Genome expansion of Arabis alpina linked with retrotransposition and reduced symmetric DNA methylation

Eva Maria Willing; Vimal Rawat; Terezie Mandáková; Florian Maumus; Geo Velikkakam James; Karl J.V. Nordström; Claude Becker; Norman Warthmann; Claudia Chica; Bogna Szarzynska; Matthias Zytnicki; Maria C. Albani; Christiane Kiefer; Sara Bergonzi; Loren Castaings; Julieta L. Mateos; Markus C. Berns; Nora Bujdoso; Thomas Piofczyk; Laura De Lorenzo; Cristina Barrero-Sicilia; Isabel Mateos; Mathieu Piednoël; Jörg Hagmann; Romy Chen-Min-Tao; Raquel Iglesias-Fernández; Stephan C. Schuster; Carlos Alonso-Blanco; François Roudier; Pilar Carbonero; Javier Paz-Ares; Seth J. Davis; Ales Pecinka; Hadi Quesneville; Vincent Colot; Martin A. Lysak; Detlef Weigel; George Coupland; Korbinian Schneeberger

doi:10.1038/nplants.2014.23

Genome expansion of Arabis alpina linked with retrotransposition and reduced symmetric DNA methylation

Eva Maria Willing, Vimal Rawat, Terezie Mandáková, Florian Maumus, Geo Velikkakam James, Karl J.V. Nordström, Claude Becker, Norman Warthmann, Claudia Chica, Bogna Szarzynska, Matthias Zytnicki, Maria C. Albani, Christiane Kiefer, Sara Bergonzi, Loren Castaings, Julieta L. Mateos, Markus C. Berns, Nora Bujdoso, Thomas Piofczyk, Laura De LorenzoCristina Barrero-Sicilia, Isabel Mateos, Mathieu Piednoël, Jörg Hagmann, Romy Chen-Min-Tao, Raquel Iglesias-Fernández, Stephan C. Schuster, Carlos Alonso-Blanco, François Roudier, Pilar Carbonero, Javier Paz-Ares, Seth J. Davis, Ales Pecinka, Hadi Quesneville, Vincent Colot, Martin A. Lysak, Detlef Weigel, George Coupland, Korbinian Schneeberger

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Abstract

Despite evolutionary conserved mechanisms to silence transposable element activity, there are drastic differences in the abundance of transposable elements even among closely related plant species. We conducted a de novo assembly for the 375 .Mb genome of the perennial model plant, Arabis alpina. Analysing this genome revealed long-lasting and recent transposable element activity predominately driven by Gypsy long terminal repeat retrotransposons, which extended the low-recombining pericentromeres and transformed large formerly euchromatic regions into repeat-rich pericentromeric regions. This reduced capacity for long terminal repeat retrotransposon silencing and removal in A. alpina co-occurs with unexpectedly low levels of DNA methylation. Most remarkably, the striking reduction of symmetrical CG and CHG methylation suggests weakened DNA methylation maintenance in A. alpina compared with Arabidopsis thaliana. Phylogenetic analyses indicate a highly dynamic evolution of some components of methylation maintenance machinery that might be related to the unique methylation in A. alpina.

Original language	English
Article number	14023
Journal	Nature Plants
Volume	1
DOIs	https://doi.org/10.1038/nplants.2014.23
Publication status	Published - 2 Feb 2015

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Willing, E. M., Rawat, V., Mandáková, T., Maumus, F., James, G. V., Nordström, K. J. V., Becker, C., Warthmann, N., Chica, C., Szarzynska, B., Zytnicki, M., Albani, M. C., Kiefer, C., Bergonzi, S., Castaings, L., Mateos, J. L., Berns, M. C., Bujdoso, N., Piofczyk, T., ... Schneeberger, K. (2015). Genome expansion of Arabis alpina linked with retrotransposition and reduced symmetric DNA methylation. Nature Plants, 1, Article 14023. https://doi.org/10.1038/nplants.2014.23

@article{c089907727ae45538d783f68b53e8643,

title = "Genome expansion of Arabis alpina linked with retrotransposition and reduced symmetric DNA methylation",

abstract = "Despite evolutionary conserved mechanisms to silence transposable element activity, there are drastic differences in the abundance of transposable elements even among closely related plant species. We conducted a de novo assembly for the 375 .Mb genome of the perennial model plant, Arabis alpina. Analysing this genome revealed long-lasting and recent transposable element activity predominately driven by Gypsy long terminal repeat retrotransposons, which extended the low-recombining pericentromeres and transformed large formerly euchromatic regions into repeat-rich pericentromeric regions. This reduced capacity for long terminal repeat retrotransposon silencing and removal in A. alpina co-occurs with unexpectedly low levels of DNA methylation. Most remarkably, the striking reduction of symmetrical CG and CHG methylation suggests weakened DNA methylation maintenance in A. alpina compared with Arabidopsis thaliana. Phylogenetic analyses indicate a highly dynamic evolution of some components of methylation maintenance machinery that might be related to the unique methylation in A. alpina.",

author = "Willing, {Eva Maria} and Vimal Rawat and Terezie Mand{\'a}kov{\'a} and Florian Maumus and James, {Geo Velikkakam} and Nordstr{\"o}m, {Karl J.V.} and Claude Becker and Norman Warthmann and Claudia Chica and Bogna Szarzynska and Matthias Zytnicki and Albani, {Maria C.} and Christiane Kiefer and Sara Bergonzi and Loren Castaings and Mateos, {Julieta L.} and Berns, {Markus C.} and Nora Bujdoso and Thomas Piofczyk and {De Lorenzo}, Laura and Cristina Barrero-Sicilia and Isabel Mateos and Mathieu Piedno{\"e}l and J{\"o}rg Hagmann and Romy Chen-Min-Tao and Raquel Iglesias-Fern{\'a}ndez and Schuster, {Stephan C.} and Carlos Alonso-Blanco and Fran{\c c}ois Roudier and Pilar Carbonero and Javier Paz-Ares and Davis, {Seth J.} and Ales Pecinka and Hadi Quesneville and Vincent Colot and Lysak, {Martin A.} and Detlef Weigel and George Coupland and Korbinian Schneeberger",

note = "This document is the Accepted Manuscript version, made available in accordance to Springer Nature Terms of reuse of archived manuscripts. ",

year = "2015",

month = feb,

day = "2",

doi = "10.1038/nplants.2014.23",

language = "English",

volume = "1",

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Willing, EM, Rawat, V, Mandáková, T, Maumus, F, James, GV, Nordström, KJV, Becker, C, Warthmann, N, Chica, C, Szarzynska, B, Zytnicki, M, Albani, MC, Kiefer, C, Bergonzi, S, Castaings, L, Mateos, JL, Berns, MC, Bujdoso, N, Piofczyk, T, De Lorenzo, L, Barrero-Sicilia, C, Mateos, I, Piednoël, M, Hagmann, J, Chen-Min-Tao, R, Iglesias-Fernández, R, Schuster, SC, Alonso-Blanco, C, Roudier, F, Carbonero, P, Paz-Ares, J, Davis, SJ, Pecinka, A, Quesneville, H, Colot, V, Lysak, MA, Weigel, D, Coupland, G & Schneeberger, K 2015, 'Genome expansion of Arabis alpina linked with retrotransposition and reduced symmetric DNA methylation', Nature Plants, vol. 1, 14023. https://doi.org/10.1038/nplants.2014.23

TY - JOUR

T1 - Genome expansion of Arabis alpina linked with retrotransposition and reduced symmetric DNA methylation

AU - Willing, Eva Maria

AU - Rawat, Vimal

AU - Mandáková, Terezie

AU - Maumus, Florian

AU - James, Geo Velikkakam

AU - Nordström, Karl J.V.

AU - Becker, Claude

AU - Warthmann, Norman

AU - Chica, Claudia

AU - Szarzynska, Bogna

AU - Zytnicki, Matthias

AU - Albani, Maria C.

AU - Kiefer, Christiane

AU - Bergonzi, Sara

AU - Castaings, Loren

AU - Mateos, Julieta L.

AU - Berns, Markus C.

AU - Bujdoso, Nora

AU - Piofczyk, Thomas

AU - De Lorenzo, Laura

AU - Barrero-Sicilia, Cristina

AU - Mateos, Isabel

AU - Piednoël, Mathieu

AU - Hagmann, Jörg

AU - Chen-Min-Tao, Romy

AU - Iglesias-Fernández, Raquel

AU - Schuster, Stephan C.

AU - Alonso-Blanco, Carlos

AU - Roudier, François

AU - Carbonero, Pilar

AU - Paz-Ares, Javier

AU - Davis, Seth J.

AU - Pecinka, Ales

AU - Quesneville, Hadi

AU - Colot, Vincent

AU - Lysak, Martin A.

AU - Weigel, Detlef

AU - Coupland, George

AU - Schneeberger, Korbinian

N1 - This document is the Accepted Manuscript version, made available in accordance to Springer Nature Terms of reuse of archived manuscripts.

PY - 2015/2/2

Y1 - 2015/2/2

N2 - Despite evolutionary conserved mechanisms to silence transposable element activity, there are drastic differences in the abundance of transposable elements even among closely related plant species. We conducted a de novo assembly for the 375 .Mb genome of the perennial model plant, Arabis alpina. Analysing this genome revealed long-lasting and recent transposable element activity predominately driven by Gypsy long terminal repeat retrotransposons, which extended the low-recombining pericentromeres and transformed large formerly euchromatic regions into repeat-rich pericentromeric regions. This reduced capacity for long terminal repeat retrotransposon silencing and removal in A. alpina co-occurs with unexpectedly low levels of DNA methylation. Most remarkably, the striking reduction of symmetrical CG and CHG methylation suggests weakened DNA methylation maintenance in A. alpina compared with Arabidopsis thaliana. Phylogenetic analyses indicate a highly dynamic evolution of some components of methylation maintenance machinery that might be related to the unique methylation in A. alpina.

AB - Despite evolutionary conserved mechanisms to silence transposable element activity, there are drastic differences in the abundance of transposable elements even among closely related plant species. We conducted a de novo assembly for the 375 .Mb genome of the perennial model plant, Arabis alpina. Analysing this genome revealed long-lasting and recent transposable element activity predominately driven by Gypsy long terminal repeat retrotransposons, which extended the low-recombining pericentromeres and transformed large formerly euchromatic regions into repeat-rich pericentromeric regions. This reduced capacity for long terminal repeat retrotransposon silencing and removal in A. alpina co-occurs with unexpectedly low levels of DNA methylation. Most remarkably, the striking reduction of symmetrical CG and CHG methylation suggests weakened DNA methylation maintenance in A. alpina compared with Arabidopsis thaliana. Phylogenetic analyses indicate a highly dynamic evolution of some components of methylation maintenance machinery that might be related to the unique methylation in A. alpina.

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U2 - 10.1038/nplants.2014.23

DO - 10.1038/nplants.2014.23

M3 - Article

AN - SCOPUS:84986194435

VL - 1

JO - Nature Plants

JF - Nature Plants

M1 - 14023

ER -

Genome expansion of Arabis alpina linked with retrotransposition and reduced symmetric DNA methylation

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