Activation of plant LTR-retrotransposons under in vitro culture stress

  • I. I. Konvalyuk Institute of Molecular Biology and Genetics of NAS of Ukraine, Ukraine, 03143, Kyiv, Akademika Zabolotnogo str., 150
  • O. M. Bublyk Institute of Molecular Biology and Genetics of NAS of Ukraine, Ukraine, 03143, Kyiv, Akademika Zabolotnogo str., 150
  • I. O. Andreev Institute of Molecular Biology and Genetics of NAS of Ukraine, Ukraine, 03143, Kyiv, Akademika Zabolotnogo str., 150

Abstract

Retrotransposons make up a significant part of plant genome and are probably the most dynamic part of it, so they play a significant role in the generation of genetic variation. In particular, their activation can lead to structural reorganization of genome and changes in genome size, the emergence of novel genetic and phenotypic variants, as well as changes in gene expression, thus providing the raw material for adaptation and evolution. This review summarizes literature data on the activation of LTR-retrotransposons of the superfamilies Ty1/Copia and Ty3/Gypsy during in vitro culture and under various abiotic and biotic stress conditions. Their structure, classification, and significance for the organization and functioning of plant genome are reviewed. The main mechanisms of activation of LTR-retrotransposons under stress conditions are explored, including changes in DNA methylation and interaction of stress-induced transcription factors with retrotransposon promoters due to the presence of specific binding sites and other regulatory elements. The review also discusses consequences of activation of retrotransposons and control of their activity by self-inactivation mechanisms and the epigenetic regulation of genome.
Keywords: retrotransposons, Ty1/Copia, Ty3/Gypsy, in vitro culture, abiotic and biotic stress.

References

Alzohairy A. M., Sabir J. S. M., Gyulai G., Younis R. A. A., Jansen R. K., Bahieldin A. Environmental stress activation of plant long-terminal repeat retrotransposons. Funct. Plant. Biol. 2014. Vol. 41. P. 557-567. doi: 10.1071/FP13339.

Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature. 2000. Vol. 408. P. 796-815. doi: 10.1038/35048692.

Bayram E., Yilmaz S., Hamat-Mecbur H., Kartal-Alacam G., Gozukirmizi N. Nikita retrotransposon movements in callus cultures of barley (Hordeum vulgare L.). Plant Omics J. 2012. Vol. 5. P. 211-215.

Bednarek P. T., Oriowska R. Plant tissue culture environment as a switch-key of (epi)genetic changes. Plant Cell Tiss. Organ Cult. 2020. Vol. 140. P. 245257. doi: 10.1007/s11240-019-01724-1.

Bennetzen J. L. Transposable element contributions to plant gene and genome evolution. Plant Mol. Biol. 2000. Vol. 42. P. 251-269. doi: 10.1023/A:1006344508454

Bennetzen J. L., Ma J., Devos K.M. Mechanisms of recent genome size variation in flowering plants. Ann. Bot. 2005. Vol. 95. P. 127-132. doi: 10.1093/aob/mci008.

Capy P., Gaspery G., Biemont C., Bazin C. Stress and transposable elements: co-evolution or useful parasites? Heredity. 2000. Vol. 85. P. 101-106. doi: 10.1046/j.1365-2540.2000.00751.x.

Carrier G., Le Cunff L., Dereeper A. et al. Transposable elements are a major cause of somatic polymorphism in Vitis vinifera L. PLoS ONE. 2012. Vol. 7(3). P. e32973. doi: 10.1371/journal.pone.0032973.

Casacuberta J. M., Santiago N. Plant LTR-retrotransposons and MITEs: control of transposition and impact on the evolution of plant genes and genomes. Mol. Ecol. 2013. Vol. 22. P. 1503-1517. doi: 10.1111/mec.12170.

Cheng C., Daigen M., Hirochika H. Epigenetic regulation of the rice retrotransposon Tos17. Mol. Genet. Genomics. 2006. Vol. 276. P. 378-90. doi: 10.1007/s00438-006-0141-9

Esposito S., Barteri F., Casacuberta J. et al. LTR-TEs abundance, timing and mobility in Solanum commersonii and S. tuberosum genomes following cold-stress conditions. Planta. 2019. Vol. 250. P. 1781-1787. doi: 10.1007/s00425-019-03283-3.

Evrensel C., Yilmaz S., Temel A. et al. Variations in BARE-1 insertion patterns in barley callus cultures. Genet. Mol. Res. 2011. Vol. 10(2). P. 980-987. doi: 10.4238/vol10-2gmr965.

Flavell A. J., Dunbar E., Anderson R., Pearce S. R., Hartley R., Kumar A. Ty1-copia group retrotransposons are ubiquitous and heterogeneous in higher plants. Nucl. Acids. Res. 1992. Vol. 20. P. 3639-3644. doi: 10.1093/nar/20.14.3639.

Fras A., Juchimiuk J., Siwinska D., Maluszynska J. Cytological events in explants of Arabidopsis thaliana during early callogenesis. Plant Cell. Rep. 2007. Vol. 26. P. 1933-1939. doi: 10.1007/s00299-007-0415-7.

Giordani T., Cossu R. M., Mascagni F. et al. Genome-wide analysis of LTR-retrotransposon expression in leaves of populus X Canadensis water-deprived plants. Tree Genet. Genomes. 2016. Vol. 12. P. 75. doi: 10.1007/s11295-016-1036-5.

Gozukirmizi N. Transposons continue the amaze. Int. J. Sci. Lett. 2019. Vol. 1(1). P. 1-13. doi: 10.38058/ijsl.585052.

Grandbastien M. A. Activation of plant retrotransposons under stress conditions. Trends Plant Sci. 1998. Vol. 3. P. 181-187. doi: 10.1016/S1360-1385(98)01232-1.

Grandbastien M. A., Spielmann A., Caboche M. Tnt1, a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics. Nature. 1989. Vol. 337. P. 376-380. doi: 10.1038/337376a0.

Han M., Sun Q., Zhou J. et al. Insertion of a solo LTR retrotransposon associates with spur mutations in ‘Red Delicious’ apple (Malus x domestica). Plant Cell Rep. 2017. Vol. 36. P. 1375-1385. doi: 10.1007/s00299-017-2160-x.

Hirochika H., Sugimoto K., Otsuki Y. et al. Retrotransposons of rice involved in mutations induced by tissue culture. Proc. Nat. Acad. Sci. USA. 1996. Vol. 93. P. 7783-7788. doi: 10.1073/pnas.93.15.7783.

Horvath V., Merenciano M., Gonzalez J. Revisiting the relationship between transposable elements and the eukaryotic stress response. Trends Genet. 2017. Vol. 33(11). P. 832-841. doi: 10.1016/j.tig.2017.08.007.

Hou J., Lu D., Mason A.S. et al. Non-coding RNAs and transposable elements in plant genomes: emergence, regulatory mechanisms and roles in plant development and stress responses. Planta. 2018. Vol. 250. P. 23-40. doi: 10.1007/s00425-019-03166-7

Kalendar R, Muterko A., Boronnikova S. Retrotransposable elements: DNA fingerprinting and the assessment of genetic diversity. In: Besse P. (ed.) Molecular plant taxonomy. Methods in molecular biology, vol. 2222. New York, NY: Humana, 2021. P. 263-286. doi: 10.1007/978-1-0716-0997-2_15.

Kalendar R., Tanskanen J., Immonen S. et al. Genome evolution of wild barley (Hordeum spontaneum) by BARE-1 retrotransposon dynamics in response to sharp microclimatic divergence. Proc. Natl. Acad. Sci. USA. 2000. Vol. 97. P. 6603-6607. doi: 10.1073/pnas.110587497.

Kalendar R.N., Aizharkyn K.S., Khapilina O.N., Amenov A.A., Tagimanova D.S. Plant diversity and transcriptional variability assessed by retrotransposon-based molecular markers. Vavilov J. Genet. Breed. 2017. Vol. 21(1). P. 128-134. doi: 10.18699/VJ17.231.

Kartal-Alacam G., Yilmaz S., Marakli S. et al. Sukkula retrotransposon insertion polymorphisms in barley. Russ. J. Plant Physiol. 2014. Vol. 61:828. doi: 10.1134/S1021443714060107

Kimura Y., Tosa Y., Shimada S. et al. OARE-1, a Ty1-copia retrotransposon in oat activated by abiotic and biotic stresses. Plant Cell Physiol. 2001. Vol. 42. P. 1345-1354. doi: 10.1093/pcp/pce171.

Kunakh V. A. Biotechnology of medicinal plants. Genetic, physiological and biochemical basis. Kyiv: Logos, 2005. 730 p. [in Ukrainian].

Kunakh V. A. Mobile genetic elements and plant genome plasticity. Kyiv: Logos, 2013. 288 p. [in Ukrainian].

Lanciano S., Mirouze M. Transposable elements: all mobile, all different, some stress responsive, some adaptive? Curr. Opin. Genet. Dev. 2018. Vol. 49. P. 106-114. doi: 10.1016/j.gde.2018.04.002.

Lerat E., Casacuberta J., Chaparro C., Vieira C. On the importance to acknowledge transposable elements in epigenomic analyses. Genes. 2019. Vol. 10:258. doi: 10.3390/genes10040258

Li Z. Y., Chen S. Y., Zheng X. W., Zhu L H. Identification and chromosomal localization of a transcriptionally active retrotransposon of Ty3-gypsy type in rice. Genome. 2000. Vol. 43. P. 404-408. doi:.10.1139/g99-137.

Liang Zh., Anderson S. N., Noshay J. M. et al. Genetic and epigenetic contributions to variation in transposable element expression responses to abiotic stress in maize. BioRxiv. 2020. 2020.08.26.268102. doi: 10.1101/2020.08.26.268102.

Lorens C., Futami R., Covelli L. et al. The Gypsy database (GyDB) of mobile genetic elements: release 2.0. Nucl. Acids. Res. (NARESE). 2011. Vol. 39. P. 70-74. doi: 10.1093/nar/gkq1061.

Luo Y., Tian D., Teo J. Ch., Ong K. H., Yin Z. Inactivation of retrotransposon Tos17Chr.7 in rice cultivar Nipponbare through CRISPR/Cas9-mediated gene editing. Plant Biotechnol. - NAR. 2018. Vol. 37. P. 69-75. doi: 10.5511/plantbiotechnology.20.0123a

Manninen O., Schulman A. H. BARE-1, a Copia-like retroelement in barley (Hordeum vulgare L). Plant Mol. Biol. 1993. Vol. 22. P. 829-846. doi: 10.1007/BF00027369.

Matsuoka Y., Tsunewaki K. Evolutionary dynamics of Ty1-copia group retrotransposons in grass shown by reverse transcriptase domain analysis. Mol. Biol. Evol. 1999. Vol. 16. P. 208-217. doi: 10.1093/oxfordjournals.molbev.a026103.

McClintock B. Controlling elements and the gene. Cold Spring Harb. Symp. Quant. Biol. 1956. Vol. 21. P. 197-216. doi: 10.1101/sqb.1956.021.01.017.

McClintock B. The significance of responses of the genome to challenge. Science. 1984. Vol. 226. P. 792-801. doi: 10.1126/science.15739260.

Mozgova I., Mikulski P., Pecinka A., Farrona S. Epigenetic mechanisms of abiotic stress response and memory in plants. In: Alvarez-Venegas R., De-la-Pena C., Casas-Mollano J. (eds.) Epigenetics in plants of agronomic importance: fundamentals and applications. Cham: Springer, 2019. P. 1-64. doi: 10.1007/978-3-030-14760-0_1.

Nie Q., Qiao G., Peng L., Wen X. Transcriptional activation of long terminal repeat retrotransposon sequences in the genome of pitaya under abiotic stress. Plant Physiol. Biochem. 2019. Vol. 135. P. 460-468. doi: 10.1016/j.plaphy.2018.11.014.

Oliver K. R., McComb J. A., Greene W. K. Transposable elements: powerful contributors to angiosperm evolution and diversity. Genome Biol. Evol. 2013. Vol. 5(10). P. 1886-1901. doi: 10.1093/gbe/evt141.

Orlowska R., Machczynska J., Oleszczuk S. et al. DNA methylation changes and TE activity induced in tissue cultures of barley (Hordeum vulgare L.). J. Biol. Res. (Thessalon). 2016. Vol. 23(19). doi: 10.1186/s40709-016-0056-5.

Orozco-Arias S., Isaza G., Guyot R. Retrotransposons in plant genomes: structure, identification, and classification through bioinformatics and machine learning. Int. J. Mol. Sci. 2019. Vol. 20. P. 3837. doi:10.3390/ijms20153837.

Picault N., Chaparro C., Piegu B. et al. Identification of an active LTR retrotransposon in rice. Plant J. 2009. Vol. 58. P. 754-765. doi: 10.1111/j.1365-313X.2009.03813.x.

Pykalo S.V., Dubrovna O.V. Variability of the triticale genome in culture in vitro. Cytol. Genet. 2018. Vol. 52. P. 385-393. doi: 10.3103/S0095452718050092.

Sabot F. Tos17 rice element: incomplete but effective. Mobile DNA. 2014. Vol. 5(1). P. 10. doi: 10.1186/1759-8753-5-10.

SanMiguel P., Tikhonov A., Jin Y.K. et al. Nested retrotransposons in the intergenic regions of the maize genome. Science. 1996. Vol. 274. P. 765768. doi: 10.1126/science.274.5288.765.

Skaptsov M. V., Kutsev M. G., Krasnoborod kina M. A. et al. Variability of methylation of satellite DNA and mobile genetic elements of the Rumex acetosa in culture in vitro. Problemy botaniki Yuzhnoy Sibiri i Mongolii. 2017. Vol. 16. P. 264-267. [in Russian].

Songstad D. D., Petolino J. F., Voytas D. F., Reichert N. A. Genome editing of plants. CRC Crit. Rev. Plant Sci. 2017. Vol. 36(1). P. 1-23. doi: 10.1080/07352689.2017.1281663.

Steward N., Ito M., Yamaguchi Y., Koizumi N., Sano H. Periodic DNA methylation in maize nucleosomes and demethylation by environmental stress. J. Biol. Chem. 2002. Vol. 277(40). P. 3774137746. doi: 10.1074/jbc.M204050200.

Sugimoto K., Takeda S., Hirochika H. MYB-related transcription factor NtMYB2 induced by wounding and elicitors is a regulator of the tobacco retrotransposon Tto1 and defense-related genes. Plant Cell. 2000. Vol. 12. P. 2511-2527. doi: 10.1105/tpc.12.12.2511.

Suoniemi A., Tanskanen J., Schulman A. H. Gypsy-like retrotransposons are widespread in the plant kingdom. Plant J. 1998. Vol. 13. P. 699-705. doi: 10.1046/j.1365-313X.1998.00071.x.

Takeda S., Sugimoto K., Otsuki H., Hirochika H. A 13-bp cis-regulatory element in the LTR promoter of the tobacco retrotransposon Tto1 is involved in responsiveness to tissue culture, wounding, methyl jasmonate and fungal elicitors. Plant J. 1999. Vol. 18. P. 383-393. doi: 10.1046/j.1365-313X.1999.00460.x.

Taspinar M.S., Aydin M., Sigmaz B. et al. Aluminum-induced changes on DNA damage, DNA methylation and LTR retrotransposon polymorphism in maize. Arab. J. Sci. Eng. 2018. Vol. 43. P. 123-131. doi: 10.1007/s13369-017-2697-6.

Todorovska E. Retrotransposons and their role in plant-genome evolution. Biotechnol. Biotechnol. Equip. 2007. Vol. 21(3). P. 294-305. doi: 10.1080/13102818.2007.10817464.

Vernhettes S., Grandbastien M. A., Casacuberta J. M. The evolutionary analysis of the Tnt1 retrotransposon in Nicotiana species reveals the high variability of its regulatory sequences. Mol. Biol. Evol. 1998. Vol. 15. P. 827-836. doi: 10.1023/A:1005826605598.

Vicient C. M., Casacuberta J. M. Impact of transposable elements on polyploid plant genomes. Ann. Bot. 2017. Vol. 120. P. 195-207. doi:10.1093/aob/mcx078.

Vicient C. M., Casacuberta J. M. Additional ORFs in plant LTR-retrotransposons. Front Plant Sci. 2020. Vol. 11. P. 555. doi: 10.3389/fpls.2020.00555.

Vicient C. M., Kalendar R., Schulman A. H. Variability, recombination, and mosaic evolution of the barley BARE-1 retrotransposon. J. Mol. Evol. 2005. Vol. 61. P. 275-291. doi: 10.1007/s00239-004-0168-7.

Voronova A. Retrotransposon expression in response to in vitro inoculation with two fungal pathogens of Scots pine (Pinus sylvestris L.). BMC Res. Notes. 2019. Vol. 12. P. 243. doi: 10.1186/s13104-019-4275-3

Wessler S. R. Turned on by stress. Plant retrotransposons. Curr. Biol. 1996. Vol. 6(8). P. 959-961. doi: 10.1016/S0960-9822(02)00638-3.

Wicker T., Sabot F., Hua-Van A. et al. A unified classification system for eukaryotic transposable elements. Nat. Rev. Genet. 2007. Vol. 8. P. 973982. doi: 10.1038/nrg2165.

Yigider E., Taspinar M.S., Aydin M. et al. Cobalt-induced retrotransposon polymorphism and humic acid protection on maize genome. Biol. Futura. 2019. Vol. 71. P. 123-130. doi: 10.1007/s42977-020-00001-z

Yilmaz S., Gozukirmizi N. Variation of retrotransposon movement in callus culture and regenerated shoots of barley. Biotechnol. Biotechnol. Equip. 2013. Vol. 27(6). P. 4227-4230. doi: 10.5504/BBEQ.2013.0076.

Zhou M., Liang L., Hänninen H. A transposition-active Phyllostachys edulis long terminal repeat (LTR) retrotransposon. J. Plant Res. 2018. Vol. 131. P. 203-210. doi: 10.1007/s10265-017-0983-8.