How a Retrotransposon Exploits the Plant's Heat Stress Response for Its Activation


Retrotransposons are major components of plant and animal genomes. They amplify by reverse transcription and reintegration into the host genome but their activity is usually epigenetically silenced. In plants, genomic copies of retrotransposons are typically associated with repressive chromatin modifications installed and maintained by RNA-directed DNA methylation. To escape this tight control, retrotransposons employ various strategies to avoid epigenetic silencing. Here we describe the mechanism developed by ONSEN, an LTR-copia type retrotransposon in Arabidopsis thaliana. ONSEN has acquired a heat-responsive element recognized by plant-derived heat stress defense factors, resulting in transcription and production of full length extrachromosomal DNA under elevated temperatures. Further, the ONSEN promoter is free of CG and CHG sites, and the reduction of DNA methylation at the CHH sites is not sufficient to activate the element. Since dividing cells have a more pronounced heat response, the extrachromosomal ONSEN DNA, capable of reintegrating into the genome, accumulates preferentially in the meristematic tissue of the shoot. The recruitment of a major plant heat shock transcription factor in periods of heat stress exploits the plant's heat stress response to achieve the transposon's activation, making it impossible for the host to respond appropriately to stress without losing control over the invader.


Vyšlo v časopise: How a Retrotransposon Exploits the Plant's Heat Stress Response for Its Activation. PLoS Genet 10(1): e32767. doi:10.1371/journal.pgen.1004115
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004115

Souhrn

Retrotransposons are major components of plant and animal genomes. They amplify by reverse transcription and reintegration into the host genome but their activity is usually epigenetically silenced. In plants, genomic copies of retrotransposons are typically associated with repressive chromatin modifications installed and maintained by RNA-directed DNA methylation. To escape this tight control, retrotransposons employ various strategies to avoid epigenetic silencing. Here we describe the mechanism developed by ONSEN, an LTR-copia type retrotransposon in Arabidopsis thaliana. ONSEN has acquired a heat-responsive element recognized by plant-derived heat stress defense factors, resulting in transcription and production of full length extrachromosomal DNA under elevated temperatures. Further, the ONSEN promoter is free of CG and CHG sites, and the reduction of DNA methylation at the CHH sites is not sufficient to activate the element. Since dividing cells have a more pronounced heat response, the extrachromosomal ONSEN DNA, capable of reintegrating into the genome, accumulates preferentially in the meristematic tissue of the shoot. The recruitment of a major plant heat shock transcription factor in periods of heat stress exploits the plant's heat stress response to achieve the transposon's activation, making it impossible for the host to respond appropriately to stress without losing control over the invader.


Zdroje

1. CallinanPA, BatzerMA (2006) Retrotransposable elements and human disease. Genome Dynamics 1: 104–115.

2. HedgesDJ, DeiningerPL (2007) Inviting instability: Transposable elements, double-strand breaks, and the maintenance of genome integrity. Mutation Research 616: 46–59.

3. SinzelleL, IzsvakZ, IvicsZ (2009) Molecular domestication of transposable elements: from detrimental parasites to useful host genes. Cellular and Molecular Life Science 66: 1073–1093.

4. LischD (2012) How important are transposons for plant evolution? Nature Reviews Genetics 14: 49–61.

5. LischD (2009) Epigenetic regulation of transposable elements in plants. Annual Reviews in Plant Biology 60: 43–66.

6. SlotkinRK, MartienssenR (2007) Transposable elements and the epigenetic regulation of the genome. Nature Reviews Genetics 8: 272–285.

7. ZhangH, ZhuJ-K (2011) RNA-directed DNA methylation. Current Opinion in Plant Biology 14: 142–147.

8. MirouzeM, ReindersJ, BucherE, NishimuraT, SchneebergerK, et al. (2009) Selective epigenetic control of retrotransposition in Arabidopsis. Nature 461: 427–430.

9. MiuraA, YonebayashiS, WatanabeK, ToyamaT, ShimadaH, et al. (2001) Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature 411: 212–214.

10. TsukaharaS, KobayashiA, KawabeA, MathieuO, MiuraA, et al. (2009) Bursts of retrotransposition reproduced in Arabidopsis. Nature 461: 423–426.

11. LippmanZ, GendrelAV, BlackM, VaughnMW, DedhiaN, et al. (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature 430: 471–476.

12. McClintockB (1984) The significance of responses of the genome to challenge. Science 226: 792–801.

13. GrandbastienMA (1998) Activation of plant retrotransposons under stress conditions. Trends in Plant Science 3: 181–187.

14. GrandbastienM, AudeonC, BonnivardE, CasacubertaJM, ChalhoubB, et al. (2005) Stress activation and genomic impact of Tnt1 retrotransposons in Solanaceae. Cytogenetic and Genome Research 110: 229–241.

15. HarrisonBJ, FinchamJRS (1964) Instability at PAL locus in Antirrhinum majus. I. Effects of environment on frequencies of somatic and germinal mutation. Heredity 19: 237–258.

16. HashidaSN, UchiyamaT, MartinC, KishimaY, SanoY, et al. (2006) The temperature-dependent change in methylation of the Antirrhinum transposon Tam3 is controlled by the activity of its transposase. Plant Cell 18: 104–118.

17. StewardN, ItoM, YamaguchiY, KoizumiN, SanoH (2002) Periodic DNA methylation in maize nucleosomes and demethylation by environmental stress. Journal of Biological Chemistry 277: 37741–37746.

18. De FeliceB, WilsonRR, ArgenzianoC, KafantarisI, ConicellaC (2009) A transcriptionally active copia-like retroelement in Citrus limon. Cellular & Molecular Biology Letters 14: 289–304.

19. PecinkaA, DinhHQ, BaubecT, RosaM, LettnerN, et al. (2010) Epigenetic regulation of repetitive elements is attenuated by prolonged heat stress in Arabidopsis. Plant Cell 22: 3118–3129.

20. Tittel-ElmerM, BucherE, BrogerL, MathieuO, PaszkowskiJ, et al. (2010) Stress-induced activation of heterochromatic transcription. PLoS Genetics 6: e1001175.

21. ItoH, GaubertH, BucherE, MirouzeM, VaillantI, et al. (2011) An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 472: 115–119.

22. MatsunagaW, KobayashiA, KatoA, ItoH (2012) The effects of heat induction and the siRNA biogenesis pathway on the transgenerational transposition of ONSEN, a copia-like retrotransposon in Arabidopsis thaliana. Plant Cell Physiology 53: 824–833.

23. ItoH, YoshidaT, TsukaharaS, KawabeA (2013) Evolution of the ONSEN retrotransposon family activated upon heat stress in Brassicaceae. Gene 518: 256–261.

24. KotakS, LarkindaleJ, LeeU, von Koskull-DoringP, VierlingE, et al. (2007) Complexity of the heat stress response in plants. Current Opinions in Plant Biology 10: 310–316.

25. HaveckerER, GaoX, VoytasDF (2004) The diversity of LTR retrotransposons. Genome Biology 5: 225.

26. HirochikaH, OtsukiH (1995) Extrachromosomal circular forms of the tobacco retrotransposon Tto1. Gene 165: 229–232.

27. FeuerbachF, DrouaudJ, LucasH (1997) Retrovirus-like end processing of the tobacco Tnt1 retrotransposon linear intermediates of replication. Journal of Virology 71: 4005–4015.

28. BerkhoutB, DasAT, BeerensN (2001) HIV-1 RNA editing, hypermutation, and error-prone reverse transcription. Science 292: 7.

29. CaoX, JacobsenSE (2002) Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyltransferase genes. Proceedings of the National Academy of Sciences USA 99(Suppl 4): 16491–16498.

30. WuC (1995) Heat shock transcription factors: structure and regulation. Annual Reviews in Cellular and Developmental Biology 11: 441–469.

31. von Koskull-DöringP, ScharfKD, NoverL (2007) The diversity of plant heat stress transcription factors. Trends in Plant Science 12: 452–457.

32. YoshidaT, OhamaN, NakajimaJ, KidokoroS, MizoiJ, et al. (2011) Arabidopsis HsfA1 transcription factors function as the main positive regulators in heat shock-responsive gene expression. Molecular Genetics and Genomics 286: 321–332.

33. BuschW, WunderlichM, SchofflF (2005) Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. Plant Journal 41: 1–14.

34. SchrammF, GanguliA, KiehlmannE, EnglichG, WalchD, et al. (2006) The heat stress transcription factor HsfA2 serves as a regulatory amplifier of a subset of genes in the heat stress response in Arabidopsis. Plant Molecular Biology 60: 759–772.

35. NishizawaA, YabutaY, YoshidaE, MarutaT, YoshimuraK, et al. (2006) Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant Journal 48: 535–547.

36. Garcia GuerreiroMP (2012) What makes transposable elements move in the Drosophila genome? Heredity 108: 461–468.

37. StrandDJ, McdonaldJF (1985) Copia Is transcriptionally responsive to environmental stress. Nucleic Acids Research 13: 4401–4410.

38. TakedaS, SugimotoK, KakutaniT, HirochikaH (2001) Linear DNA intermediates of the Tto1 retrotransposon in Gag particles accumulated in stressed tobacco and Arabidopsis thaliana. Plant Journal 28: 307–317.

39. Lang-MladekC, PopovaO, KiokK, BerlingerM, RakicB, et al. (2010) Transgenerational inheritance and resetting of stress-induced loss of epigenetic gene silencing in Arabidopsis. Molecular Plant 3: 594–602.

40. LiuHC, CharngYY (2013) Common and distinct functions of Arabidopsis class A1 and A2 heat shock factors in diverse abiotic stress responses and development. Plant Physiology 163: 276–290.

41. SlotkinRK, VaughnM, BorgesF, TanurdzicM, BeckerJD, et al. (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136: 461–472.

42. OhtsuK, SmithMB, EmrichSJ, BorsukLA, ZhouR, et al. (2007) Global gene expression analysis of the shoot apical meristem of maize (Zea mays L.). Plant Journal 52: 391–404.

43. MartinezG, SlotkinRK (2012) Developmental relaxation of transposable element silencing in plants: functional or byproduct? Current Opinions in Plant Biology 15: 496–502.

44. Arabidopsis GenomeI (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815.

45. HuettelB, KannoT, DaxingerL, AufsatzW, MatzkeAJ, et al. (2006) Endogenous targets of RNA-directed DNA methylation and Pol IV in Arabidopsis. EMBO Journal 25: 2828–2836.

46. JacksonJP, LindrothAM, CaoXF, JacobsenSE (2002) Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416: 556–560.

47. ZemachA, KimMY, HsiehPH, Coleman-DerrD, Eshed-WilliamsL, et al. (2013) The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153: 193–205.

48. ShuH, WildhaberT, SiretskiyA, GruissemW, HennigL (2012) Distinct modes of DNA accessibility in plant chromatin. Nature Communications 3: 1281.

49. ButelliE, LicciardelloC, ZhangY, LiuJ, MackayS, et al. (2012) Retrotransposons control fruit-specific, cold-dependent accumulation of anthocyanins in blood oranges. Plant Cell 24: 1242–1255.

50. LischD, SlotkinRK (2011) Strategies for silencing and escape: the ancient struggle between transposable elements and their hosts. International Reviews in Cellular and Molecular Biology 292: 119–152.

51. CharngYY, LiuHC, LiuNY, ChiWT, WangCN, et al. (2007) A heat-inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis. Plant Physiology 143: 251–262.

52. HendersonIR, JacobsenSE (2008) Tandem repeats upstream of the Arabidopsis endogene SDC recruit non-CG DNA methylation and initiate siRNA spreading. Genes & Development 22: 1597–1606.

53. LohmannC, Eggers-SchumacherG, WunderlichM, SchofflF (2004) Two different heat shock transcription factors regulate immediate early expression of stress genes in Arabidopsis. Molecular Genetics and Genomics 271: 11–21.

54. HruzT, WyssM, DocquierM, PfafflMW, MasanetzS, et al. (2011) RefGenes: identification of reliable and condition specific reference genes for RT-qPCR data normalization. BMC Genomics 12: 156.

55. CzechowskiT, StittM, AltmannT, UdvardiMK, ScheibleWR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiology 139: 5–17.

56. ChurchGM, GilbertW (1984) Genomic sequencing. Proceedings of the National Academy of Sciences of the USA 81: 1991–1995.

57. HetzlJ, FoersterAM, RaidlG, Mittelsten ScheidO (2007) CyMATE: a new tool for methylation analysis of plant genornic DNA after bisulphite sequencing. Plant Journal 51: 526–536.

58. HellmanLM, FriedMG (2007) Electrophoretic mobility shift assay (EMSA) for detecting protein-nucleic acid interactions. Nature Protocols 2: 1849–1861.

59. KarimiM, InzeD, DepickerA (2002) GATEWAY((TM)) vectors for Agrobacterium-mediated plant transformation. Trends in Plant Science 7: 193–195.

60. CloughSJ, BentAF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant Journal 16: 735–743.

61. PecinkaA, RosaM, SchikoraA, BerlingerM, HirtH, et al. (2009) Transgenerational stress memory is not a general response in Arabidopsis. PLoS One 4: e5202.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2014 Číslo 1
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa