Abstract
In order to better understand the molecular basis of heterosis in maize, the methylation-sensitive amplification polymorphism method was used to estimate patterns of cytosine methylation in seedling roots and leaves and 15-d postfertilization embryo and endosperm tissues of hybrids and their parental lines Zheng58 and Chang7-2. In all tissues, total relative methylation levels in the hybrids were lower than corresponding mid-parent values, with a higher number of demethylation events inferred for the hybrids. The trend of reduced methylation and increased demethylation in the hybrids relative to their parents may allow de-repression and possibly the expression of various genes associated with a hybrid phenotypic variation. To further investigate observed methylation pattern changes, we sequenced 50 differentially displayed DNA fragments. The BLAST analysis revealed that 13 fragments shared similarity with known functional proteins in maize or other plant species including proteins related to metabolism, transposons/retrotransposons, development, stress response, and signal transduction. The genes associated with these proteins may thus contribute significantly to maize hybrid vigour.
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Abbreviations
- C:
-
Chang7-2
- MSAP:
-
methylation sensitive amplification polymorphism
- Z:
-
Zheng58
References
Birchler, J.A., Yao, H., Chudalayandi, S., Vaiman, D., Veitia, R.A.: Heterosis. — Plant Cell 22: 2105–2112, 2010.
Bruce, A.B.: The Mendelian theory of heredity and the augmentation of vigor. — Science 32: 627–628, 1910.
Candaele, J., Demuynck, K., Mosoti, D., Beemster, G.T.S., Inzé, D., Nelissen, H.: Differential methylation during maize leaf growth targets developmentally regulated genes. —Plant Physiol. 164: 1350–1364, 2014.
Chen, Z.J.: Molecular mechanisms of polyploidy and hybrid vigor. — Trends Plant Sci. 15: 57–71, 2010.
Dyachenko, O.V., Tarlachkov, S.V., Marinitch, D.V., Shevchuk, T.V., Buryanov, Y.I.: Expression of exogenous DNA methyltransferases: application in molecular and cell biology. — Biochemistry 79: 77–87, 2014.
Fang, J.G., Chao, C.T.: Methylation-sensitive amplification polymorphism in date palms (Phoenix dactylifera L.) and their off-shoots. — Plant Biol. 9: 526–533, 2007.
Frascaroli, E., Cane, M.A., Landi, P., Pea, G., Gianfranceschi, L., Villa, M., Morgante, M., Pè, M.E.: Classical genetic and quantitative trait loci analyses of heterosis in a maize hybrid between two elite inbred lines. — Genet. J. 176: 625–644, 2007.
Greaves, I.K., Groszmann, M., Ying, H., Taylor, J.M., Peacock, W.J., Dennis, E.S.: Trans-chromosomal methylation in Arabidopsis hybrids. — Proc. nat. Acad. Sci. USA 109: 3570–3575, 2012.
Groszmann, M., Greaves, I.K., Albertyn, Z.I., Scofield, G.N., Peacock, W.J., Dennis, E.S.: Changes in 24-nt siRNA levels in Arabidopsis hybrids suggest an epigenetic contribution to hybrid vigor. — Proc. nat. Acad. Sci. USA 108: 2617–2622, 2010.
Guo, W.L., Wu, R., Zhang, Y.F., Liu, X.M., Wang, H.Y., Gong, L., Zhang, Z.H., Liu, B.: Tissue culture-induced locusspecific alteration in DNA methylation and its correlation with genetic variation in Codonopsis lanceolata Benth. et Hook. f. — Plant Cell Rep. 26: 1297–1307, 2007.
He, G., Elling, A.A., Deng, X.W.: The epigenome and plant development. — Annu. Rev. Plant Biol. 62: 411–435, 2011.
He, G.M., Zhu, X.P., Elling, A.A., Chen, L.B., Wang, X.F., Guo, L., Liang, M.Z., He, H., Zhang, H.Y., Chen, F.F., Qi, Y.J., Chen, R.S., Deng, X.W.: Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. — Plant Cell 22: 17–33, 2010.
Hochholdinger, F., Hoecker, N.: Towards the molecular basis of heterosis. — Trends Plant Sci. 12: 427–432, 2007.
Hsieh, T.F., Ibarra, C.A., Silva, P., Zemach, A., Eshed-Williams, L., Fischer, R.L., Zilberman, D.: Genome-wide demethylation of Arabidopsis endosperm. — Sci. J. 324: 1451–1454, 2009.
Joel, A.J., Zhang, Q.: Differential cytosine methylation in rice. — In: Book of Abstracts of 8th National Rice Biotechnology Network Meeting. Pp. 226–230. Aurangabad 2001.
Karan, R., DeLeon, T., Biradar, H., Subudhi, P.K.: Salt stress induced variation in DNA methylation pattern and its influence on gene expression in contrasting rice genotypes. — PLoS ONE 7(6): e40203. 2012.
Kidwell, K.K., Osborn, T.C.: Simple plant DNA isolation procedures. — In: Beckman, J.S., Osborn, T.C. (ed.): Plant Genomes. Methods for Genetic and Physical Mapping. Pp. 1–13. Kluwer Academic Publishers, Dordrecht 1992.
Kumari, R., Yadav, G., Sharma, V., Sharma, V., Kumar, S.: Cytosine hypomethylation at CHG and CHH sites in the pleiotropic mutants of Mendelian inheritance in Catharanthus roseus. — J. Genet. 92: 499–511, 2013.
Li, A., Song, W.Q., Chen, C.B., Zhou, Y.N., Qi, L.W., Wang, C.G.: DNA methylation status is associated with the formation of heterosis in Larix kaempferi intraspecific hybrids. — Mol. Breed. 31: 463–475, 2013.
Li, A., Hu, B.Q., Xue, Z.Y., Chen, L., Wang, W.X., Song, W.Q., Chen, C.B., Wang, C.G.: DNA methylation in genomes of several annual herbaceous and woody perennial plants of varying ploidy as detected by MSAP. — Plant mol. Biol. Rep. 29: 784–793, 2011.
Li, Y., Shan, X., Liu, X., Hu, L., Guo, W., Liu, B.: Utility of the methylation-sensitive amplified polymorphism (MSAP) marker for detection of DNA methylation polymorphism and epigenetic population structure in a wild barley species (Hordeum brevisubulatum). — Ecol. Res. 23: 927–930, 2008.
Lister, R., O'Malley, R.C., Tonti-Filippini, J., Gregory, B.D., Berry, C.C., Millar, A.H., Ecker, J.R.: Highly integrated single base resolution maps of the epigenome in Arabidopsis. — Cell 133: 523–536, 2008.
Lu, Y., Rong, T., Cao, M.: Analysis of DNA methylation in different maize tissues. — J. Genet. Genomics 35: 41–48, 2008.
Lu, G., Wu, X., Chen, B., Gao, G., Xu, K., Li, X.: Detection of DNA methylation changes during seed germination in rapeseed (Brassica napus). — Chin. sci. Bull. 51: 182–190, 2006.
Meng, F.R., Li, Y.C., Yin, J., Liu, H., Chen, X.J., Ni, Z.F., Sun, Q.X.: Analysis of DNA methylation during the germination of wheat seeds. — Biol. Plant. 56: 269–275, 2012.
Nakamura, S., Hosaka, K.: DNA methylation in diploid inbred lines of potatoes and its possible role in the regulation of heterosis. — Theor. appl. Genet. 120: 205–214, 2010.
Osabe, K., Clement, J.D., Bedon, F., Pettolino, F. A., Ziolkowski, L., Llewellyn, D.J., Finnegan, E. J., Wilson I.W.: Genetic and DNA methylation changes in cotton (Gossypium) genotypes and tissues. — PLOS one 9(1): e86049, 2014.
Radoev, M., Becker, H.C., Ecke, W.: Genetic analysis of heterosis for yield and yield components in rapeseed (Brassica napus L.) by quantitative trait locus mapping. — Genetics 179: 1547–1558, 2008.
Rapp, R.A., Wendel, J.F.: Epigenetics and plant evolution. — New Phytol. 168: 81–91, 2005.
Riddle, N.C., Richards, E.J.: Genetic variation in epigenetic inheritance of ribosomal RNA gene methylation in Arabidopsis. — Plant J. 41: 524–532, 2005.
Rodriguez, M.P., Cervigni, G.D.L., Quarin, C.L., Ortiz, J.P.A.: Frequencies and variation in cytosine methylation patterns in diploid and tetraploid cytotypes of Paspalum notatum. — Biol. Plant. 56: 276–282, 2012.
Ronemus, M.J., Galbiati, M., Ticknor, C., Chen, J., Dellaporta, S.L.: Demethylation-induced developmental pleiotropy in Arabidopsis. — Science 273: 654–657, 1996.
Salmon, A., Ainouche, M.L., Wendel, J.F.: Genetic and epigenetic consequences of recent hybridization and polyploidy in Spartina (Poaceae). — Mol. Ecol. 14: 1163–1175, 2005.
Sambrook, J., Fritsch, E.F., Maniatis, T.: Commonly Used Techniques in Molecular Cloning. Molecular Cloning: a Laboratory Manual. — Cold Spring Harbor Laboratory Press, New York 1989.
Sanetomo, R., Hosaka, K.: Reciprocal differences in DNA sequence and methylation status of the pollen DNA between F1 hybrids of Solanum tuberosum × S. demissum. — Euphytica 182: 219–229, 2011.
Shan, X.H., Wang, X.Y., Yang, G., Wu, Y., Su, S.Z., Li, S.P., Liu, H.K., Yuan, Y.P.: Analysis of the DNA methylation of maize (Zea mays L.) in response to cold stress based on methylation-sensitive amplified polymorphisms. — J. Plant Biol. 56: 32–38, 2013.
Shen, H., He, H., Li, J., Chen, W., Wang, X., Guo, L., Peng, Z., He, G., Zhong, S., Qi, Y., Terzaghi, W., Deng, X.W.: Genome-wide analysis of DNA methylation and gene expression changes in two Arabidopsis ecotypes and their reciprocal hybrids. — Plant Cell 24: 875–892, 2012.
Shull, G.H.: The composition of a field of maize. — Amer. Breeders Assoc. Rep. 4: 296–301, 1908.
Shull, G.H.: Beginnings of the heterosis concept. — In: Gowen, J.W. (ed.): Heterosis. A Record of Researches Directed Toward Explaining and Utilizing the Vigor of Hybrids. Pp. 14–48. Iowa State College Press, Ames 1952.
Wang, H., Feng Q.Z., Zhang M.S., Yang C.W., Sha W., Liu B.: Alteration of DNA methylation level and pattern in sorghum (Sorghum bicolor L.) pure-lines and inter-line F1 hybrids following low-dose laser irradiation. — J. Photochem. Photobiol. B Biol. 99: 150–153, 2010.
Wang, W.S., Zhao, X.Q., Pan, Y.J., Zhu, L.H., Fu, B.Y., Li, Z.K.: DNA methylation changes detected by methylationsensitive amplified polymorphism in two contrasting rice genotypes under salt stress. — J. Genet. Genome 38: 419–424, 2011.
Wang, X.R., Wu, R., Lin, X.Y., Bai, Y., Song, C.D., Yu, X.M., Xu, C.M., Zhao, N., Dong, Y.Z., Liu, B.: Tissue cultureinduced genetic and epigenetic alterations in rice pure-lines, F1 hybrids and polyploids. — BMC Plant Biol. 13: 1–12, 2013.
Xu, M.L., Li, X.Q., Korban, S.S.: AFLP-based detection of DNA methylation. — Plant mol. Biol. Rep. 18: 361–368, 2000.
Yang, W., Jiang, D., Jiang, J., He, Y.H.: A plant-specific histone H3 lysine 4 demethylase represses the floral transition in Arabidopsis. — Plant J. 62: 663–673, 2010.
You, W.H., Tyczewska, A., Spencer, M., Daxinger, L., Schmid, M.W., Grossniklaus, U., Simon, S.A., Meyers, B.C., Matzke, A., Matzke, M.: Atypical DNA methylation of genes encoding cysteine-rich peptides in Arabidopsis thaliana. — BMC Plant Biol. 12: 1–15, 2012.
Zhang, M., Xu, C., Von Wettstein, D., Liu, B.: Tissue-specific differences in cytosine methylation and their association with differential gene expression in Sorghum bicolar. — Plant Physiol. 156: 1955–1966, 2011.
Zhang, Y., Liu, Z.H., Liu, C., Yang, Z.J., Deng, K.J., Peng, J.H., Zhou, J.P., Li, G.R., Tang, Z.X., Ren, Z.L.: Analysis of DNA methylation variation in wheat genetic background after alien chromatin introduction based on methylationsensitive amplification polymorphism. — Chin. sci. Bull. 53: 58–69, 2008.
Zhao, X.X., Chai, Y., Liu, B.: Epigenetic inheritance and variation of DNA methylation level and pattern in maize intra-specific hybrids. — Plant Sci. 172: 930–938, 2007.
Zhao, Y., Yu, S., Xing, C., Fan, S., Song, M.: Analysis of DNA methylation in cotton hybrids and their parents. — Mol. Biol. 42: 169–178, 2008.
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Acknowledgments: This research was supported by the National High Technology Reasearch and Development Program of China (863 Program, No. 2011AA10A103), the Science Development Planning of Jilin Province (No. 20126030), and the Science and Technology Backbone Research Startup Projects in Crop Science at the Heilongjiang Bayi Agricultural University (No. ZWXQDJ-6). We thank the reviewers for their constructive suggestions for improving this manuscript.
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Sun, L.F., Liu, T.J., Shan, X.H. et al. Analysis of DNA cytosine methylation patterns in maize hybrids and their parents. Biol Plant 59, 266–272 (2015). https://doi.org/10.1007/s10535-015-0490-5
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DOI: https://doi.org/10.1007/s10535-015-0490-5