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Plant Molecular Biology

, Volume 63, Issue 3, pp 405–417 | Cite as

Retrograde regulation of nuclear gene expression in CW-CMS of rice

  • Sota Fujii
  • Setsuko Komatsu
  • Kinya Toriyama
Article

Abstract

The CW-cytoplasmic male sterility (CMS) line has the cytoplasm of Oryza rufipogon Griff, and mature pollen is morphologically normal under an optical microscope but lacks the ability to germinate; restorer gene Rf17 has been identified as restoring this ability. The difference between nuclear gene expression in mature anthers was compared for the CW-CMS line, [cms-CW] rf17rf17, and a maintainer line with normal cytoplasm of Oryza sativa L., [normal] rf17rf17. Using a 22-k rice oligoarray we detected 58 genes that were up-regulated more than threefold in the CW-CMS line. Expression in other organs was further investigated for 20 genes using RT-PCR. Five genes, including genes for alternative oxidase, were found to be preferentially expressed in [cms-CW] rf17rf17 but not in [normal] rf17rf17 or [cms-CW] Rf17Rf17. Such [cms-CW] rf17rf17-specific gene expression was only observed in mature anthers but not in leaves, stems, or roots, indicating the presence of anther-specific mitochondrial retrograde regulation of nuclear gene expression, and that Rf17 has a role in restoring the ectopic gene expression. We also used a proteomic approach to discover the retrograde regulated proteins and identified six proteins that were accumulated differently. These results reveal organ-specific induced mitochondrial retrograde pathways affecting nuclear gene expression possibly related to CMS.

Keywords

Cytoplasmic male sterility ms-CW Oligoarray Oryza sativaOryza rufipogon Griff Proteome 

Abbreviations

CMS

cytoplasmic male sterility

Rf

fertility restorer gene

Notes

Acknowledgements

This study was partially supported by a grant from the Ministry of Agriculture, Forestry, and Fisheries of Japan (Green Technology Project QT-2007), and by a Grant-in-Aid for Special Research on Priority Areas (No. 18075002) from the Ministry of Education, Science, Sports, and Culture, Japan. S.F. is the recipient of Research Fellowships of the Japan Society for the promotion of Science for Young Scientists. We thank the Rice Genome Resource Center at the National Institute of Agrobiological Sciences, Japan, for use of the rice microarray analysis system and the technical support provided by Dr Nagamura and Mrs Motoyama.

Supplementary material

References

  1. Akagi H, Nakamura A, Yokozeki-Misono Y, Inagaki A, Takahashi H, Mori K, Fujimura T (2004) Positional cloning of the rice Rf-1 gene, a restorer of BT-type cytoplasmic male sterility that encodes a mitochondria-targeting PPR protein. Theor Appl Genet 108:1449–1457PubMedCrossRefGoogle Scholar
  2. Balk L, Leaver CJ (2001) The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release. Plant Cell 13:1803–1818PubMedCrossRefGoogle Scholar
  3. Becker JD, Boavida LC, Carneiro J, Haury M, Feijo JA (2003) Transcriptional profiling of Arabidopsis tissues reveals the unique characteristics of the pollen transcriptome. Plant Physiol 133:713–725PubMedCrossRefGoogle Scholar
  4. Bentolila S, Alfonso A, Hanson MR (2002) A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proc Natl Acad Sci USA 99:10887–10892PubMedCrossRefGoogle Scholar
  5. Bollenbach TJ, Stern DB (2003) Divalent metal-dependent catalysis and cleavage specificity of CSP41, a chloroplast endoribonuclease belonging to the short chain dehydrogenase/reductase superfamily. Nucleic Acids Res 31:4317–4325PubMedCrossRefGoogle Scholar
  6. Brown GG, Formanova N, Jin H, Wargachuk R, Dendy C, Patil P, Laforest M, Zhang J, Cheung WY, Landry BS (2003) The radish Rfo restorer gene Ogura cytoplasmic male sterility encode a protein with multiple pentatricopeptide repeats. Plant J 35:262–272PubMedCrossRefGoogle Scholar
  7. Butow RA, Avadhani NG (2004) Mitochondrial signaling: the retrograde response. Mol Cell 14:1–15PubMedCrossRefGoogle Scholar
  8. Cosgrove DJ, Bedinger P, Durachko DM (1997) Group I allergens of grass pollen as cell wall-loosening agents. Proc Natl Acad Sci USA 94:6559–6564PubMedCrossRefGoogle Scholar
  9. Cui X, Wise RP, Schnable PS (1996) The Rf2 nuclear restorer gene of male-sterile T-cytoplasm maize. Science 272:1334–1336PubMedCrossRefGoogle Scholar
  10. Diener C, Gaxiola A, Fink R (2001) Arabidopsis ALF5, a multidrug efflux transporter gene family member, confers resistance to toxins. Plant Cell 13:1477–1480CrossRefGoogle Scholar
  11. Djajanegara I, Finnegan PM, Mathieu C, McCabe T, Whelan J, Day DA (2002) Regulation of alternative oxidase gene expression in soybean. Plant Mol Biol 50: 735–742PubMedCrossRefGoogle Scholar
  12. Dojcinovic D, Krosting J, Harris AJ, Wagner DJ, Rhoads DM (2005) Identification of a region of the Arabidopsis AtAOX1a promoter necessary for mitochondrial retrograde regulation of expression. Plant Mol Biol 58:159–175PubMedCrossRefGoogle Scholar
  13. Fujii S, Toriyama K (2005) Molecular mapping of the fertility restorer gene for rice ms-CW-type cytoplasmic male sterility of rice. Theor Appl Genet 111:696–701PubMedCrossRefGoogle Scholar
  14. Geddy R, Mahe L, Brown GG (2004) Cell-specific regulation of a Brassica napus CMS-associated gene by a nuclear restorer with related effects on a floral homeotic gene promoter. Plant J 41:333–345CrossRefGoogle Scholar
  15. Gray GR, Maxwell DP, Villarimo AR, McIntosh L (2004) Mitochondria/nuclear signaling of alternative oxidase gene expression occurs through distinct pathways involving organic acids and reactive oxygen species. Plant Cell Rep 23:497–503PubMedCrossRefGoogle Scholar
  16. Hanson MR, Bentolila S (2004) Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16:S154–S169PubMedCrossRefGoogle Scholar
  17. Hilden L, Johansson G (2004) Recent developments on cellulases and carbohydrate-binding modules with cellulose affinity. Biotech Lett 26:1683–1693CrossRefGoogle Scholar
  18. Hochholdinger F, Guo L, Schnable PS (2004) Cytoplasmic regulation of the accumulation of nuclear-encoded proteins in the mitochondrial proteome of maize. Plant J 37:199–208PubMedGoogle Scholar
  19. Hony D, Twell D (2003) Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiol 132: 640–652CrossRefGoogle Scholar
  20. Karpova OV, Kuzmin EV, Elthon TE, Newton KJ (2002) Differential expression od alternative oxidase genes in maize mitochondrial mutants. Plant Cell 14:3271–3284PubMedCrossRefGoogle Scholar
  21. Katsuo K, Mizushima U (1958) Studies on the cytoplasmic difference among rice varieties, Oryza sativa L. 1. On the fertility of hybrids obtained reciprocally between cultivated and wild varieties. Japan J Breed 8:1–5Google Scholar
  22. Kazama T, Toriyama K (2003) A pentatricopeptide repeat-containing gene that promote the processing of abberant atp6 RNA of cytoplasmic male-sterile rice. FEBS Lett 544:99–102PubMedCrossRefGoogle Scholar
  23. Kobayashi Y, Yamamoto S, Minami H, Kagaya Y, Hattori T (2004) Differential activation of the rice sucrose nonfermenting1-related protein kinase2 family by hyperosmotic stress and abscisic acid. Plant Cell 16:1163–1177PubMedCrossRefGoogle Scholar
  24. Koizuka N, Imai R, Fujimoto H, Hayakawa T, Kimura Y, Kohno-Murase J, Sakai T, Kawasaki S, Imamura J (2003) Genetic characterization of pentatricopeptide repeat protein gene, orf687, that restores fertility in the cytoplasmic male-sterile Kosena radish. Plant J 34:407–415PubMedCrossRefGoogle Scholar
  25. Komori T, Ohta S, Murai N, Takakura Y, Kuraya Y, Suzuki S, Hiei Y, Imaseki H, Nitta N (2004) Map-based cloning of a fertility restorer gene, Rf-1 in rice (Oryza sativa L.). Plant J 37:315–325PubMedCrossRefGoogle Scholar
  26. Lee Y, Choi D, Kende H (2001) Expansins: ever-expanding numbers and functions. Curr Opin Plant Biol 4:527–532PubMedCrossRefGoogle Scholar
  27. Li Y, Jones L, McQueen-Mason S (2003) Expansins and cell growth. Curr Opin Plant Biol 6:603–610PubMedCrossRefGoogle Scholar
  28. Linke B, Nothnagel T, Borner T (2003) Flower development in carrot CMS plants: mitochondria affect the expression of MADS box genes homologous to GLOBOSA and DEFICIENS. Plant J 34:27–37PubMedCrossRefGoogle Scholar
  29. Marín-Rodríguez MC, Orchard J, Seymour GB (2002) Pectate lyases, cell wall degradation and fruit softening. J Exp Bot 377:2115–2119CrossRefGoogle Scholar
  30. Mascarenhas JP (1975) The biochemistry of angiosperm pollen development. Bot Rev 41:259–314Google Scholar
  31. Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325PubMedCrossRefGoogle Scholar
  32. O’Farrell PH (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250:4007–4021PubMedGoogle Scholar
  33. Park YW, Tominaga R, Sugiyama J, Furuta Y, Tanimoto E, Samejima M, Sakai F, Hayashi T (2003) Enhancement of growth by expression of poplar cellulase in Arabidopsis thaliana. Plant J 33:1099–1077PubMedCrossRefGoogle Scholar
  34. Pina C, Pinto F, Feijo JA, Becker JD (2005) Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiol 138:744–756PubMedCrossRefGoogle Scholar
  35. Rodriguez-Concepcion R, Yalovsky S, Zik M, Fromm H, Gruissem W (1999) The prenylation status of a novel plant calmodulin directs plasma membrane or nuclear localization of the protein. EMBO J 18:1996–2007PubMedCrossRefGoogle Scholar
  36. Sekito T, Thomson J, Butow RA (2000) Mitochondria-to-nuclear signaling is regulated by the subcellular localization of the transcription factors Rtg1p and Rtg3p. Mol Biol Cell 11:2103–2115PubMedGoogle Scholar
  37. Siedow JN, Umbach AL (2000) The mitochondrial cyanide-resistant oxidase: structural conservation amid regulatory diversity. Biochim Biophys Acta 1459:432–439PubMedCrossRefGoogle Scholar
  38. Tanaka N, Fujita M, Handa H, Murayama S, Uemura M, Kawamura Y, Mitsui T, Mikami S, Tozawa Y, Yoshinaga T, Komatsu S (2004) Proteomics of the rice cell: systematic identification of the protein populations in subcellular compartments. Mol Gen Genom 271:566–576CrossRefGoogle Scholar
  39. Teixeira RT, Farbos I, Glimelius K (2005) Expression levels of meristem identity and homeotic genes are modified by nuclear-mitochondrial interactions in alloplasmic male-sterile lines of Brassica napus. Plant J 42:731–742PubMedCrossRefGoogle Scholar
  40. Toriyama K, Hinata K (1987) Anther culture application to breeding of a restorer for male-sterile cytoplasm of wild rice [ms-CW]. Jpn J Breed 37:469–473Google Scholar
  41. Wang Z, Zou Y, Li X, Zhang Q, Chen L, Wu H, Su D, Chen Y, Guo J, Luo D, Long Y, Zhong Y, Liu YG (2006) Cytoplasmic male sterility of rice with Boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing. Plant Cell 18:676–687PubMedCrossRefGoogle Scholar
  42. Wastl J, Duin C, Iuzzolino L, Dorner W, Link T, Hoffmann S, Sticht H, Dau H, Lingelbach K, Maier G (2000) Eukaryotically encoded and chloroplast-located rubredoxin is associated with photosystem II. J Biol Chem 275:30058–30063PubMedCrossRefGoogle Scholar
  43. Zubko MK (2004) Mitochondrial turning fork in nuclear homeotic functions. Trends Plant Sci 9:61–64PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  1. 1.Laboratory of Environmental Biotechnology, Graduate School of Agricultural ScienceTohoku UniversitySendaiJapan
  2. 2.Laboratory of Gene Regulation, Department of Molecular GeneticsNational Institute of Agrobiological SciencesTsukubaJapan

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