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DNA methylation affected by male sterile cytoplasm in rice (Oryza sativa L.)

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Abstract

Male sterile cytoplasm plays an important role in hybrid rice, and cytoplasmic effects are sufficiently documented. However, no reports are available on DNA methylation affected by male sterile cytoplasm in hybrid rice. We used a methylation-sensitive amplified polymorphism technique to characterize DNA methylation in four male sterile cytoplasms that are widely commercialized in China. In total, 12 pairs of selective primers in combinations of EcoRI and MspI/HpaII amplified 350 bands among four male sterile (A) lines and the corresponding maintainer (B) lines. Sites b1 and b3 were fully methylated only in all the B lines, while b2 was fully methylated only in all the A lines. These results implied a relationship of DNA methylation at these sites specifically with male sterile cytoplasms, as well as male sterility, since the only difference between the A and B lines was the cytoplasm. The DNA methylation was markedly affected by male sterile cytoplasms. WA-type and Yinshui-type cytoplasms affected the methylation to a much greater degree than G-type and D-type cytoplasms, as indicated by the number and degree of methylated sites, ratio of methylated sites, number of fully methylated sites, ratio of fully methylated sites, and polymorphism between A and B lines for these cytoplasms. The genetic distance between the cytoplasm and nucleus for the WA-type is much greater than for G- and D-types because the former is between wild and cultivated species and the latter is within indica subspecies between African and Asian cultivars. This difference in genetic distance may be responsible for the variation in methylation which we observed.

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References

  • Ashikawa I (2001) Surveying CpG methylation at 5′-CCGG in the genomes of rice cultivars. Plant Mol Biol 45:31–39

    Article  PubMed  CAS  Google Scholar 

  • Cervera MT, Ruiz-García L, Martínez-Zapater JM (2002) Analysis of DNA methylation in Arabidopsis thaliana based on methylation-sensitive AFLP markers. Mol Genet Genomics 268:543–552

    Article  PubMed  CAS  Google Scholar 

  • Chakrabarty D, Yu KW, Paek KY (2003) Detection of DNA methylation changes during somatic embryogenesis of Siberian ginseng (Eleuterococcus senticosus). Plant Sci 165:61–68

    Article  CAS  Google Scholar 

  • Cheng S, Cao L, Yang S, Zhai H (2004) Forty years’ development of hybrid rice: China’s experience. Rice Sci 11:225–230

    Google Scholar 

  • Cheng SH, Zhuang JY, Fan YY, Du JH, Cao LY (2007a) Progress in research and development on hybrid rice: a super-domesticate in China. Ann Bot 100:959–966

    Article  PubMed  Google Scholar 

  • Cheng S, Cao L, Zhuang J, Chen S, Zhan X, Fan Y, Zhu D, Min S (2007b) Super hybrid rice breeding in china: achievements and prospects. J Integr Plant Biol 49:805–810

    Article  CAS  Google Scholar 

  • Dalmacio R, Brar DS, Ishii T, Sitch LA, Virmani SS, Khush GS (1995) Identification and transfer of a new cytoplasmic male sterility source from Oryza perennis into indica rice (O. sativa). Euphytica 82:221–225

    Article  Google Scholar 

  • Deng Y, Xiao C, Zhang H, Deng X, Zhou P, Deng H (2010) A preliminary study on floral and stigma exsertion characters of II-32A/B. Hybrid Rice 25:73–75

    Google Scholar 

  • Finnegan EJ (1996) The role of DNA methylation in plant development. In: Russo VEA, Martienssen RA, Riggs AD (eds) Epigenetic mechanism of gene regulation. Cold Spring Harbor Laboratory Press, New York, pp 127–140

    Google Scholar 

  • Fraga MF, Esteller M (2002) DNA methylation: a profile of methods and applications. Biotechniques 33:632–649

    PubMed  CAS  Google Scholar 

  • Gao L, Xia Z, Jiang G, Peng H, Zhao X, Zhai W (2011) Generation of marker-free, bacterial blight-resistant transgenic sterile line and hybrid rice with Xa21. Plant Breed 130:438–443

    Article  CAS  Google Scholar 

  • Giegéa P, Sweetloveb LJ, Cognata V, Leaverb CJ (2005) Coordination of nuclear and mitochondrial genome expression during mitochondrial biogenesis in Arabidopsis. Plant Cell 17:1497–1512

    Article  Google Scholar 

  • Huang W, Wang L, Yi P, Tan XL, Zhang XM, Zhang ZJ, Li YS, Zhu YG (2006) RFLP analysis for mitochondrial genome of CMS-rice. Acta Genet Sin 33:330–338. doi:10.1016/s0379-4172(06)60058-9

    Article  PubMed  CAS  Google Scholar 

  • Johannes F, Colot V, Jansen RC (2008) Epigenome dynamics: a quantitative genetics perspective. Nat Rev Genet 9:883–889

    Article  PubMed  CAS  Google Scholar 

  • Kinoshita T (1997) Gene symbols and information on male sterility. Rice Genet Newslett 14:13–22

    Google Scholar 

  • Li S (1997) Breeding, utilization and genetic study on G-type and D-type hybrid rice. Hybrid Rice 12:1–25 (in Chinese with English abstract)

    Google Scholar 

  • Li J, Yuan L (2010) Hybrid rice: genetics, breeding, and seed production. Plant breeding reviews. Wiley, New York, pp 15–158

  • Li L, Zhou H, Zhan X, Zhuang J, Cheng S (2007) Mapping of rice fettility restoring gene for Yinshui cytoplasmic male sterility in a restorer line R68. Chin J Rice Sci 21:547–549

    CAS  Google Scholar 

  • Li X, Wang X, He K, Ma Y, Su N, He H, Stolc V, Tongprasit W, Jin W, Jiang J, Terzaghi W, Li S, Deng XW (2008) High-resolution mapping of epigenetic modifications of the rice genome uncovers interplay between DNA methylation, histone methylation, and gene expression. Plant Cell 20:259–276

    Article  PubMed  CAS  Google Scholar 

  • Ng HH, Adrian B (1999) DNA methylation and chromatin modification. Curr Opin Genet Devel 9:158–163

    Article  CAS  Google Scholar 

  • Noyer JL, Causse S, Tomekpe K, Bouet A, Baurens FC (2005) A new image of plantain diversity assessed by SSR, AFLP and MSAP markers. Genetica 124:61–69. doi:10.1007/s10709-004-7319-z

    Article  PubMed  CAS  Google Scholar 

  • Ou L, Huang G, Li W, Kang G, Chen J, Luan S, Chen L (2009) Chloroplast DNA polymorphism in different types of cytoplasmic male sterile rice. Biol Plant 53:593–596. doi:10.1007/s10535-009-0108-x

    Article  CAS  Google Scholar 

  • Peng H, Kan D (2002) A summary of the techniques for Gang 46A to achieve high yield and quality in its multiplication and hybrid seed production. Hybrid Rice 17:28–29

    Google Scholar 

  • Peng S, Cassman KG, Virmani SS, Sheehy J, Khush GS (1998) Yield potential trends of tropical rice since the release of IR8 and the challenge of increasing rice yield potential. Crop Sci 39:1552–1559

    Article  Google Scholar 

  • Peraza-Echeverria S, Herrera-Valencia VA, Kay A (2001) Detection of DNA methylation changes in micropropagated banana plants using methylation-sensitive amplification polymorphism (MSAP). Plant Sci 161:359–367

    Article  PubMed  CAS  Google Scholar 

  • Reyna-López GE, Simpson J, Ruiz-Herrera J (1997) Differences in DNA methylation patterns are detectable during the dimorphic transition of fungi by amplification of restriction polymorphisms. Mol Gen Genet MGG 253:703–710

    Article  Google Scholar 

  • Salmon A, Clotault J, Jenczewski E, Chable V, Manzanares-Dauleux MJ (2008) Brassica oleracea displays a high level of DNA methylation polymorphism. Plant Sci 174:61–70

    Article  CAS  Google Scholar 

  • Sha AH, Lin XH, Huang JB, Zhang DP (2005) Analysis of DNA methylation related to rice adult plant resistance to bacterial blight based on methylation-sensitive AFLP (MSAP) analysis. Mol Genet Genomics 273:484–490

    Article  PubMed  CAS  Google Scholar 

  • Virmani SS, Ilyas-Ahmed M (2001) Environment-sensitive genic male sterility (EGMS) in crops. Advances in Agronomy. Academic Press, New York, pp 139–195

    Google Scholar 

  • Wang F (1990) The method of estimating the genetic effects of cytoplasm, nucleus and nucleo-cytoplasmic interacton in three-line hybrid rice. J Southwest Agric Univ 12:418–425 (in Chinese with English abstract)

    Google Scholar 

  • Wang W, Zhou K, Wen H (1997) The diversity of cytoplasmic effects on some quantitative traits in hybrid rice. Chin J Rice Sci 11:65–69 (in Chinese with English abstract)

    Google Scholar 

  • Wang Z, Zou Y, Li X, Zhang Q (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 18:676–687

    Article  PubMed  CAS  Google Scholar 

  • Wang WS, Pan YJ, Zhao XQ, Dwivedi D, Zhu LH, Ali J, Fu BY, Li ZK (2011) Drought-induced site-specific DNA methylation and its association with drought tolerance in rice (Oryza sativa L.). J Exp Bot 62:1951–1960

    Article  PubMed  CAS  Google Scholar 

  • Woodson JD, Chory J (2008) Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet 9:383–395

    Article  PubMed  CAS  Google Scholar 

  • Wu X (2008) Prospects of developing hybrid rice with super high yield. Agron J 101:688–695

    Article  Google Scholar 

  • Xia S, Li Y (1992) The breeding of male sterile line Jin 23A. Hybrid Rice 29–31 (in Chinese with English abstract)

  • Xiong LZ, Xu CG, Saghai Maroof MA, Zhang Q (1999) Patterns of cytosine methylation in an elite rice hybrid and its parental lines, detected by a methylation-sensitive amplification polymorphism technique. Mol Gen Genet 261:439–446

    Article  PubMed  CAS  Google Scholar 

  • Xu M, Li X, Korban S (2000) AFLP-based detection of DNA methylation. Plant Mol Biol Rep 18:361–368

    Article  CAS  Google Scholar 

  • Xu JF, Jiang L, Wei XJ, Zhang WW, Liu SJ, Chen LM, Wang CM, Luo LG, Wan JM (2006) Genotyping the heading date of male-sterile rice line II-32A. J Integr Plant Biol 48:440–446

    Article  CAS  Google Scholar 

  • Young JB, Virmani SS (1990) Effects of cytoplasm on heterosis and combining ability for agronomic traits in rice (Oryza sativa L.). Euphytica 48:177–188

    Article  Google Scholar 

  • Yuan L (1974) A report on development of three lines in hybrid rice through wild abortive rice. Hunan Agric Sci 4:13–19 (in Chinese with English abstract)

    Google Scholar 

  • Yuan L (1990) Progress of two-line system hybrid rice breeding. Agric Sci China 23:1–6 (in Chinese with English abstract)

    Google Scholar 

  • Zeng Q, Zhou K, Zhu Z, Luo Q (2000) Current status in the use of hybrid rice heterosis in China. Chin J Rice Sci 14:243–246 (in Chinese with English abstract)

    Google Scholar 

  • Zhang H, Peng H, Li Y, Xu P, Wang X, Wu X (2006) Patterns of DNA cytosine methylation between haploids and corresponding diploids in rice. Chin Sci Bull 51:1721–1728

    Article  CAS  Google Scholar 

  • Zhang C, Qi L, Hou X, Shi G, Zhang J (2010a) Differential gene expression analysis of a new Ogura CMS line and its maintainer in non-heading Chinese cabbage by cDNA-AFLP. Acta Physiol Plant 32:781–787

    Article  CAS  Google Scholar 

  • Zhang M, Kimatu JN, Xu K, Liu B (2010b) DNA cytosine methylation in plant development. J Genet Genomics 37:1–12

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Anna M. McClung and Ellen McWhirter for critical review. This work was financially supported by the National Natural Science Foundation of China (31100879).

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Correspondence to Wengui Yan or Xianjun Wu.

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Xu, P., Yan, W., He, J. et al. DNA methylation affected by male sterile cytoplasm in rice (Oryza sativa L.). Mol Breeding 31, 719–727 (2013). https://doi.org/10.1007/s11032-012-9829-1

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