From immunity to susceptibility: Virus resistance induced in tomato by a silenced transgene is lost as TGS overcomes PTGS

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From immunity to susceptibility : Virus resistance induced in tomato by a silenced transgene is lost as TGS overcomes PTGS. / Catoni, Marco; Lucioli, Alessandra; Doblas-Ibáñez, Paula; Accotto, Gian Paolo; Vaira, Anna Maria.

In: Plant Journal, Vol. 75, No. 6, 01.09.2013, p. 941-953.

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Catoni, Marco ; Lucioli, Alessandra ; Doblas-Ibáñez, Paula ; Accotto, Gian Paolo ; Vaira, Anna Maria. / From immunity to susceptibility : Virus resistance induced in tomato by a silenced transgene is lost as TGS overcomes PTGS. In: Plant Journal. 2013 ; Vol. 75, No. 6. pp. 941-953.

Bibtex

@article{9cd40c1d12f44988a7af7dad27222fb7,
title = "From immunity to susceptibility: Virus resistance induced in tomato by a silenced transgene is lost as TGS overcomes PTGS",
abstract = "Tomato line 30.4 was obtained engineering the nucleocapsid (N) gene of tomato spotted wilt virus into plant genome, and immunity to tomato spotted wilt virus infection of its self-pollinated homozygous progeny was observed. Despite the presence of a high amount of transgenic transcripts, transgenic proteins have not been detected, suggesting a mechanism of resistance mediated by RNA. In the present study, we identify post-transcriptional gene silencing as the main mechanism of resistance, which is able to spread systemically through grafting, and show that the line 30.4 resistant plants produce both 24 and 21-22 nt N-gene specific siRNA classes. The transgenic locus in chromosome 4 shows complex multiple insertions of four T-DNA copies in various orientations, all with 3′ end deletions in the terminator and part of the N gene. However, for three of them, polyadenylated transcripts are produced, due to flanking tomato genome sequences acting as alternative terminators. Interestingly, starting at the fifth generation after the transformation event, some individual plants show a tomato spotted wilt virus-susceptible phenotype. The change is associated with the disappearance of transgene-specific transcripts and siRNAs, and with hyper-methylation of the transgene, which proceeds gradually through the generations. Once it reaches a critical threshold, the shift from post-transcriptional gene silencing to transcriptional silencing of the transgene eliminates the previously well established virus resistance.",
keywords = "DNA methylation, epigenetics, grafting, Solanum lycopersicum, systemic resistance, tospovirus, transgenerational methylation, transgenerational silencing",
author = "Marco Catoni and Alessandra Lucioli and Paula Doblas-Ib{\'a}{\~n}ez and Accotto, {Gian Paolo} and Vaira, {Anna Maria}",
year = "2013",
month = sep,
day = "1",
doi = "10.1111/tpj.12253",
language = "English",
volume = "75",
pages = "941--953",
journal = "The Plant journal : for cell and molecular biology",
issn = "0960-7412",
publisher = "Wiley",
number = "6",

}

RIS

TY - JOUR

T1 - From immunity to susceptibility

T2 - Virus resistance induced in tomato by a silenced transgene is lost as TGS overcomes PTGS

AU - Catoni, Marco

AU - Lucioli, Alessandra

AU - Doblas-Ibáñez, Paula

AU - Accotto, Gian Paolo

AU - Vaira, Anna Maria

PY - 2013/9/1

Y1 - 2013/9/1

N2 - Tomato line 30.4 was obtained engineering the nucleocapsid (N) gene of tomato spotted wilt virus into plant genome, and immunity to tomato spotted wilt virus infection of its self-pollinated homozygous progeny was observed. Despite the presence of a high amount of transgenic transcripts, transgenic proteins have not been detected, suggesting a mechanism of resistance mediated by RNA. In the present study, we identify post-transcriptional gene silencing as the main mechanism of resistance, which is able to spread systemically through grafting, and show that the line 30.4 resistant plants produce both 24 and 21-22 nt N-gene specific siRNA classes. The transgenic locus in chromosome 4 shows complex multiple insertions of four T-DNA copies in various orientations, all with 3′ end deletions in the terminator and part of the N gene. However, for three of them, polyadenylated transcripts are produced, due to flanking tomato genome sequences acting as alternative terminators. Interestingly, starting at the fifth generation after the transformation event, some individual plants show a tomato spotted wilt virus-susceptible phenotype. The change is associated with the disappearance of transgene-specific transcripts and siRNAs, and with hyper-methylation of the transgene, which proceeds gradually through the generations. Once it reaches a critical threshold, the shift from post-transcriptional gene silencing to transcriptional silencing of the transgene eliminates the previously well established virus resistance.

AB - Tomato line 30.4 was obtained engineering the nucleocapsid (N) gene of tomato spotted wilt virus into plant genome, and immunity to tomato spotted wilt virus infection of its self-pollinated homozygous progeny was observed. Despite the presence of a high amount of transgenic transcripts, transgenic proteins have not been detected, suggesting a mechanism of resistance mediated by RNA. In the present study, we identify post-transcriptional gene silencing as the main mechanism of resistance, which is able to spread systemically through grafting, and show that the line 30.4 resistant plants produce both 24 and 21-22 nt N-gene specific siRNA classes. The transgenic locus in chromosome 4 shows complex multiple insertions of four T-DNA copies in various orientations, all with 3′ end deletions in the terminator and part of the N gene. However, for three of them, polyadenylated transcripts are produced, due to flanking tomato genome sequences acting as alternative terminators. Interestingly, starting at the fifth generation after the transformation event, some individual plants show a tomato spotted wilt virus-susceptible phenotype. The change is associated with the disappearance of transgene-specific transcripts and siRNAs, and with hyper-methylation of the transgene, which proceeds gradually through the generations. Once it reaches a critical threshold, the shift from post-transcriptional gene silencing to transcriptional silencing of the transgene eliminates the previously well established virus resistance.

KW - DNA methylation

KW - epigenetics

KW - grafting

KW - Solanum lycopersicum

KW - systemic resistance

KW - tospovirus

KW - transgenerational methylation

KW - transgenerational silencing

UR - http://www.scopus.com/inward/record.url?scp=84883770073&partnerID=8YFLogxK

U2 - 10.1111/tpj.12253

DO - 10.1111/tpj.12253

M3 - Article

C2 - 23738576

AN - SCOPUS:84883770073

VL - 75

SP - 941

EP - 953

JO - The Plant journal : for cell and molecular biology

JF - The Plant journal : for cell and molecular biology

SN - 0960-7412

IS - 6

ER -