Abstract
Heterosis plays an important role in the breeding of commercial crops, but the molecular mechanism behind this phenomenon is still unclear. To better understand the molecular basis of heterosis in soybean, the correlation between DNA methylation status and heterosis in soybean was tested. From three soybean varieties used as parents, six hybrid combinations were generated. Twelve traits of the nine materials were investigated to study the relationship between DNA methylation level differences and heterosis. In this study, MethylRAD technique was used to evaluate the genomic methylation status among the six reciprocal soybean F1 hybrids and their parents in the immature grains. Results showed that the total site number of methylation and methylation levels of the F1 hybrids with strong heterosis were in a status between the two parents and the ones with weak heterosis were generally below that of two parents. Thus, it was beneficial to promote heterosis when the numbers of methylation sites and methylation levels were between two parents. Among three types of methylation variations, the type that parental demethylated and the progeny methylated (type A) may be relative to improve heterosis of some traits. The type A of methylation variations was significantly positively correlated with the mid-parent heterosis (MPH) of the fat content (r = 0.98**), the branch number per plant (r = 0.84), and also was significantly positively correlated with the BPH of the branch number per plant (r = 0.82*) and the stems thick (r = 0.81*). These results implied that both the methylation and demethylation in hybrids relative to their parents may control the expression of the genes that were associated with partial phenotypic variation in hybrids.
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References
Alleman M, Doctor J (2000) Genomic imprinting in plants: observations and evolutionary implications. Plant Mol Biol 43(2–3):147–161. https://doi.org/10.1023/a:1006419025155
Bruce AB (1910) The mendelian theory of heredity and the augmentation of vigor. Science 32(827):627–628. https://doi.org/10.1126/science.32.827.627-a
Dai M, Thompson RC, Maher C, Contreras-Galindo R, Kaplan MH, Markovitz DM, Omenn G, Meng F (2010) NGSQC: cross-platform quality analysis pipeline for deep sequencing data. BMC Genomics 11(Suppl 4):S7. https://doi.org/10.1186/1471-2164-11-s4-s7
Davenport CB (1908) Degeneration, albinism and inbreeding. Science 28(718):454–455. https://doi.org/10.1126/science.28.718.454-b
East EM (1908) Inbreeding in corn. Rep Conn Agric Exp Stn 1907:419–428
Fehr WR, Caviness CE (2019) Stages of soybean development. Coop Ext Serv 80:1–12
Feng S, Jacobsen SE, Reik W (2010) Epigenetic reprogramming in plant and animal development. Science 330(6004):622–627. https://doi.org/10.1126/science.1190614
Frommer M, McDonald LE, Millar DS, Collis CM, Watt F, Grigg GW, Molloy PL, Paul CL (1992) A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proc Natl Acad Sci USA 89(5):1827–1831. https://doi.org/10.1073/pnas.89.5.1827
Kawanabe T, Ishikura S, Miyaji N, Sasaki T, Wu LM, Itabashi E, Takada S, Shimizu M, Takasaki-Yasuda T, Osabe K, Peacock WJ, Dennis ES, Fujimoto R (2016) Role of DNA methylation in hybrid vigor in Arabidopsis thaliana. Proc Natl Acad Sci USA 113(43):E6704–E6711. https://doi.org/10.1073/pnas.1613372113
Kidwell KK, Osborn TC (1992) Simple plant DNA isolation procedures. In: Beckmann JS, Osborn TC (eds) Plant genomes: methods for genetic and physical mapping. Springer, Netherlands, pp 1–13. https://doi.org/10.1007/978-94-011-2442-3_1
Lauss K, Wardenaar R, Oka R, van Hulten M, Guryev V, Keurentjes J, Stam M, Johannes F (2018) Parental DNA methylation states are associated with heterosis in epigenetic hybrids. Plant Physiol 176(2):1627–1645. https://doi.org/10.1104/pp.17.01054
Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11(3):204–220. https://doi.org/10.1038/nrg2719
Li R, Li Y, Kristiansen K, Wang J (2008) SOAP: short oligonucleotide alignment program. Bioinformatics (Oxford, England) 24:713–714. https://doi.org/10.1093/bioinformatics/btn025
Li H, Yuan J, Wu M, Han Z, Li L, Jiang H, Jia Y, Han X, Liu M, Sun D, Chen C, Song W, Wang C (2018) Transcriptome and DNA methylome reveal insights into yield heterosis in the curds of broccoli (Brassica oleracea L. var.). BMC Plant Biol 18(1):168. https://doi.org/10.1186/s12870-018-1384-4
Liu TJ, Sun LF, Shan XH, Wu Y, Su SZ, Li SP, Liu HK, Han JY, Yuan YP (2014) Analysis of DNA methylation patterns and levels in maize hybrids and their parents. Genet Mol Res 13(4):8458–8468. https://doi.org/10.4238/2014.october.20.22
Meissner A, Gnirke A, Bell G, Ramsahoye B, Lander E, Jaenisch R (2005) Reduced representation bisulfite sequencing for comparative high-resolution DNA methylation analysis. Nucleic Acids Res 33:5868–5877. https://doi.org/10.1093/nar/gki901
Powers L (1944) An expansion of Jones’s theory for the explanation of heterosis. Am Nat 78(776):275–280. https://doi.org/10.1086/281199
Shu X, Shu S, Cheng H, Tang S, Yang L, Li H, Zhang M, Zhu Z, Liu D, Li K, Dong Z, Cheng L, Ding J (2018) Genome-wide DNA methylation analysis during palatal fusion reveals the potential mechanism of enhancer methylation regulating epithelial mesenchyme transformation. DNA Cell Biol 37(6):560–573. https://doi.org/10.1089/dna.2018.4141
Shull GH (1908) The composition of a field of maize. J Hered 4(1):296–301. https://doi.org/10.1093/jhered/os-4.1.296
Wang S, Lv J, Zhang L, Dou J, Sun Y, Li X, Fu X, Dou H, Mao J, Hu X, Bao Z (2015) MethylRAD: a simple and scalable method for genome-wide DNA methylation profiling using methylation-dependent restriction enzymes. Open Biol 5(11):150130. https://doi.org/10.1098/rsob.150130
Wang Y, Zhang K, Sun L, Han X, Fan S, Li X, Qu Y, Yao D, Wang P, Zhang J (2018) Study on the relationship between genetic variation of DNA methylation and heterosis in soybean leaves. Euphytica 214(5):85. https://doi.org/10.1007/s10681-018-2161-z
Williams W (1959) Heterosis and the genetics of complex characters. Nature 184:527–530. https://doi.org/10.1038/184527a0
Zhang MS, Yan HY, Zhao N, Lin XY, Pang JS, Xu KZ, Liu LX, Liu B (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(2):195–207. https://doi.org/10.1007/s00122-007-0555-8
Zhang Y, Zhaohui L, Liu C, Yang Z, Kejun D, Jinhua P, Jianping Z, Guangrong L, Tang Z, Zhenglong R (2008) Analysis of DNA methylation variation in wheat genetic background after alien chromatin introduction based on methylation-sensitive amplification polymorphism. Chin Sci Bull. https://doi.org/10.1007/s11434-008-0049-3
Zhao X, Chai Y, Liu B (2007) Epigenetic inheritance and variation of DNA methylation level and pattern in maize intra-specific hybrids. Plant Sci 172:930–938. https://doi.org/10.1016/j.plantsci.2007.01.002
Acknowledgements
This study was supported by the Jilin Scientific and Technological Development Program (CN)(Grant No. 20180101266JC) and Education Department of Jilin Province (Grant No. JJKH20180641KJ).
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Jun Zhang conceived and designed the experiment. Baixing Song, Yuanqian Wang, Xiao Han, Xueying Li and Sujie Fan performed the experiments. Jing Qu, Zhuo Zhang and Yang Song analyzed the data. Dan Yao contributed the reagents and materials. Yuanqiang Wang, Baixing Song, Songnan Yang and Abraham Lamboro wrote the paper. All authors read and approved the final version of the manuscript.
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Song, B., Wang, Y., Yang, S. et al. Evaluation of the relationship between DNA methylation status and heterosis in soybean with MethylRAD technique. Euphytica 216, 102 (2020). https://doi.org/10.1007/s10681-020-02639-1
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DOI: https://doi.org/10.1007/s10681-020-02639-1