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Endosperm-specific hypomethylation, and meiotic inheritance and variation of DNA methylation level and pattern in sorghum (Sorghum bicolor L.) inter-strain hybrids

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Abstract

Understanding dynamics and inheritance of DNA methylation represents important facets for elucidating epigenetic paradigms in plant development and evolution. Using four sets of sorghum (Sorghum bicolor L.) inter-strain hybrids and their inbred parents, the developmental stability and inheritance of cytosine methylation in two tissues, leaf and endosperm, by MSAP analysis were investigated. It was found that in all lines (inbred and hybrid) studied, endosperm exhibited a markedly reduced level of full methylation of the external cytosine or both cytosines at the CCGG sites relative to leaf, which caused a variable reduction in the estimated total methylation level in endosperm by 6.89–19.69% (11.47% on average). For both tissues, a great majority of cytosine methylation profiles transmitted to F1 hybrids, however, from 1.69 to 3.22% of the profiles showed altered patterns in hybrids. Both inherited and altered methylation profiles can be divided into distinct groups, and their frequencies are variable among the cross-combinations, and between the two tissues. The variations in methylation level and pattern detected in the hybrids were not caused by parental heterozygosity, and they could be either non-random or stochastic among hybrid individuals. Homology analysis of isolated bands that showed endosperm-specific hypomethylation or variation in hybrids indicated that diverse sequences were involved, including known-function cellular genes and mobile elements. RT-PCR analysis of six genes representing endosperm-specific hypomethylation in MSAP profiles indicated that all showed higher expression in endosperm than in leaf, suggesting involvement of methylation state in regulating tissue-specific or tissue-biased expression in sorghum. Analysis on leaf-RNA from 5-azacytidine-treated plants further corroborated this possibility.

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Acknowledgments

This study was supported by the Program for Changjiang Scholars and Innovative Research Team (PCSIRT) in University (#IRT0519), the National Natural Science Foundation of China (30225003, 30430060), and the State Key Basic Research and Development Plan of China (2001CB1088). We are particularly grateful to an anonymous reviewer for critical reading of an earlier version of the manuscript and constructive suggestions to improve it.

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Authors and Affiliations

  1. Laboratory of Plant Molecular Epigenetics, Institute of Genetics and Cytology, Northeast Normal University, Changchun, 130024, China

    M. S. Zhang, N. Zhao, X. Y. Lin, J. S. Pang & B. Liu

  2. Department of Agronomy, Jilin Agricultural University, Changchun, 130118, China

    M. S. Zhang & K. Z. Xu

  3. Institute of Crop Science, Jilin Academy of Agricultural Sciences, Gongzhuling, 136100, China

    H. Y. Yan

  4. Key Laboratory of Vegetation Ecology of MOE, Northeast Normal University, Changchun, 130024, China

    L. X. Liu

  5. Key Laboratory of Applied Statistics of MOE, Northeast Normal University, Changchun, 130024, China

    B. Liu

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Correspondence to B. Liu.

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Communicated by A. Schulman.

Electronic supplementary material

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122_2007_555_MOESM1_ESM.doc

Supplementary Table 1 Sequence of adaptors, pre-amplification primers and selective amplification primer combinations in MSAP analysis (Doc 42 kb)

Supplementary Table 2 Selected MSAP bands for transcriptional analysis by RT-PCR (Doc 43 kb)

122_2007_555_MOESM3_ESM.doc

Supplementary Table 3 Inheritance and variation of cytosine methylation patterns at the CCGG sites in sorghum inter-strain hybrids (Doc 87 kb)

122_2007_555_MOESM4_ESM.doc

Supplementary Table 4 Putative function, identity and restriction map of the sequenced MSAP profiles showing variation in sorghum inter-strain hybrids relative to their inbred parents (Doc 220 kb)

122_2007_555_MOESM5_ESM.doc

Supplementary Table 5 Putative function, identity and restriction map of the sequenced MSAP profiles showing difference in methylation pattern between leaf and endosperm (Doc 127 kb)

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Zhang, M.S., Yan, H.Y., Zhao, N. et al. 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 (2007). https://doi.org/10.1007/s00122-007-0555-8

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