International Journal of Innovative Approaches in Agricultural Research
Abbreviation: IJIAAR | ISSN (Online): 2602-4772 | DOI: 10.29329/ijiaar

Original article    |    Open Access
International Journal of Innovative Approaches in Agricultural Research 2022, Vol. 6(2) 112-128

Comparative Expression Profiles of SUVH7 in Sexual and Apomict Boechera spp. Display Differential Expression

Aslıhan Özbi̇len & Kemal Melih Taşkın

pp. 112 - 128   |  DOI: https://doi.org/10.29329/ijiaar.2022.451.5

Published online: June 30, 2022  |   Number of Views: 9  |  Number of Download: 55


Abstract

Genomic imprinting is parent-of-origin specific gene expression in embryo nourishing tissues endosperm and placenta in flowering plants and mammals, respectively. Seeds are formed with double fertilization in flowering plants and the endosperm has a 3n chromosome set with the contribution of 2 maternal and 1 paternal genome. Any deviation from this ratio (2m+1p) results in seed abortion in many species, however, apomict species modify their gametogenesis or fertilization to survive. Boechera divaricarpa is a diploid apomict plant species that can produce seeds with a 4m:1p parental genome ratio in endosperm and produce viable seeds. SUVH7, on the other hand, is a histone methyltransferase that has a catalytic SET domain responsible for epigenetic control of gene expression. In this study, we characterized the structures of the SUVH7 gene and compared the mRNA levels of SUVH7 in diploid apomict and sexual Boechera spp. in unopened immature buds and manually pollinated siliques representing the -pre and -post pollination stages, respectively. The expression level of SUVH7 in apomict B. divaricarpa has reached the max level 48 hours later following pollination, while in sexual B. stricta its expression level has dramatically decreased. Therefore, our study suggests the importance of epigenetic reprogramming in apomicts during seed development since chromatin marks via SUVH7 are commonly associated with the activation of transcription in plants.

Keywords: SUVH7, Boechera divaricarpa, Boechera stricta, Apomixis, Seed development, qPCR


How to Cite this Article

APA 6th edition
Ozbi̇len, A. & Taskin, K.M. (2022). Comparative Expression Profiles of SUVH7 in Sexual and Apomict Boechera spp. Display Differential Expression . International Journal of Innovative Approaches in Agricultural Research, 6(2), 112-128. doi: 10.29329/ijiaar.2022.451.5

Harvard
Ozbi̇len, A. and Taskin, K. (2022). Comparative Expression Profiles of SUVH7 in Sexual and Apomict Boechera spp. Display Differential Expression . International Journal of Innovative Approaches in Agricultural Research, 6(2), pp. 112-128.

Chicago 16th edition
Ozbi̇len, Aslihan and Kemal Melih Taskin (2022). "Comparative Expression Profiles of SUVH7 in Sexual and Apomict Boechera spp. Display Differential Expression ". International Journal of Innovative Approaches in Agricultural Research 6 (2):112-128. doi:10.29329/ijiaar.2022.451.5.

References
  1. Al-Shehbaz, I.A. Transfer of most North American species of Arabis to Boechera (Brassicaceae). Novon 2003, 13(4), 381-391. [Google Scholar]
  2. Anderson, J. T.; Perera, N.; Chowdhury, B.; Mitchell-Olds, T. Microgeographic patterns of genetic divergence and adaptation across environmental gradients in Boechera stricta (Brassicaceae). The American Naturalist 2015, 186, 60-73. [Google Scholar]
  3. Asker S.E.; Jerling L. Apomixis in Plants. 1992, CRC Press, Boca Raton. [Google Scholar]
  4. Baumbusch, L. O.; Thorstensen, T.; Krauss, V.; Fischer, A.; Naumann, K.; Assalkhou, R.; ... & Aalen, R. B. The Arabidopsis thaliana genome contains at least 29 active genes encoding SET domain proteins that can be assigned to four evolutionarily conserved classes. Nucleic Acids Res. 2001, 29(21), 4319-4333. [Google Scholar]
  5. Boisnard-Lorig, C.; Colon-Carmona, A.; Bauch, M.; Hodge, S.; Doerner, P.; Bancharel, E.; ... & Berger, F. (2001). Dynamic analyses of the expression of the HISTONE: YFP fusion protein in Arabidopsis show that syncytial endosperm is divided in mitotic domains. The Plant Cell 2001, 13(3), 495-509. [Google Scholar]
  6. Carman J. G. Asynchronous Expression of Duplicate Genes in Angiosperms May Cause Apomixis, Bispory, Tetraspory, and Polyembryony. Biol. J. Linn. Soc. 1997, 61, 51-94. [Google Scholar]
  7. Dobeš, C.; Mitchell‐Olds, T.; Koch, M. A. Intraspecific diversification in North American Boechera stricta (= Arabis drummondii), Boechera× divaricarpa, and Boechera holboellii (Brassicaceae) inferred from nuclear and chloroplast molecular markers—an integrative approach. Am. J. Bot. 2004, 91(12), 2087-2101. [Google Scholar]
  8. Edgar R.C. MUSCLE : multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32 (5), 1792–1797. [Google Scholar]
  9. Gasteiger E.; Hoogland C.; Gattiker A.; Duvaud S.; Wilkins M.R.; Appel R.D.; Bairoch A. Protein Identification and Analysis Tools on the ExPASy Server. In: The Proteomics Protocols Handbook. Humana Press, 2005, Hatfield. 571–607. [Google Scholar]
  10. Gehring M.; Huh J.H.; Hsieh T.; Penterman J.; Choi Y.; Harada J.J.; Goldberg R.B.; Fischer R.L. DEMETER DNA Glycosylase Establishes MEDEA Polycomb Gene Self-Imprinting by Allele-Specific Demethylation. Cell 2006, 124, 495-506. [Google Scholar]
  11. Gehring M.; Bubb K. L.; Henikoff S. Extensive Demethylation of Repetitive Elements During Seed Development Underlies Gene Imprinting. Science 2009, 324; 1447-1451. [Google Scholar]
  12. Gehring M.; Missirian V.; Henikoff S. Genomic Analysis of Parent-of-Origin Allelic Expression in Arabidopsis thaliana Seeds. PLoS ONE 2011, 6 (8), e23687. [Google Scholar]
  13. Goodstein, D. M.; Shu, S.; Howson, R.; Neupane, R.; Hayes, R. D.; Fazo, J.; ... Rokhsar, D. S. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 2012, 40(1), 1178-1186. [Google Scholar]
  14. Grimanelli, D.; García, M.; Kaszas, E.; Perotti, E.; Leblanc, O. Heterochronic expression of sexual reproductive programs during apomictic development in Tripsacum. Genetics 2003, 165(3), 1521-1531. [Google Scholar]
  15. Grossniklaus, U.; Spillane, C.; Page, D. R.; Köhler, C. Genomic imprinting and seed development: endosperm formation with and without sex. Curr Opin in Plant Biol. 2001, 4(1), 21-27. [Google Scholar]
  16. Haig, D.; Westoby, M. Parent-specific gene expression and the triploid endosperm. The American Naturalist 1989, 134(1), 147-155. [Google Scholar]
  17. Hanna W. W.; Bashaw E. C. Apomixis: Its Identification and Use in Plant Breeding. Crop Sci. 1987, 27(6), 1136-1139. [Google Scholar]
  18. Huh, J. H.; Rim, H. J. DNA demethylation and gene imprinting in flowering plants. In Epigenetic Memory and Control in Plants, 2013, (pp. 201-232). Springer, Berlin, Heidelberg. [Google Scholar]
  19. Hsieh, T. F.; Ibarra, C. A.; Silva, P.; Zemach, A.; Eshed-Williams, L.; Fischer, R. L.; Zilberman, D. Genome-wide demethylation of Arabidopsis endosperm. Science 2009, 324(5933), 1451-1454. [Google Scholar]
  20. Hsieh T.; Shin J.; Uzawa R.; Silva P.; Cohen S.; Bauer M.J.; Hashimoto M.; Kirkbride R.C.; Harada J.J.; Zilberman D.; Fischer R. L. Regulation of imprinted gene expression in Arabidopsis endosperm. Plant Biol. 2011, 108: 1755-1762. [Google Scholar]
  21. Ingelbrecht, I.; Van Houdt, H.; Van Montagu, M.; Depicker, A. Posttranscriptional silencing of reporter transgenes in tobacco correlates with DNA methylation. P. Natl. A. Sci. 1994, 91(22), 10502-10506. [Google Scholar]
  22. Jeong, C. W.; Park, G. T.; Yun, H.; Hsieh, T. F.; Choi, Y. D.; Choi, Y.; Lee, J. S. Control of paternally expressed imprinted UPWARD CURLY LEAF1, a gene encoding an F-box protein that regulates CURLY leaf polycomb protein, in the Arabidopsis endosperm. PloS ONE 2015, 10(2), e0117431. [Google Scholar]
  23. Johnson, L. M.; Bostick, M.; Zhang, X.; Kraft, E.; Henderson, I.; Callis, J.; Jacobsen, S. E. The SRA methyl-cytosine-binding domain links DNA and histone methylation. Curr. Biol. 2007, 17(4), 379-384. [Google Scholar]
  24. Kearse, M.; Moir, R.; Wilson, A.; Stones-Havas, S.; Cheung, M.; Sturrock, S.; ... & Drummond, A. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012, 28(12), 1647-1649. [Google Scholar]
  25. Koch, M. A.; Dobeš, C.; Mitchell-Olds, T. Multiple hybrid formation in natural populations: concerted evolution of the internal transcribed spacer of nuclear ribosomal DNA (ITS) in North American Arabis divaricarpa (Brassicaceae). Mol, Biol, Evol. 2003, 20(3), 338-350. [Google Scholar]
  26. Koltunow, A. M.; Bicknell, R. A.; Chaudhury, A. M. Apomixis: Molecular Strategies for the Generation of Genetically ldentical Seeds without Fertilization. Plant Physiol. 1995, 108: 1345-1352. [Google Scholar]
  27. Kradolfer, D.; Wolff, P.; Jiang, H.; Siretskiy, A.; Köhler, C. An imprinted gene underlies postzygotic reproductive isolation in Arabidopsis thaliana. Dev. Cell 2013, 26(5), 525-535. [Google Scholar]
  28. Lafon-Placette, C.; Hatorangan, M. R.; Steige, K. A.; Cornille, A.; Lascoux, M.; Slotte, T.; Köhler, C. Paternally expressed imprinted genes associate with hybridization barriers in Capsella. Nat. Plants 2018, 4(6), 352-357. [Google Scholar]
  29. Lee, CR.; Wang, B.; Mojica, J. et al. Young inversion with multiple linked QTLs under selection in a hybrid zone. Nat Ecol Evol 2017, 1, 0119. https://doi.org/10.1038/s41559-017-0119. [Google Scholar] [Crossref] 
  30. Lescot, M.; Dehais, P.; Thijs, G.; Marchal, K.; Moreau, Y.; Van der Peer, Y.; Rouze, P.; Rombauts, S. PlantCARE , a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 2002, 30 (1), 325–327. [Google Scholar]
  31. Li, Ming. Identification and Expression Analyses of Genes involved in Early Endosperm Development in Arabidopsis and Cereals. Doctoral thesis, School of Agriculture, Food and Wine, The University of Adelaide, 2011, 10. [Google Scholar]
  32. Luo, M.; Bilodeau, P.; Dennis, E. S.; Peacock, W. J.; Chaudhury, A. Expression and parent-of-origin effects for FIS2, MEA, and FIE in the endosperm and embryo of developing Arabidopsis seeds. PNAS 2000, 97 (19), 10637–10642. [Google Scholar]
  33. Luo, M.; Taylor, J. M.; Spriggs, A.; Zhang, H.; Wu, X.; Russell, S.; … Koltunow, A. A Genome-Wide Survey of Imprinted Genes in Rice Seeds Reveals Imprinting Primarily Occurs in the Endosperm. PLoS Genetics 2011, 7(6), e1002125. doi:10.1371/journal.pgen.1002125. [Google Scholar] [Crossref] 
  34. Matzk, F.; Meister, A.; Schubert, I. An efficient screen for reproductive pathways using mature seeds of monocots and dicots. The Plant Journal 2000, 21(1), 97-108. [Google Scholar]
  35. Matzk, F.; Meister, A.; Brutovská, R.; Schubert, I. Reconstruction of reproductive diversity in Hypericum perforatum L. opens novel strategies to manage apomixis. The Plant Journal 2001, 26(3), 275-282. [Google Scholar]
  36. Mette, M. F.; Aufsatz, W.; van der Winden, J.; Matzke, M. A.; Matzke, A. J. Transcriptional silencing and promoter methylation triggered by double-stranded RNA. EMBO J. 2000 2;19(19),5194-201. doi: 10.1093/emboj/19.19.5194. PMID: 11013221; PMCID: PMC302106. [Google Scholar] [Crossref] 
  37. Park, K.; Kim, M. Y.; Vickers, M.; Park, J. S.; Hyun, Y.; Okamoto, T.; ... & Scholten, S. DNA demethylation is initiated in the central cells of Arabidopsis and rice. P. Natl. A. Sci. 2016, 113(52), 15138-15143. [Google Scholar]
  38. Paszkowski, J.; Whitham, S. A. Gene silencing and DNA methylation processes. Curr. Opin. in Plant Biol. 2001, 4(2), 123-129. [Google Scholar]
  39. Pellino, M.; Sharbel, T.F.; Mau, M. et al. Selection of reference genes for quantitative real-time PCR expression studies of microdissected reproductive tissues in apomictic and sexual Boechera. BMC Res Notes 2011, 4, 303. https://doi.org/10.1186/1756-0500-4-303. [Google Scholar] [Crossref] 
  40. Rodríguez‐Negrete, E.; Lozano‐Durán, R.; Piedra‐Aguilera, A.; Cruzado, L.; Bejarano, E. R.; Castillo, A. G. Geminivirus Rep protein interferes with the plant DNA methylation machinery and suppresses transcriptional gene silencing. New Phytol. 2013, 199(2), 464-475. [Google Scholar]
  41. Satish, M.; Nivya, M. A.; Abhishek, S.; Nakarakanti, N. K.; Shivani, D.; Vani, M. V.; Rajakumara, E. Computational characterization of substrate and product specificities, and functionality of S‐adenosylmethionine binding pocket in histone lysine methyltransferases from Arabidopsis, rice and maize. Proteins: Structure, Function, and Bioinformatics 2018, 86(1), 21-34. [Google Scholar]
  42. Schranz M.E.; Dobes C.; Koch M.A.; Mitchell-Olds T. Sexual Reproduction, Hybridization, Apomixis, and Polyploidization in the Genus Boechera (Brassicaceae). Am, J. Bot. 2005, 92(11), 1797-1810. [Google Scholar]
  43. Scott R.J.; Spielman M.; Bailey J.; Dickinson H.G. Parent-of-origin Effects on Seed Development in Arabidopsis thaliana. Development 1998, 125, 3329-3341. [Google Scholar]
  44. Spielman M.; Vinkenoog R.; Scott R.J. Genetic Mechanisms of Apomixis. Philos. T. R. Soc. Lond. 2003. 358: 1095-1103. [Google Scholar]
  45. Spillane, C.; Steimer, A.; Grossniklaus, U. Apomixis in agriculture: the quest for clonal seeds. Sex Plant Reprod 2001, 14, 179–187. https://doi.org/10.1007/s00497-001-0117-1. [Google Scholar] [Crossref] 
  46. Taşkin, K. M.; Özbilen, A.; Sezer, F.; Hürkan, K.; Güneş, Ş. Structure and expression of dna methyltransferase genes from apomictic and sexual Boechera species. Comput. Biol. Chem. 2017, 67, 15-21. [Google Scholar]
  47. Thorstensen, T.; Grini, P. E.; Aalen, R. B. SET domain proteins in plant development. BBA-Gene Regul. Mech. 2011, 1809(8), 407-420. [Google Scholar]
  48. Tuteja, R.; McKeown, P. C.; Ryan, P.; Morgan, C. C.; Donoghue, M. T.; Downing, T., ... & Spillane, C. Paternally expressed imprinted genes under positive Darwinian selection in Arabidopsis thaliana. Mol. Biol. Evol. 2019, 36(6), 1239-1253. [Google Scholar]
  49. Vinkenoog, R.; Scott, R. J. Autonomous endosperm development in flowering plants: how to overcome the imprinting problem? Sex. Plant Reprod. 2001, 14(4), 189-194. [Google Scholar]
  50. Vinkenoog, R.; Bushell, C.; Spielman, M.; Adams, S.; Dickinson, H. G.; Scott, R. J. Genomic imprinting and endosperm development in flowering plants. Mol. Biotechnol. 2003, 25(2), 149-184. [Google Scholar]
  51. Wolff, P.; Jiang, H.; Wang, G.; Santos-Gonzalez, J.; Köhler, C. Paternally expressed imprinted genes establish postzygotic hybridization barriers in Arabidopsis thaliana. Elife 2015, 4, e10074. [Google Scholar]
  52. Wollmann, H.; Berger, F. Epigenetic reprogramming during plant reproduction and seed development. Curr Opin. Plant Biol. 2012, 15(1), 63-69. [Google Scholar]
  53. Xiao, X.; Zhang, J.; Li, T.; Fu, X.; Satheesh, V.; Niu, Q.; ... & Lei, M. A group of SUVH methyl‐DNA binding proteins regulate expression of the DNA demethylase ROS1 in Arabidopsis. J. Integr Plant Biol. 2019, 61(2), 110-119. [Google Scholar]
  54. Yu C.; Chen Y.; Lu C.; Hwang J. Prediction of Protein Subcellular Localization. PROTEINS: Structure, Function, and Bioinformatics 2006, 64, 643–651. [Google Scholar]
  55. Zhang M.; Zhao H.; Xie S.; Chen J.; Xu Y.; Wang K.; Zhao H.; Guan H.; Hu X.; Jiao Y.; Song W.; Lai J. Extensive, Clustered Parental Imprinting of Protein-Coding and Noncoding RNAs in Developing Maize Endosperm. PNAS 2011, 108(50), 20042-20047. [Google Scholar]