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PLOS ONE  2013 

DNA Methylation Alterations at 5′-CCGG Sites in the Interspecific and Intraspecific Hybridizations Derived from Brassica rapa and B. napus

DOI: 10.1371/journal.pone.0065946

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Abstract:

DNA methylation is an important regulatory mechanism for gene expression that involved in the biological processes of development and differentiation in plants. To investigate the association of DNA methylation with heterosis in Brassica, a set of intraspecific hybrids in Brassica rapa and B. napus and interspecific hybrids between B. rapa and B. napus, together with parental lines, were used to monitor alterations in cytosine methylation at 5′-CCGG sites in seedlings and buds by methylation-sensitive amplification polymorphism analysis. The methylation status of approximately a quarter of the methylation sites changed between seedlings and buds. These alterations were related closely to the genomic structure and heterozygous status among accessions. The methylation status in the majority of DNA methylation sites detected in hybrids was the same as that in at least one of the parental lines in both seedlings and buds. However, the association between patterns of cytosine methylation and heterosis varied among different traits and between tissues in hybrids of Brassica, although a few methylation loci were associated with heterosis. Our data suggest that changes in DNA methylation at 5′-CCGG sites are not associated simply with heterosis in the interspecific and intraspecific hybridizations derived from B. rapa and B. napus.

References

[1]  Melchinger AE (1999) Genetic diversity and heterosis. In: Coors CG, Pandey S (eds) Genetic and exploitation of heterosis in crops. American Society of Agronomy:Madison 99–118.
[2]  Hua J, Xing Y, Wu W, Xu C, Sun X, et al. (2003) Single-locus heterotic effects and dominance by dominance interactions can adequately explain the genetic basis of heterosis in an elite rice hybrid. Proc Natl Acad Sci U S A 100: 2574–2579.
[3]  Stuber CW, Lincoln SE, Wolff DW, Helentjaris T, Lander ES (1992) Identification of genetic factors contributing to heterosis in a hybrid from two elite maize inbred lines using molecular markers. Genetics 132: 823–839.
[4]  Xiao J, Li J, Yuan L, Tanksley SD (1995) Dominance is the major genetic basis of heterosis in rice as revealed by QTL analysis using molecular markers. Genetics 140: 745–754.
[5]  Yu SB, Li JX, Xu CG, Tan YF, Gao YJ, et al. (1997) Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. Proc Natl Acad Sci U S A 94: 9226–9231.
[6]  Auger DL, Gray AD, Ream TS, Kato A, Coe EH, et al. (2005) Nonadditive gene expression in diploid and triploid hybrids of maize. Genetics 169: 389–397.
[7]  Guo M, Rupe MA, Zinselmeier C, Habben J, Bowen BA, et al. (2004) Allelic variation of gene expression in maize hybrids. Plant Cell 16: 1707–1716.
[8]  Song RT, Messing J (2003) Gene expression of a gene family in maize based on noncollinear haplotypes. Proc Natl Acad Sci U S A 100: 9055–9060.
[9]  Stupar RM, Springer NM (2006) Cis-transcriptional variation in maize inbred lines B73 and Mo17 leads to additive expression patterns in the F-1 hybrid. Genetics 173: 2199–2210.
[10]  Guo M, Rupe MA, Yang XF, Crasta O, et al. (2006) Genome-wide transcript analysis of maize hybrids: allelic additive gene expression and yield heterosis. Theor Appl Genet 113: 831–845.
[11]  Swanson-Wagner RA, Jia Y, DeCook R, Borsuk LA, Nettleton D, et al. (2006) All possible modes of gene action are observed in a global comparison of gene expression in a maize F-1 hybrid and its inbred parents. Proc Natl Acad Sci U S A 103: 6805–6810.
[12]  Birchler JA, Auger DL, Riddle NC (2003) In search of the molecular basis of heterosis. Plant Cell 15: 2236–9.
[13]  Siegfried Z, Simon I (2010) DNA methylation and gene expression. Wiley Interdiscip Rev Syst Biol Med 2: 362–371.
[14]  Adams S, Vinkenoog R, Spielman M, Dickinson HG, Scott RJ (2000) Parent-of-origin effects on seed development in Arabidopsis thaliana require DNA methylation. Development 127: 2493–2502.
[15]  Jacobsen SE, Sakai H, Finnegan EJ, Cao X, Meyerowitz EM (2000) Ectopic hypermethylation of flower-specific genes in Arabidopsis. Curr Biol 10: 179–186.
[16]  Xiao WY, Custard KD, Brown RC, Lemmon BE, Harada JJ, et al. (2006) DNA methylation is critical for Arabidopsis embryogenesis and seed viability. Plant Cell 18: 805–814.
[17]  Chinnusamy V, Zhu JK (2009) Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol 12: 133–139.
[18]  Shen H, He H, Li J, Chen W, Wang X, et al. (2012) Genome-wide analysis of DNA methylation and gene expression changes in two Arabidopsis ecotypes and their reciprocal hybrids. Plant Cell 24: 3875–3892.
[19]  Chodavarapu RK, Feng S, Ding B, Simon SA, Lopez D, et al. (2012) Transcriptome and methylome interactions in rice hybrids. PNAS 109: 12040–12045.
[20]  Gaeta RT, Pires JC, Iniguez-Luy F, Leon E, Osborn TC (2007) Genomic changes in resynthesized Brassica napus and their effect on gene expression and phenotype. Plant Cell 19: 3403–3417.
[21]  Jin HJ, Hu W, Wei Z, Wan LL, Li G, et al. (2008) Alterations in cytosine methylation and species-specific transcription induced by interspecific hybridization between Oryza sativa and O-officinalis. Theor Appl Genet 117: 1271–1279.
[22]  Madlung A, Masuelli RW, Watson B, Reynolds SH, Davison J, et al. (2002) Remodeling of DNA methylation and phenotypic and transcriptional changes in synthetic Arabidopsis allotetraploids. Plant Physiology 129: 733–746.
[23]  Salmon A, Ainouche ML, Wendel JF (2005) Genetic and epigenetic consequences of recent hybridization and polyploidy in Spartina (Poaceae). Molecular Ecology 14: 1163–1175.
[24]  Xu YH, Zhong L, Wu XM, Fang XP, Wang JB (2009) Rapid alterations of gene expression and cytosine methylation in newly synthesized Brassica napus allopolyploids. Planta 229: 471–483.
[25]  Banaei Moghaddam AM, Fuchs J, Czauderna T, Houben A, Mette MF (2010) Intraspecific hybrids of Arabidopsis thaliana revealed no gross alterations in endopolyploidy, DNA methylation, histone modifications and transcript levels. Theor Appl Genet 120: 215–226.
[26]  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.
[27]  Dahal D, Mooney BP, Newton KJ (2012) Specific changes in total and mitochondrial proteomes are associated with higher levels of heterosis in maize hybrids. Plant J. 2012 72: 70–83.
[28]  Qian W, Liu R, Meng J (2003) Genetic effects on biomass yield in interspecific hybrids between Brassica napus and B. rapa. Euphytica 134: 9–15.
[29]  Li MT, Chen X, Meng JL (2006) Potential of intersubgenomic heterosis in rapeseed production with a partial new-typed Brassica napus containing subgenome Ar from B. rapa and Cc from B. carinata. Crop Science 46: 234–242.
[30]  Qian W, Chen X, Fu D, Zou J, Meng J (2005) Intersubgenomic heterosis in seed yield potential observed in a new type of Brassica napus introgressed with partial Brassica rapa genome. Theor Appl Genet 110: 1187–1194.
[31]  Poethig RS (2003) Phase change and the regulation of developmental timing in plants. Science 301: 334–336.
[32]  Rohlf FJ (1997) NTSYSpc: numerical taxonomy and multivariate analysis system, version 2.02.
[33]  Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci U S A 76: 5269–5273.
[34]  Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evol Bioinform Online 1: 47–50.
[35]  Institute S. SAS Users Guide: Statistic. SAS Institute, Cary, NC 1996.
[36]  Finnegan EJ, Genger RK, Peacock WJ, Dennis ES (1998) DNA Methylation in Plants. Annu Rev Plant Physiol Plant Mol Biol 49: 223–247.
[37]  Xiong LZ, Yang GP, Xu CG (1998) Relationships of differential gene expression in leaves with heterosis and heterozygosity in a rice diallel cross. Molecular Breeding 4: 129–136.
[38]  Ruiz-Garcia L, Cervera MT, Martinez-Zapater JM (2005) DNA methylation increases throughout Arabidopsis development. Planta 222: 301–306.
[39]  Zhang MS, Yan HY, Zhao N, Lin XY, Pang JS, et al. (2007) Endosperm-specific hypomethylation, and meiotic inheritance and variation of DNA methylation level and pattern in sorghum (Sorghum bicolor L.) inter-strain hybrids. Theor Appl Genet 115: 195–207.
[40]  Bjornsson HT, Sigurdsson MI, Fallin MD, Irizarry RA, Aspelund T, et al. (2008) Intra-individual change over time in DNA methylation with familial clustering. Jama 299: 2877–2883.
[41]  Lukens LN, Pires JC, Leon E, Vogelzang R, Oslach L, et al. (2006) Patterns of sequence loss and cytosine methylation within a population of newly resynthesized Brassica napus allopolyploids. Plant Physiology 140: 336–348.
[42]  Udall JA, Quijada PA, Osborn TC (2005) Detection of chromosomal rearrangements derived from homologous recombination in four mapping populations of Brassica napus L. Genetics. 169: 967–979.
[43]  Szadkowski E, Eber F, Huteau V, Lode M, Huneau C, et al. (2010) The first meiosis of resynthesized Brassica napus, a genome blender. New Phytol 186: 102–112.
[44]  Henikoff S, Matzke MA (1997) Exploring and explaining epigenetic effects. Trends Genet 13: 293–295.
[45]  Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11: 204–220.

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