PS (1997)Rf8 andRf mediate unique T-urf13-transcript accumulation, revealing a mitochondrial consensus sequence associated with RNA processing and restoration of pollen fertility in T-cytoplasm maize. Genetics 147: 1367–1379.

    PubMed  CAS  Google Scholar 

  • Duvick DN (1965) Cytoplasmic pollen sterility in corn. Adv Genet 13: 1–56.

    Article  Google Scholar 

  • Evans PT and Malmberg RL (1989) Do polyamines have roles in plant development? Annu Rev Plant Physiol Plant Mol Biol 40: 235–269.

    Article  CAS  Google Scholar 

  • Frank SA and Barr CM (2003) Programmed cell death and hybrid incompatibility. J Hered 94(2): 181–3.

    Article  PubMed  CAS  Google Scholar 

  • Gabay-Laughnan S, Chase CD, Ortega VM, and Zhao L (2004) Molecular-genetic characterization of CMS-S restorer-of-fertility alleles identified in Mexican maize and teosinte. Genetics 166: 959–970.

    Article  PubMed  CAS  Google Scholar 

  • Gracen VE and Grogan CO (1974) Diversity and suitability for hybrid production of different sources of cytoplasmic male sterility in maize. Agron J 66: 654–657.

    Article  Google Scholar 

  • Greenberg JT (1996) Programmed cell death: a way of life for plants. Proc Natl Acad Sci USA 93: 12094–12097.

    Article  PubMed  CAS  Google Scholar 

  • Hückelhoven R, Dechert C, and Kogel K (2003) Overexpression of barley BAX inhibitor 1 induces breakdown of mlo-mediated penetration resistance toBlumeria graminis. Proc Natl Acad Sci USA 100: 5555–5560.

    Article  PubMed  Google Scholar 

  • Kamps TL and Chase CD (1997) RFLP mapping of the maize gametophytic restorer-of-fertility locus (rf3) and aberrant pollen transmission of the nonrestoring rf3 allele. Theor Appl Genet 95: 525–531.

    Article  CAS  Google Scholar 

  • Kawai M, Pan L, Reed JC, and Uchimiya H (1999) Evolutionally conserved plant homologue of the Bax inhibitor-1 (BI-1) gene capable of suppressing Bax-induced cell death in yeast. FEBS Lett 464: 143–147.

    Article  PubMed  CAS  Google Scholar 

  • Kazama T and Toriyama KA (2003) Pentatricopeptide repeat-containing gene that promotes the processing of aberrant atp6 RNA of cytoplasmic male-sterile rice. FEBS Lett 544: 99–102.

    Article  PubMed  CAS  Google Scholar 

  • Ku S, Yoon H, Suh HS, and Chung YY (2003) Male-sterility of thermosensitive genic male-sterile rice is associated with premature programmed cell death of the tapetum. Planta 217: 559–565.

    Article  PubMed  CAS  Google Scholar 

  • Kumar A, Taylor MA, Mad-Arif SA, and Davies HV (1996) Potato plants expressing antisenseS-adenosylmethionine decarboxylase (SAMDC) transgenes show altered levels of polyamines and ethylene: antisense plants displayed abnormal phenotypes. Plant J 9: 147–158.

    Article  CAS  Google Scholar 

  • Laughnan JR and Gabay SJ (1978) Nuclear and cytoplasmic mutation to fertility in S male-sterile maize. In: Walden DB (ed), Maize Breeding and Genetics, pp 427–477, J. Wiley & Sons, New York.

    Google Scholar 

  • Laughnan JR and Gabay-Laughnan S (1983) Cytoplasmic male sterility in maize. Annu Rev Genet. 17: 27–48.

    Article  PubMed  CAS  Google Scholar 

  • Lawen A (2003) Apoptosis—an introduction. Bioessays 25: 888–896.

    Article  PubMed  CAS  Google Scholar 

  • Liu F X, Cui H, Horner T, Weiner H, and Schnable PS (2001) Mitochondrial aldehyde dehydrogenase activity is required for male fertility in maize. Plant Cell 13: 1063–1078.

    PubMed  CAS  Google Scholar 

  • Mandaron P, Niogret MF, Mache R, and Moneger F (1990) In vitro protein synthesis in isolated microspores ofZea mays at several stages of development. Theor Appl Genet 80: 134–138.

    Article  CAS  Google Scholar 

  • Rhee CH, Hess K, Jabbur J, Ruiz M, Yang Y, Chen S, Chenchik A, Fuller GN, and Zhang W (1999) cDNA expression array reveals heterogeneous gene expression profiles in three glioblastoma cell lines. Oncogene 18: 2711–2717.

    Article  PubMed  CAS  Google Scholar 

  • Riggio LB, Siripant MN, and Chase CD (2004) Nuclease and protease activities associated with pollen collapse in S male-sterile maize. Available at: http://abstracts.aspb.org/pb2004/public/P47/7186.html. Accessed March 9, 2005.

  • Rodriguez PL (1998) Protein phosphatase (PP2C) function in higher plants. Plant Mol Biol 38: 919–927.

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J and Russell DW (2001) Molecular Cloning: A Laboratory Manual, 3rd ed, Cold Spring Harbor Laboratory Press, Cold Spring Harbor New York.

    Google Scholar 

  • Schnable PS and Wise RP (1998) The molecular basis of cytoplasmic male sterility and fertility restoration. Trends Plant Sci 3: 176–180.

    Article  Google Scholar 

  • Solomon M, Belenghi B, Delledonne M, Menachem E, and Levine A (1999) The involvemen of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell 11: 431–443.

    PubMed  CAS  Google Scholar 

  • Wen L and Chase CD (1999a) Pleiotropic effects of a nuclear restorer-of-fertility locus on mitochondrial transcripts in male-fertile and S male-sterile maize. Curr Genet 35: 521–526.

    Article  PubMed  CAS  Google Scholar 

  • Wen L and Chase CD (1999b) Mitochondrial gene expression in developing male gametophytes of male-fertile and S male-sterile maize. Sex Plant Reprod 11: 323–330.

    Article  CAS  Google Scholar 

  • Wen L, Ruesch KL, Ortega VM, Kamps TL, Gabay-Laughnan S, and Chase CD (2003) A nuclear restorer-of-fertility mutation disrupts accumulation of mitochondrial ATP synthase subunit-α in developing pollen of S male-sterile maize. Genetics 165: 771–779.

    PubMed  CAS  Google Scholar 

  • Wu HM and Cheung AY (2000) Programmed cell death in plant reproduction. Plant Mol Biol 44: 267–281.

    Article  PubMed  Google Scholar 

  • Xia JH and Zheng YL (2002) Molecular marker-assisted backcross breeding of maize Rf3 NIL and its efficient analysis. Acta Agromica Sinica 28: 339–344.

    Google Scholar 

  • Xu L, Hui L, Wang S, Gong J, Jin Y, Wang Y Ji Y, Wu X, Han Z, and Hu G (2001) Expression profiling suggested a regulatory role of liver-enriched transcription factors in human hepatocellular carcinoma. Cancer Res 61: 3176–3181.

    PubMed  CAS  Google Scholar 

  • Yaffe MB (2002) How do 14-3-3 proteins work? Gatekeeper phosphorylation and the molecular anvil hypothesis. FEBS Lett 513: 53–57.

    Article  PubMed  CAS  Google Scholar 

  • Yamada T, Ohta H, Shinohara A, Iwamatsu A, Shimada H, Tsuchiya T, Masuda T, and Takamiya K (2000) A cysteine protease from maize isolated in a complex with cystatin. Plant Cell Physiol 41: 185–191.

    Article  PubMed  CAS  Google Scholar 

  • Yi L, Jones L, and McQueen-Mason S (2003) Expansins and cell growth. Curr Opin Plant Biol 6: 603–610.

    Article  Google Scholar 

  • Zabala G, Gabay-Laughnan S, and Laughnan JR (1997) The nuclear geneRf3 affects the expression of the mitochondrial chimeric sequence R implicated in S-type male-sterility in maize. Genetics 147: 847–860.

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, 430070, Wuhan, PR China

    Zuxin Zhang, Wanhu Tang, Fangdong Zhang & Yonglian Zheng

  2. College of Agronomy, Hubei Agricultural University, 071000, Baoding, PR China

    Zuxin Zhang

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  1. Zuxin Zhang
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  2. Wanhu Tang
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Zhang, Z., Tang, W., Zhang, F. et al. Fertility restoration mechanisms in S-type cytoplasmic male sterility of maize (Zea mays L.) revealed through expression differences identified by cDNA microarray and suppression subtractive hybridization. Plant Mol Biol Rep 23, 17–38 (2005). https://doi.org/10.1007/BF02772644

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