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Tissue culture-induced variation at simple sequence repeats in sorghum (Sorghum bicolor L.) is genotype-dependent and associated with down-regulated expression of a mismatch repair gene, MLH3

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Abstract

Somaclonal variation is a common phenomenon associated with plant tissue culture. Microsatellites or simple sequence repeats (SSRs) are ubiquitous components of eukaryotic genomes, and are intrinsically unstable under various stress conditions including tissue culture. Here, we assessed genetic stability of a set of 29 mapped SSR loci in calli and regenerated plants derived from a pair of reciprocal sorghum inter-strain F1 hybrids and their pure line parents. We further measured the steady-state transcripts of a set of nine mismatch repair (MMR)-encoding genes and a DEMETER (DME), a DNA glycosylase domain protein-encoding gene in these lines, and tested for a possible relationship between altered expression of a given MMR or DME gene and the SSR variations. We found that SSR variations occurred in calli and regenerated plants of both the studied pure lines though at sharply different frequencies (20.7 vs. 6.9%), but no variation was detected in calli and regenerated plants of the pair of F1 hybrids. Compared with the donor seed plants, markedly altered expression of all nine studied MMR genes and the DME gene was observed in calli, and more conspicuously, in the regenerated plants. However, only one gene, i.e., MLH3, showed an altered expression pattern that is genotype specific and significantly correlated with the occurrence of SSR instability.

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References

  • Bertagnolli MM, Niedzwiecki D, Compton CC, Hahn HP, Hall M, Damas B, Jewell SD, Mayer RJ, Goldberg RM, Saltz LB, Warren RS, Redston M (2009) Microsatellite instability predicts improved response to adjuvant therapy with irinotecan, fluorouracil, and leucovorin in stage III colon cancer: cancer and leukemia group B protocol 89803. J Clin Oncol 27:1814–1821

    Article  CAS  PubMed  Google Scholar 

  • Boyko A, Kovalchuk I (2008) Epigenetic control of plant stress response. Environ Mol Mutagen 49:61–72

    Article  CAS  PubMed  Google Scholar 

  • Chowdari KV, Ramakrishna W, Tamhankar SA, Hendre RR, Gupta VS, Sahasrabudhe NA, Ranjekar PK (1998) Identification of minor DNA variations in rice somaclonal variants. Plant Cell Rep 18:55–58

    Article  CAS  Google Scholar 

  • Gao DY, Vallejo VA, He B, Gai YC, Sun LH (2009) Detection of DNA changes in somaclonal mutants of rice using SSR markers and transposon display. Plant Cell Tissue Org Cult 98:187–196

    Article  CAS  Google Scholar 

  • Haugen AC, Goel A, Yamada K, Marra G, Nguyen TP, Nagasaka T, Kanazawa S, Koike J, Kikuchi Y, Zhong X, Arita M, Shibuya K, Oshimura M, Hemmi H, Boland CR, Koi M (2008) Genetic instability caused by loss of MutS homologue 3 in human colorectal cancer. Cancer Res 68:8465–8472

    Article  CAS  PubMed  Google Scholar 

  • Joyce SM, Cassells AC, Jain SM (2003) Stress and aberrant phenotypes in in vitro culture. Plant Cell Tissue Org 74:103–121

    Article  CAS  Google Scholar 

  • Kaeppler SM, Kaeppler HF, Rhee Y (2000) Epigenetic aspects of somaclonal variation in plants. Plant Mol Biol 43:179–188

    Article  CAS  PubMed  Google Scholar 

  • Krizova K, Fojtova M, Depicker A, Kovarik A (2009) Cell culture-induced gradual and frequent epigenetic reprogramming of invertedly repeated tobacco transgene epialleles. Plant Physiol 149:1493–1504

    Article  CAS  PubMed  Google Scholar 

  • Larkin PJ, Scowcroft WR (1981) Somaclonal variation—a novel source of variability from cell cultures for plant improvement. Theor Appl Genet 60:197–214

    Article  Google Scholar 

  • Luo X, Fu Y, Zhang P, Wu S, Tian F, Liu J, Zhu Z, Yang J, Sun C (2009) Additive and over-dominant effects resulting from epistatic loci are the primary genetic basis of heterosis in rice. J Integr Plant Biol 51:393–408

    Article  Google Scholar 

  • Madlung A, Comai L (2004) The effect of stress on genome regulation and structure. Ann Bot 94:481–495

    Article  CAS  PubMed  Google Scholar 

  • Marum L, Rocheta M, Maroco J, Oliveira MM, Miguel C (2009) Analysis of genetic stability at SSR loci during somatic embryogenesis in maritime pine (Pinus pinaster). Plant Cell Rep 28:673–682

    Article  CAS  PubMed  Google Scholar 

  • McClintock B (1984) The significance of responses of the genome to challenge. Science 226:792–801

    Article  CAS  PubMed  Google Scholar 

  • Mohan Jain S (2001) Tissue culture-derived variation in crop improvement. Euphytica 118:153–166

    Article  Google Scholar 

  • Nag DK, Suri M, Stenson EK (2004) Both CAG repeats and inverted DNA repeats stimulate spontaneous unequal sister-chromatid exchange in Saccharomyces cerevisiae. Nucleic Acids Res 32:5677–5684

    Article  CAS  PubMed  Google Scholar 

  • Phillips RL, Kaeppler SM, Olhoft P (1994) Genetic instability of plant tissue cultures: breakdown of normal controls. Proc Natl Acad Sci USA 91:5222–5226

    Article  CAS  PubMed  Google Scholar 

  • Rahman MH, Rajora OP (2001) Microsatellite DNA somaclonal variation in micropropagated trembling aspen (Populus tremuloides). Plant Cell Rep 20:531–536

    Article  CAS  Google Scholar 

  • Rodríguez López CM, Wetten AC, Wilkinson MJ (2004) Detection and quantification of in vitro-culture induced chimerism using simple sequence repeat (SSR) analysis in Theobroma cacao (L.). Theor Appl Genet 110:157–166

    Article  PubMed  Google Scholar 

  • Ryu TH, Yi SI, Kwon YS, Kim BD (2007) Microsatellite DNA somaclonal variation of regenerated plants via cotyledon culture of hot pepper (Capsicum annuum L.). Kor J Genet 29:459–464

    CAS  Google Scholar 

  • Schellenbaum P, Mohler V, Wenzel G, Walter B (2008) Variation in DNA methylation patterns of grapevine somaclones (Vitis vinifera L.). BMC Plant Biol 8:78. doi:10.1186/1471-2229-8-78

    Article  PubMed  Google Scholar 

  • Tanurdzic M, Vaughn MW, Jiang H, Lee TJ, Slotkin RK, Sosinski B, Thompson WF, Doerge RW, Martienssen RA (2008) Epigenomic consequences of immortalized plant cell suspension culture. PLoS Biol 6:2880–2895

    Article  CAS  PubMed  Google Scholar 

  • Varshney RK, Graner A, Sorrells ME (2005) Genic microsatellite markers in plants: features and applications. Trend Biotechnol 23:48–55

    Article  CAS  Google Scholar 

  • Vilar E, Scaltriti M, Balmãa J, Saura C, Guzman M, Arribas J, Baselga J, Tabernero J (2008) Microsatellite instability due to hMLH1 deficiency is associated with increased cytotoxicity to irinotecan in human colorectal cancer cell lines. Br J Cancer 99:1607–1612

    Article  CAS  PubMed  Google Scholar 

  • Wang HY, Chai Y, Chu XC, Zhao YY, Wu Y, Zhao JH, Ngezahayo F, Xu CM, Liu B (2009) Molecular characterization of a rice mutator-phenotype derived from an incompatible cross-pollination reveals transgenerational mobilization of multiple transposable elements and extensive epigenetic instability. BMC Plant Biol 9. doi:10.1186/1471-2229-9-63

  • Wu YQ, Huang Y (2007) An SSR genetic map of Sorghum bicolor (L.) Moench and its comparison to a published genetic map. Genome 50:84–89

    Article  CAS  PubMed  Google Scholar 

  • Wu SY, Culligan K, Lamers M, Hays J (2003) Dissimilar mispair-recognition spectra of Arabidopsis DNA-mismatch-repair proteins MSH2·MSH6 (Musα) and MSH2·MSH7 (Musγ). Nucleic Acids Res 31:6027–6034

    Article  CAS  PubMed  Google Scholar 

  • Yu J, Mallon MA, Zhang W, Freimuth RR, Marsh S, Watson MA, Goodfellow PJ, McLeod HL (2006) DNA repair pathway profiling and microsatellite instability in colorectal cancer. Clin Cancer Res 12:5104–5111

    Article  CAS  PubMed  Google Scholar 

  • Zhang MS, Xu CM, Yan HY, Zhao N, Von Wettstein D, Liu B (2009) Limited tissue culture-induced mutations and linked epigenetic modifications in F1 hybrids of sorghum pure lines are accompanied by increased transcription of DNA methyltransferases and 5-methylcytosine glycosylases. Plant J 57:666–679

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This study was supported by the National Natural Science Foundation of China (30870178, 30870198), and the Program for Introducing Talents to University (111 project #B07017). We are grateful to Professor Diter von Wettstein of the Washington State University for his interest in this study and constructive suggestions to improve the manuscript.

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Correspondence to Bao Liu.

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Communicated by P. Kumar.

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Zhang, M., Wang, H., Dong, Z. et al. Tissue culture-induced variation at simple sequence repeats in sorghum (Sorghum bicolor L.) is genotype-dependent and associated with down-regulated expression of a mismatch repair gene, MLH3. Plant Cell Rep 29, 51–59 (2010). https://doi.org/10.1007/s00299-009-0797-9

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