Abstract
Plant genomes contain a sizeable fraction, ranging from 14 to 75% of retrotransposons (class I elements), predominantly comprising LTR (Long Terminal Repeat) elements. Movement of these elements is mediated via an RNA intermediate by copy-and-paste mechanism. The transposition of the elements is tightly regulated, however, under certain conditions such as stress; they are transcriptionally and possibly transpositionally activated. The 5’-LTRs of retrotransposons contain regulatory sequences required for their transcriptional activation. Each element is usually present in multiple copies and not all copies of an element may be functional possibly due to alterations in its internal sequence domains, without affecting the functionality of their 5’-LTRs. We analyzed the transcriptional activation of six Ty1-copia family of retrotransposons selected from six different plants (two monocots and four dicots) by monitoring pattern of GUS expression directed by 5’-LTRs in transgenic tobacco plants in response to a variety of stress factors (cold, UV, H2O2, HgCl2, CdCl2, CuCl2, 2,4-D, SA, ABA) and tissue-specific (callus, root, leaf, stem and flower) cues. We show that different 5’-LTRs show differential activation under various conditions. Two retroelements which were considered non-functional apparently have functional 5’-LTRs. No apparent correlation between the presence of sequence elements in the 5-LTRs and transcriptional activation of the retroelements in response to stress and tissue-specific signals could be established. The results suggest that the transcriptional activation and possibly silencing of different retrotransposons is a complex process and may be mediated by multiple interconnected pathways.
Similar content being viewed by others
Abbreviations
- LTR:
-
Long Terminal Repeat
- LINE:
-
Long Interspersed Nuclear Element
- SINE:
-
Short Interspersed Nuclear Element
- ABA:
-
Absissic acid
- SA:
-
Salicylic acid
References
Aprile A, Mastrangelo AM, De Leonardis AM, Galiba G, Roncaglia E, Ferrari F (2009) Transcriptional profiling in response to terminal drought stress reveals differential responses along the wheat genome. BMC Genom 10:279
Baker SS, Wilhelm KS, Thomashow MF (1994) The 5′-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold, drought and ABA-regulated gene expression. Plant Mol Biol 24:701–713
Bate N, Twell D (1998) Functional architecture of a late pollen promoter: pollen-specific transcription is developmentally regulated by multiple stage-specific and co-dependent activator elements. Plant Mol Biol 37:859–869
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182
Cordaux R, Batzer MA (2009) The impact of retrotransposons on human genome evolution. Nat Rev Genet 10:691–703
El Baidouri M, Panaud O (2013) Comparative genomic paleontology across plant kingdom reveals the dynamics of TE-driven genome evolution. Genome Biol Evol 5:954–965
Elmayan T, Tepfer M (1995) Evaluation in tobacco of the organ specificity and strength of the rolD promoter, domain A of the 35S promoter and the 35S2 promoter. Transgenic Res 4:388–396
Garber K, Bilic I, Pusch O, Tohme J, Bachmair A, Schweizer D, Jantsch V (1999) The Tpv2 family of retrotransposons of Phaseolus vulgaris: structure, integration characteristics, and use for genotype classification. Plant Mol Biol 39:797–807
Grandbastien MA (2015) LTR retrotransposons, handy hitchhikers of plant regulation and stress response. Biochim Biophys Acta 1849:403–416
Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11
Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300
Hirochika H, Sugimoto K, Otsuki Y, Tsugawa H, Kanda M (1996) Retrotransposons of rice involved in mutations induced by tissue culture. Proc Natl Acad Sci USA 93:7783–7788
Horsch RB, Klee HJ (1986) Rapid assay of foreign gene expression in leaf discs transformed by Agrobacterium tumefaciens: Role of T-DNA borders in the transfer process. Proc Natl Acad Sci USA 83:4428–4432
Jaaskelainen M, Chang W, Moisy C, Schulman AH (2013) Retrotransposon BARE displays strong tissue-specific differences in expression. New Phytol 200:1000–1008
Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907
Jiang C, Iu B, Singh J (1996) Requirement of a CCGAC cis-acting element for cold induction of the BN115 gene from winter Brassica napus. Plant Mol Biol 30:679–684
Kalendar R, Tanskanen J, Immonen S, Nevo E, Schulman AH (2000) Genome evolution of wild barley (Hordeum spontaneum) by BARE-1 retrotransposon dynamics in response to sharp microclimatic divergence. Proc Natl Acad Sci USA 97:6603–6607
Kimura Y, Tosa Y, Shimada S, Sogo R, Kusaba M, Sunaga T, Betsuyaku S, Eto Y, Nakayashiki H, Mayama S (2001) OARE-1, a Ty1-copia retrotransposon in oat activated by abiotic and biotic stresses. Plant Cell Physiol 42:1345–1354
Koukalova B, Fojtova M, Lim KY, Fulnecek J, Leitch AR, Kovarik A (2005) Dedifferentiation of tobacco cells is associated with ribosomal RNA gene hypomethylation, increased transcription, and chromatin alterations. Plant Physiol 139:275–286
Kumar A, Bennetzen JL (1999) Plant retrotransposons. Annu Rev Genet 33:479–532
Lall IP, Maneesha, Upadhyaya KC (2002) Panzee, a copia-like retrotransposon from the grain legume, pigeonpea (Cajanus cajan L.). Mol Genet Genom 267:271–280
Lisch D (2009) Epigenetic regulation of transposable elements in plants. Annu Rev Plant Biol 60:43–66
Liu ZL, Han FP, Tan M, Shan XH, Dong YZ, Wang XZ, Fedak G, Hao S, Liu B (2004) Activation of a rice endogenous retrotransposon Tos17 in tissue culture is accompanied by cytosine demethylation and causes heritable alteration in methylation pattern of flanking genomic regions. Theor Appl Genet 109:200–209
Madsen LH, Fukai E, Radutoiu S, Yost CK, Sandal N, Schauser L, Stougaard J (2005) LORE1, an active low-copy-number Ty3-Gypsy retrotransposon family in the model legume Lotus japonicus. Plant J 44:372–381
Marillonnet S, Wessler SR (1998) Extreme structural heterogeneity among the members of a maize retrotransposon family. Genetics 150:1245–1256
McClintock B (1984) The significance of response of the genome to challenge. Science 226:792–801
Mhiri C, Morel JB, Vernhettes S, Casacuberta JM, Lucas H, Grandbastien MA (1997) The promoter of the tobacco Tnt1 retrotransposon is induced by wounding and by abiotic stress. Plant Mol Biol 33:257–266
Miguel C, Marum L (2011) An epigenetic view of plant cells cultured in vitro: somaclonal variation and beyond. J Exp Bot 62:3713–3725
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucl Acids Res 8:4321–4326
Neumann P, Pozárková D, Macas J (2003) Highly abundant pea LTR retrotransposon Ogre is constitutively transcribed and partially spliced. J Plant Mol Biol 53:399–410
Neumann P, Novák P, Hoštáková N (2019) Macas (2019) Systematic survey of plant LTR retrotransposons elucidates phylogenetic relationships of their polyprotein domains and provides a reference for element classification. Mob DNA 10:1. https://doi.org/10.1186/s13100-018-0144-1
Quinn JM, Barraco P, Eriksson M, Merchant S (2000) Coordinate copper- and oxygen-responsive Cyc6 and Cpx1 expression in Chlamydomonas is mediated by the same element. J Biol Chem 275:6080–6089
Rieping M, Schöffl F (1992) Synergistic effect of upstream sequences, CCAAT box elements, and HSE sequences for enhanced expression of chimeric heat-shock genes in transgenic tobacco. Mol Gen Genet 231:226–232
Salazar M, González E, Casaretto JA, Casacuberta JM, Ruiz-Lara S (2007) The promoter of the TLC1.1 retrotransposon from Solanum chilense is activated by multiple stress-related signaling molecules. Plant Cell Rep 26:1861–1868
Schnable PS, Ware D, Fulton RS, Stein JC et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115
Slotkin RK, Vaughn M, Borges F, Tanurdzic M, Becker JD, Feijo JA, Martienssen RA (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136:461–472
Svensson JT, Crosatti C, Campoli C, Bassi R, Stanca AM, Close TJ, Cattivelli L (2006) Transcriptome analysis of cold acclimation in barley albina and xantha mutants. Plant Physiol 141:257–270
Tahara M, Aoki T, Suzuka S, Yamashita H, Tanaka M, Matsunaga S, Kokumai S (2004) Isolation of an active element from a high-copy-number family of retrotransposons in the sweetpotato genome. Mol Gen Genomics 272:116–127
Vicient CM (2010) Transcriptional activity of transposable elements in maize. BMC Genom 11:601
Voytas DF, Konieczny A, Cummings MP, Ausubel FM (1990) The structure, distribution and evolution of the Ta1 retrotransposable element family. Genetics 126:713–721
Wicker T, Keller B (2007) Genome-wide comparative analysis of copia retrotransposons in Triticeae, rice, and Arabidopsis reveals conserved ancient evolutionary lineages and distinct dynamics of individual copia families. Genome Res 17:1072–1081
Xiao W, Su Y, Sakamot W (2007) Isolation and characterization of Ty1/copia-like retrotransposons in mung bean (Vigna radiata). J Plant Res 120:323–328
Xue GP (2002) Characterization of the DNA-binding profile of barley HvCBF1 using an enzymatic method for rapid quantitative and high-throughput analysis of the DNA-binding activity. Nucleic Acids Res 30:e77
Yamamoto S, Nakano T, Suzuki K, Shinshi H (2004) Elicitor-induced activation of transcription via W box-related cis-acting elements from a basic chitinase gene by WRKY transcription factors in tobacco. Biochim Biophys Acta 1679:279–287
Zeller G, Henz SR, Widmer CK, Sachsenberg T, Rätsch G, Weigel D, Laubinger S (2009) Stress-induced changes in the Arabidopsis thaliana transcriptome analyzed using whole-genome tiling arrays. Plant J 58:1068–1082
Acknowledgements
Financial assistance of University Grants Commission (UGC) is gratefully acknowledged. SM acknowledges the CSIR for fellowship.
Author information
Authors and Affiliations
Contributions
SM designed and performed the experiments. KCU conceptualized the study and designed the experiments. DS contributed the lab support and some of the supplies. KCU and SM wrote the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
Authors report no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Mukherjee, S., Sharma, D. & Upadhyaya, K.C. Differential transcriptional activation of copia family of different plant retrotransposons. J. Plant Biochem. Biotechnol. 31, 915–924 (2022). https://doi.org/10.1007/s13562-022-00771-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13562-022-00771-8