Цитологія і генетика 2020, том 54, № 5, 117-119
Cytology and Genetics 2020, том 54, № 5, 493–504, doi: https://www.doi.org/10.3103/S0095452720050151

Differential transgeneration methylation of exogenous promoters in T1 transgenic wheat (Triticum aestivum)

Mona Mohamed Elseehy

  • Department of Genetics, Faculty of Agriculture, University of Alexandria, Elshatby, Alexandria, Egypt

РЕЗЮМЕ. Метилювання ДНК стало важливою молекулярною технологією для регуляції експресії генів шляхом регулювання додавання/видалення метильної групи до позиції 5 цитозину. Покоління T1 рослин T0 трансгенної пшениці використовували для вивчення трансгенераційного метилювання проксимальних регіонів двох екзогенних промотерів за допомогою бісульфітного секвенування. Було використано покоління T0 з низьким і високим рівнем експресії ізофлавон-синтази (IFS), що мають високий і низький рівні метилювання відповідно. Результати цього дослідження продемонстрували, що рослини T1, які мають промотер 35S для IFS, успадкували статус метилювання промотера 35S та експресії IFS, особливо метилювання на участках -56 і -88 CpG. З іншого боку, рослини T0 з високим рівнем експресії IFS і промотером OL для експресії IFS проходили таку ж схему експресії IFS і метилювання їхнього покоління T1, тоді як рослини Т0 з низьким рівнем експресії IFS змінили схему експресії і метилювання на високий рівень експресії T0 у своєму поколінні T1. Це вказує на те, що рослини T1 пшениці були здатні деметилювати ДНК проксимальних регіонів промотера OL, особливо в –106 і -151, та переводити експресію IFS з низького рівня на високий через одне покоління. Це також може вказувати на те, що рослинні промотери більш придатні для керування трансгеном у біотехнології рослин. Результати поглиблять наше розуміння регуляції експресії генів за допомогою метилювання ДНК і їх застосування у біотехнології рослин.

Ключові слова: трансгенний, пшениця, метилювання, трансгенераційний, епігенетичний, метилтрансферази ДНК

Цитологія і генетика
2020, том 54, № 5, 117-119

Current Issue
Cytology and Genetics
2020, том 54, № 5, 493–504,
doi: 10.3103/S0095452720050151

Повний текст та додаткові матеріали

Цитована література

1. Lopez, C.M.R. and Wilkinson, M.J., Epi-fingerprinting and epi-interventions for improved crop production and food quality, Front. Plant Sci., 2015, vol. 6, p. 397. https://doi.org/10.3389/fpls.2015.00397

2. Brautigam, K.,Vining, K.J., Lafon-Placette, C., Fossdal, C.G., Mirouze, M., Gutiérrez Marcos, J., Fluch, S., Fernández, M., Fraga, M., Guevara, Á., Abarca, D., Johnsen, Ø., Maury, S., Strauss, S.H., Campbell, M.M., Rohde, A., Díaz-Sala, C., and Cervera, M.-T., Epigenetic regulation of adaptive responses of forest tree species to the environment, Ecol. Evol., 2013, vol. 3, no. 2, pp. 399–415. https://doi.org/10.1002/ece3.461

3. Akimoto, K., Katakami, H., Kim, H., Ogawa, E., Sano, C.M., Wada, Y., and Sano, H., Epigenetic inheritance in rice plants, Ann. bot., 2007, vol. 100, pp. 205–217.

4. Law, J.A. and Jacobsen, S.E., Establishing, maintaining and modifying DNA methylation patterns in plants and animals, Nat. Rev. Genet., 2010, vol. 11, pp. 204–220.

5. Zilberman, D., An evolutionary case for functional gene body methylation in plants and animals, Genome Biol., 2017, vol. 18, p. 87.

6. Han, S. and Wagner, D., Role of chromatin in water stress responses in plants, J. Exp. Bot., 2014, vol. 65, no. 10, pp. 2785–2799.

7. Jones, L., Ratcliff, F., and Baulcombe, D.C., RNA-directed transcriptional gene silencing in plants can be inherited independently of the RNA trigger and requires Met1 for maintenance, Curr. Biol., 2001, vol. 11, pp. 747–757.

8. Chan, S.W., Henderson, I.R., and Jacobsen, S.E., Gardening the genome: DNA methylation in Arabidopsis thaliana,Nat. Rev. Genet., 2005, vol. 6, pp. 351–360.

9. Yong-Villalobos, L., González-Morales, S.I., Wrobel, K., Gutiérrez-Alanis, D., Cervantes-Peréz, S.A., Hayano-Kanashiro, C., Oropeza-Aburto, A., Cruz-Ramírez, A., Martínez, O., and Herrera-Estrella, L., Methylome analysis reveals an important role for epigenetic changes in the regulation of the Arabidopsis response to phosphate starvation, Proc. Natl. Acad. Sci. U. S.A., 2015, vol. 112, no. 52, pp. 7293–7302.

10. Ikeuchi, M., Iwase, A., and Sugimoto, K., Control of plant cell differentiation by histone modification and DNA methylation, Curr. Opin. Plant Biol., 2015, vol. 28, pp. 60–67.

11. Demeulemeester, M., Van Stallen, N., and De Proft, M., Degree of DNA methylation in chicory (Cichorium intybus L.): influence of plant age and vernalization, Plant Sci., 1999, vol. 142, no. 1, pp. 101–108.

12. Yaish, M.W., Epigenetic modifications associated with abiotic and biotic stresses in plants: an implication for understanding plant evolution, Front. Plant Sci., 2017, vol. 8, p. 1983.

13. Yaish, M.W., Al-Lawati, A., Al-Harrasi, I., and Patankar, H.V., Genome-wide DNA Methylation analysis in response to salinity in the model plant caliph medic (Medicago truncatula), BMC Genomics, 2018, vol. 19, no. 1, p. 78.

14. Fedoroff, N.V., Transposable elements, epigenetics, and genome evolution. Sci., 2012, vol. 338, no. 6108, pp. 758–767.

15. Takatsuka, H. and Umeda, M., Epigenetic control of cell division and cell differentiation in the root apex, Front. Plant Sci., 2015, vol. 6, p. 1178.

16. Suzuki, M.M. and Bird, A., DNA methylation and scapes: provocative insights from epigenomics, Nat. Rev. Genet., 2008, vol. 9, pp. 465–476.

17. Takuno, S. and Gaut, B.S., Body-methylated genes in Arabidopsis thaliana are functionally important and evolve slowly, Mol. Biol. Evol., 2012, vol. 29, pp. 219–227.

18. Bird, A., DNA methylation patterns and epigenetic memory, Gen. Dev., 2002, vol. 16, pp. 6–21.

19. Saze, H., Tsugane, K., Kanno, T., and Nishimura, T., DNA methylation in plants: relationship to small RNAs and histone modifications, and functions in transposon inactivation, Plant Cell Physiol., 2012, vol. 53, pp. 766–784.

20. Zilberman, D., Gehring, M., Tran, R.K., Ballinger, T., and Henikoff, S., Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription, Nat. Genet., 2007, vol. 39, pp. 61–69.

21. Zhang, X., Yazaki, J., Sundaresan, A., Cokus, S., Chan, S.W., Chen, H., Henderson, I.R., Shinn, P., Ellegrini, M., Jacobsen, S.E., and Ecker, J.R., Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis,Cell, 2006, vol. 126, pp. 1189–1201.

22. Hauser, M., Aufsatz, W., Jonak, C., and Luschnig, C., Transgenerational epigenetic inheritance in plants, Biochim. Biophys. Acta, 2011, vol. 1809, no. 8, pp. 459–468.

23. Berdasco, M., Alca’zar, R., Garcı’a-Ortiz, M.V., Ballestar, E., Ferna’ndez, A.F., et al., Promoter DNA hypermethylation and gene repression in undifferentiated Arabidopsis cells, PLoS One, 2008, vol. 3, no. 10. e3306.

24. Matzke, M.A., Primig, M., Trnovsky, J., and Matzke, M.A., Reversible methylation and inactivation of marker genes in sequentially transformed tobacco plants, EMBO J., 1989, vol. 8, no. 3, pp. 643–649.

25. Deng, S., Dai, H., Arenas, C., Wang, H., Niu, Q., and Chua, N., Transcriptional silencing of Arabidopsis endogenes by single-stranded RNAs targeting the promoter region plant, Cell Physiol., 2014, vol. 55, no. 4, pp. 823–833.

26. Heilersig, B.H.J.B., Loonen, A.E.H.M., Janssen, E.M., Wolters, A.A., and Visser, R.G.F., Efficiency of transcriptional gene silencing of GBSSI in potato depends on the promoter region that is used in an inverted repeat, Mol. Gen. Genom., 2006, vol. 275, pp. 437–449.

27. El-Shehawi, A.M., Fahmi, A.I., Elseehy, M.M., and Nagaty, H.H., Enhancement of nutritional quality of wheat (Triticum aestivum) by metabolic engineering of isoflavone pathway, Am. J. Biochem. Biotechnol., 2013, vol. 9, no. 4, pp. 407–417.

28. Elseehy, M.M. and El-Shehawi, A.M., Methylation of exogenous promoters regulates soybean isoflavone synthase (GmIFS) transgene in T0 transgenic wheat (Triticum aestivum), Cytol. Genet., 2020, vol. 54, no. 3, p. 271.

29. Kim, J.H., Park, F.J., Lee, T.K., and Lee, W.S., Genomic sequences of the soybean 24 kDa oleosin genes and initial analysis of their promoter sequences, Mol. Cell., 1996, vol. 6, no. 4, pp. 393–399.

30. Dai, Y., Ni1, Z., Dai, J., Zhao, T., and Sun, Q., Isolation and expression analysis of genes encoding DNA methyltransferase in wheat (Triticum aestivum L.), Biochim. Biophys. Acta, 2005, vol. 1729, pp. 118–125.

31. Saghai-Maroof, M.A., Soliman, K.M., Jorgensen, R.A., and Allard, R.W., Ribosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics, Proc. Natl. Acad. Sci. U. S. A., 1984, vol. 81, no. 24, pp. 8014–8018.

32. Ahmed, M.M., El-Shazly, A.S., El-Shehawi, A.M., and Alkafafy, M.E., Antiobesity effects of Taif and Egyptian pomegranates: molecular study, Biosci. Biotechnol. Biochem., 2015, vol. 79, no. 4, pp. 598–609.

33. Li, Y. and Tollefsbol, T.O., DNA methylation detection: bisulfite genomic sequencing analysis, Method. Mol. Biol., 2011, vol. 791, pp. 11–21.

34. Carr, I.M., Valleley, E.M.A., Cordery, S.F., Markham, A.F., and Bonthron, D.T., Sequence analysis and editing for bisulphite genomic sequencing projects, Nucleic Acids Res., 2007, vol. 35, p. 79.

35. Goll M.G., Kirpekar F., Maggert K.A., Yoder J.A., Hsieh C.L., Zhang X., Golic K.G., Jacobsen S.E., and Bestor T.H. Methylation of tRNAAsp by the DNA methyltransferase homolog Dnmt2. Sci., 2006, vol. 311, pp. 395–8.

36. Jeltscha, A., Ehrenhofer-Murray, A., Jurkowski, T.P., Lykoc, F., Reuterd, G., Ankri, S., Nellenf, W., Schaeferg, M., and Helmh, M., Mechanism and biological role of Dnmt2 in nucleic acid methylation, RNA Biol., 2017, vol. 14, no. 9, pp. 1108–1123.

37. Jorgensen, K., Rasmussen, A.V., Morant, M., Nielsen, A.H., Bjarnholt, N. Zagrobelny, M., Birger, S.B., and Møller, L., Metabolon formation and metabolic channeling in the biosynthesis of plant natural products, Curr. Opin. Plant Biol., 2005, vol. 8, pp. 280–291.

38. Liu, R., Hu, Y., Li, J., and Lin, Z., Production of soybean isoflavone genistein in non-legume plants via genetically modified secondary metabolism pathway, Metabolic. Eng., 2007, vol. 9, pp. 1–7.

39. Bucherna, N., Szabo, E., Heszky, L.S., and Nagy, I., DNA methylation and gene expression differences during alternative in vitro morphogenic processes in eggplant (Solanum melongena L.),In Vitro Cell. Dev. Biol.—Plant, 2001, vol. 37, pp. 672–677.

40. Tolley, B.J., Woodfield, H., Wanchana, S., Bruskiewich, R., and Hibberd, J.M., Light-regulated and cell-specific methylation of the maize PEPC promoter, J. Exp. Bot., 2012, vol. 63, no. 3, pp. 1381–1390.

41. Colaneri, A.C. and Jones, A.M., Genome-wide quantitative identification of DNA differentially methylated sites in Arabidopsis seedlings growing at different water potential, PLoS One, 2013, vol. 8, p. 59878.

42. Lira-Medeiros, C.F., Parisod, C., Fernandes, R.A., Mata, C.S., Cardoso, M.A., and Ferreira, P.C., Epigenetic variation in mangrove plants occurring in contrasting natural environment, PLoS One, 2010, vol. 5, p. 10326.

43. Wang, W.S., Pan, Y.J., Zhao, X.Q., Dwivedi, D., Zhu, L.H., Ali, J., Fu, B.Y., and Li, Z.K., Drought-induced site-specific DNA methylation and its association with drought tolerance in rice (Oryza sativa L.), J. Exp. Bot., 2011, vol. 62, pp. 1951–1960.

44. Moritoh, S., Eun, C., Ono, E., Asao, H., Okano, Y., Yamaguchi, K., Shimatani, Z., Koizumi, A., and Terada, R., Targeted disruption of an orthologue of DOMAINS REARRANGED METHYLASE 2, OsDRM2, impairs the growth of rice plants by abnormal DNA methylation, Plant J., 2012, vol. 71, pp. 85–98.

45. Cao, X. and Jacobsen, S.E., Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyltransferase genes, Proc. Natl. Acad. Sci. U. S. A., 2002, vol. 99, pp. 16491–16498.

46. Kurihara, Y., Matsui, A., Kawashima, M. Kaminuma, E., Ishida, J., Morosawa, T., Mochizuki, Y., Kobayashi, N., Toyoda, T., Shinozaki, K., and Seki, M., Identification of the candidate genes regulated by RNA-directed DNA methylation, Biochem. Biophys. Res. Commun., 2008, vol. 376, no. 3, pp. 553–557. https://doi.org/10.1016/j.bbrc.2008.09.046

47. Song, Q., Zhang, T., Stelly, D.M., and Chen, Z.J., Epigenomic and functional analyses reveal roles of epialleles in the loss of photoperiod sensitivity during domestication of allotetraploid cottons, Genome Biol., 2017, vol. 18, no. 1, p. 99.

48. Wei, X., Song, X., Wei, L., Tang, S., Sun, J., Hu, P., and Cao, X., An epiallele of rice AK1 affects photosynthetic capacity, J. Integr. Plant Biol., 2017, vol. 59, no. 3, pp. 158–163.

49. Conrath, U., Molecular aspects of defence priming, Trends Plant Sci., 2011, vol. 16, pp. 524–531.

50. Kathiria, P., Sidler, C., Golubov, A., Kalischuk, M., Kawchuk, L.M., and Kovalchuk, I., Tobacco mosaic virus infection results in an increase in recombination frequency and resistance to viral, bacterial, and fungal pathogens in the progeny of infected tobacco plants, Plant Physiol., 2010, vol. 153, pp. 1859–1870. https://doi.org/10.1104/pp.110.157263

51. Hauben, M., Haesendonckx, B., Standaert, E., Van DerKelen, K., Azmi, A., Akpo, H., Van Breusegem, F., Guisez, Y., Bots, M., Lambert, B., Laga, B., and De Block, M., Energy use efficiency is characterized by an epigenetic component that can be directed through artificial selection to increase yield, Proc. Natl. Acad. Sci. U. S. A., 2009, vol. 106, no. 47, pp. 20109–20114. https://doi.org/10.1073/pnas.0908755106

52. Tricker, P.J., Lopez, C.M., Gibbings, G., Hadley, P., and Wilkinson, M.J., Transgenerational, dynamic methylation of stomata genes in response to low relative humidity, Int. J. Mol. Sci., 2013, vol. 14, pp. 6674–6689.

53. Miura, K., Agetsuma, M., Kitano, H., Yoshimura, A., Matsuoka, M., Jacobsen, S.E., and Ashikari, M., A metastable DWARF1 epigenetic mutant affecting plant stature in rice, Proc. Natl. Acad. Sci. U. S. A., 2009, vol. 106, pp. 11218–11223. https://doi.org/10.1073/pnas.0901942106

54. Becker, C. and Weigel, D., Epigenetic variation: origin and transgenerational inheritance, Curr. Opin. Plant Biol., 2012, vol. 15, pp. 562–567.