Derepression of the Plant Chromovirus Induces Germline Transposition in Regenerated Plants
Transposable elements represent a large proportion of the eukaryotic genomes. Long Terminal Repeat (LTR) retrotransposons are very abundant and constitute the predominant family of transposable elements in plants. Recent studies have identified chromoviruses to be a widely distributed lineage of Gypsy elements. These elements contain chromodomains in their integrases, which suggests a preference for insertion into heterochromatin. In turn, this preference might have contributed to the patterning of heterochromatin observed in host genomes. Despite their potential importance for our understanding of plant genome dynamics and evolution, the regulatory mechanisms governing the behavior of chromoviruses and their activities remain largely uncharacterized. Here, we report a detailed analysis of the spatio-temporal activity of a plant chromovirus in the endogenous host. We examined LORE1a, a member of the endogenous chromovirus LORE1 family from the model legume Lotus japonicus. We found that this chromovirus is stochastically de-repressed in plant populations regenerated from de-differentiated cells and that LORE1a transposes in the male germline. Bisulfite sequencing of the 5′ LTR and its surrounding region suggests that tissue culture induces a loss of epigenetic silencing of LORE1a. Since LTR promoter activity is pollen specific, as shown by the analysis of transgenic plants containing an LTR::GUS fusion, we conclude that male germline-specific LORE1a transposition in pollen grains is controlled transcriptionally by its own cis-elements. New insertion sites of LORE1a copies were frequently found in genic regions and show no strong insertional preferences. These distinctive novel features of LORE1 indicate that this chromovirus has considerable potential for generating genetic and epigenetic diversity in the host plant population. Our results also define conditions for the use of LORE1a as a genetic tool.
Vyšlo v časopise:
Derepression of the Plant Chromovirus Induces Germline Transposition in Regenerated Plants. PLoS Genet 6(3): e32767. doi:10.1371/journal.pgen.1000868
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1000868
Souhrn
Transposable elements represent a large proportion of the eukaryotic genomes. Long Terminal Repeat (LTR) retrotransposons are very abundant and constitute the predominant family of transposable elements in plants. Recent studies have identified chromoviruses to be a widely distributed lineage of Gypsy elements. These elements contain chromodomains in their integrases, which suggests a preference for insertion into heterochromatin. In turn, this preference might have contributed to the patterning of heterochromatin observed in host genomes. Despite their potential importance for our understanding of plant genome dynamics and evolution, the regulatory mechanisms governing the behavior of chromoviruses and their activities remain largely uncharacterized. Here, we report a detailed analysis of the spatio-temporal activity of a plant chromovirus in the endogenous host. We examined LORE1a, a member of the endogenous chromovirus LORE1 family from the model legume Lotus japonicus. We found that this chromovirus is stochastically de-repressed in plant populations regenerated from de-differentiated cells and that LORE1a transposes in the male germline. Bisulfite sequencing of the 5′ LTR and its surrounding region suggests that tissue culture induces a loss of epigenetic silencing of LORE1a. Since LTR promoter activity is pollen specific, as shown by the analysis of transgenic plants containing an LTR::GUS fusion, we conclude that male germline-specific LORE1a transposition in pollen grains is controlled transcriptionally by its own cis-elements. New insertion sites of LORE1a copies were frequently found in genic regions and show no strong insertional preferences. These distinctive novel features of LORE1 indicate that this chromovirus has considerable potential for generating genetic and epigenetic diversity in the host plant population. Our results also define conditions for the use of LORE1a as a genetic tool.
Zdroje
1. KumarA
BennetzenJL
1999 Plant retrotransposons. Annu Rev Genet 33 479 532
2. FeschotteC
JiangN
WesslerSR
2002 Plant transposable elements: where genetics meets genomics. Nat Rev Genet 3 329 341
3. VitteC
PanaudO
QuesnevilleH
2007 LTR retrotransposons in rice (Oryza sativa, L.): recent burst amplifications followed by rapid DNA loss. BMC Genomics 8 218
4. WangH
LiuJS
2008 LTR retrotransposon landscape in Medicago truncatula: more rapid removal than in rice. BMC Genomics 9 382
5. ZhangX
WesslerSR
2004 Genome-wide comparative analysis of the transposable elements in the related species Arabidopsis thaliana and Brassica oleracea. Proc Natl Acad Sci U S A 101 5589 5594
6. DuC
SwigonováZ
MessingJ
2006 Retrotranspositions in orthologous regions of closely related grass species. BMC Evol Biol 6 62
7. VitteC
PanaudO
2005 LTR retrotransposons and flowering plant genome size: emergence of the increase/decrease model. Cytogenet Genome Res 110 91 107
8. WickerT
SabotF
Hua-VanA
BennetzenJL
CapyP
2007 A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8 973 982
9. Arabidopsis Genome Initiative 2000 Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408 796 815
10. TuskanGA
DifazioS
JanssonS
BohlmannJ
GrigorievI
2006 The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313 1596 1604
11. Rice Annotation Project 2007 Curated genome annotation of Oryza sativa ssp. japonica and comparative genome analysis with Arabidopsis thaliana. Genome Res 17 175 183
12. MingR
HouS
FengY
YuQ
Dionne-LaporteA
2008 The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452 991 996
13. SatoS
NakamuraY
KanekoT
AsamizuE
KatoT
2008 Genome structure of the legume, Lotus japonicus. DNA Res 15 227 239
14. The French-Italian Public Consortium for Grapevine Genome Characterization 2007 The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449 463 467
15. MalikHS
EickbushTH
1999 Modular evolution of the integrase domain in the Ty3/Gypsy class of LTR retrotransposons. J Virol 73 5186 5190
16. GorinsekB
GubensekF
KordisD
2004 Evolutionary genomics of chromoviruses in eukaryotes. Mol Biol Evol 21 781 798
17. NakayashikiH
AwaT
TosaY
MayamaS
2005 The C-terminal chromodomain-like module in the integrase domain is crucial for high transposition efficiency of the retrotransposon MAGGY. FEBS Lett 579 488 492
18. GaoX
HouY
EbinaH
LevinHL
VoytasDF
2008 Chromodomains direct integration of retrotransposons to heterochromatin. Genome Res 18 359 369
19. NovikovaO
MayorovV
SmyshlyaevG
FursovM
AdkisonL
2008 Novel clades of chromodomain-containing Gypsy LTR retrotransposons from mosses (Bryophyta). Plant J 56 562 574
20. ChengZ
DongF
LangdonT
OuyangS
BuellCR
2002 Functional rice centromeres are marked by a satellite repeat and a centromere-specific retrotransposon. Plant Cell 14 1691 1704
21. ZhongCX
MarshallJB
ToppC
MroczekR
KatoA
2002 Centromeric retroelements and satellites interact with maize kinetochore protein CENH3. Plant Cell 14 2825 2836
22. NagakiK
MurataM
2005 Characterization of CENH3 and centromere-associated DNA sequences in sugarcane. Chromosome Res 13 195 203
23. WeberB
SchmidtT
2009 Nested Ty3-gypsy retrotransposons of a single Beta procumbens centromere contain a putative chromodomain. Chromosome Res 17 379 396
24. CasacubertaJM
GrandbastienMA
1993 Characterisation of LTR sequences involved in the protoplast specific expression of the tobacco Tnt1 retrotransposon. Nucleic Acids Res 21 2087 2093
25. HirochikaH
1993 Activation of tobacco retrotransposons during tissue culture. EMBO J 12 2521 2528
26. HirochikaH
SugimotoK
OtsukiY
TsugawaH
KandaM
1996 Retrotransposons of rice involved in mutations induced by tissue culture. Proc Natl Acad Sci U S A 93 7783 7788
27. DingY
WangX
SuL
ZhaiJ
CaoS
2007 SDG714, a histone H3K9 methyltransferase, is involved in Tos17 DNA methylation and transposition in rice. Plant Cell 19 9 22
28. MadsenLH
FukaiE
RadutoiuS
YostCK
SandalN
2005 LORE1, an active low-copy-number Gypsy retrotransposon family in the model legume Lotus japonicus. Plant J 44 372 381
29. FukaiE
DobrowolskaAD
MadsenLH
MadsenEB
UmeharaY
2008 Transposition of a 600 thousand-year-old LTR retrotransposon in the model legume Lotus japonicus. Plant Mol Biol 68 653 663
30. ThykjærT
StillerJ
HandbergK
JonesJ
StougaardJ
1995 The maize transposable element Ac is mobile in the legume Lotus japonicus. Plant Mol Biol 27 981 993
31. SchauserL
HandbergK
SandalN
StillerJ
ThykjærT
1998 Symbiotic mutants deficient in nodule establishment identified after T-DNA transformation of Lotus japonicus. Mol Gen Genet 259 414 423
32. YokotaK
FukaiE
MadsenLH
JurkiewiczA
RuedaP
2009 Rearrangement of actin cytoskeleton mediates invasion of Lotus japonicus roots by Mesorhizobium loti. Plant Cell 21 267 284
33. HirochikaH
OkamotoH
KakutaniT
2000 Silencing of retrotransposons in Arabidopsis and reactivation by the ddm1 mutation. Plant Cell 12 357 369
34. Perez-HormaecheJ
PotetF
BeauclairL
Le MassonI
CourtialB
2008 Invasion of the Arabidopsis genome by the tobacco retrotransposon Tnt1 is controlled by reversible transcriptional gene silencing. Plant Physiol 147 1264 1278
35. McClellandM
NelsonM
RaschkeE
1994 Effect of site-specific modification on restriction endonucleases and DNA modification methyltransferases. Nucleic Acids Res 22 3640 3659
36. MetteMF
AufsatzW
van der WindenJ
MatzkeMA
MatzkeAJ
2000 Transcriptional silencing and promoter methylation triggered by double-stranded RNA. EMBO J 19 5194 5201
37. WilkinsonJE
TwellD
LindseyK
1997 Activities of CaMV 35S and nos promoters in pollen: implications for field release of transgenic plants. J Exp Bot 48 265 275
38. FischerU
KuhlmannM
PecinkaA
SchmidtR
MetteMF
2007 Local DNA features affect RNA-directed transcriptional gene silencing and DNA methylation. Plant J 53 1 10
39. BorgesF
GomesG
GardnerR
MorenoN
McCormickS
2008 Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiol 148 1168 1181
40. SlotkinRK
VaughnM
BorgesF
TanurdzicM
BeckerJD
2009 Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136 461 472
41. KomatsuM
ShimamotoK
KyozukaJ
2003 Two-step regulation and continuous retrotransposition of the rice LINE-type retrotransposon Karma. Plant Cell 15 1934 1944
42. ReindersJ
WulffBB
MirouzeM
Mari-OrdonezA
DappM
2009 Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes Dev 23 939 950
43. MeissnerA
MikkelsenTS
GuH
WernigM
HannaJ
2008 Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 454 766 770
44. TanurdzicM
VaughnMW
JiangH
LeeTJ
SlotkinRK
2008 Epigenomic consequences of immortalized plant cell suspension culture. PLoS Biol 6 e302 doi:10.1371/journal.pbio.0060302
45. SinghJ
FreelingM
LischD
2008 A position effect on the heritability of epigenetic silencing. PLoS Genet 4 e1000216 doi:10.1371/journal.pgen.1000216
46. ChengC
DaigenM
HirochikaH
2006 Epigenetic regulation of the rice retrotransposon Tos17. Mol Genet Genomics 276 378 390
47. OkadaT
EndoM
SinghMB
BhallaPL
2005 Analysis of the histone H3 gene family in Arabidopsis and identification of the male-gamete-specific variant AtMGH3. Plant J 44 557 568
48. IngouffM
HamamuraY
GourguesM
HigashiyamaT
BergerF
2007 Distinct dynamics of HISTONE3 variants between the two fertilization products in plants. Curr Biol 17 1032 1037
49. SakamotoK
OhmidoN
FukuiK
KamadaH
SatohS
2000 Site-specific accumulation of a LINE-like retrotransposon in a sex chromosome of the dioecious plant Cannabis sativa. Plant Mol Biol 44 723 732
50. CermakT
KubatZ
HobzaR
KoblizkovaA
WidmerA
2008 Survey of repetitive sequences in Silene latifolia with respect to their distribution on sex chromosomes. Chromosome Res 16 961 976
51. TsukaharaS
KobayashiA
KawabeA
MathieuO
MiuraA
2009 Bursts of retrotransposition reproduced in Arabidopsis. Nature 461 423 426
52. HandbergK
StougaardJ
1992 Lotus japonicus, an autogamous, diploid legume species for classical and molecular genetics. Plant J 2 487 496
53. ThykjærT
SchauserL
DanielsenD
FinnemanJ
StougaardJ
1998 Agrobacterium-mediated transformation of the diploid legume Lotus japonicus. Cell Biology: a Laboratory Handbook, Ed 23 518 525
54. AndersenSU
CvitanichC
GrønlundM
BuskH
JensenDB
2005 Vectors for reverse genetics and expression analysis. in: Lotus japonicus handbook Springer 289 292
55. CloughSJ
BentAF
1998 Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16 735 743
56. ChangS
PuryearJ
CairneyJ
1993 A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11 113 116
57. KumakiY
OdaM
OkanoM
2008 QUMA: quantification tool for methylation analysis. Nucleic Acids Res 36 W170 W175
58. HetzlJ
FoersterAM
RaidlG
Mittelsten ScheidO
2007 CyMATE: a new tool for methylation analysis of plant genomic DNA after bisulphite sequencing. Plant J 51 526 536
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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