Aphid feeding induces the relaxation of epigenetic control and the associated regulation of the defense response in Arabidopsis

Maria Luz Annacondia; Dimitrije Markovic; Juan Luis Reig-Valiente; Vassilis Scaltsoyiannes; Corné M J Pieterse; Velemir Ninkovic; R Keith Slotkin; German Martinez

doi:10.1111/nph.17226

Aphid feeding induces the relaxation of epigenetic control and the associated regulation of the defense response in Arabidopsis

Maria Luz Annacondia
, Dimitrije Markovic
, Juan Luis Reig-Valiente
, Vassilis Scaltsoyiannes
, Corné M J Pieterse
, Velemir Ninkovic
, R Keith Slotkin
, German Martinez

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

Environmentally induced changes in the epigenome help individuals to quickly adapt to fluctuations in the conditions of their habitats. We explored those changes in Arabidopsis thaliana plants subjected to multiple biotic and abiotic stresses, and identified transposable element (TE) activation in plants infested with the green peach aphid, Myzus persicae. We performed a genome-wide analysis mRNA expression, small RNA accumulation and DNA methylation Our results demonstrate that aphid feeding induces loss of methylation of hundreds of loci, mainly TEs. This loss of methylation has the potential to regulate gene expression and we found evidence that it is involved in the control of plant immunity genes. Accordingly, mutant plants deficient in DNA and H3K9 methylation (kyp) showed increased resistance to M. persicae infestation. Collectively, our results show that changes in DNA methylation play a significant role in the regulation of the plant transcriptional response and induction of defense response against aphid feeding.

Original language	English
Pages (from-to)	1185-1200
Number of pages	16
Journal	New Phytologist
Volume	230
Issue number	3
DOIs	https://doi.org/10.1111/nph.17226
Publication status	Published - May 2021

Bibliographical note

Funding Information:
Research in the Martinez group is supported by SLU, the Carl Tryggers Foundation and the Swedish Research Council (VR 2016‐05410). Sequencing was performed by the SNP&SEQ Technology Platform in Uppsala. The facility is part of the National Genomics Infrastructure (NGI) Sweden and Science for Life Laboratory. The SNP&SEQ Platform is also supported by the Swedish Research Council and the Knut and Alice Wallenberg Foundation.

Publisher Copyright:
© 2021 The Authors New Phytologist ©2021 New Phytologist Foundation

Keywords

Arabidopsis
aphids
defense response
epigenetics
transcriptional regulation
transposable elements

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nph.17226Final published version, 3.16 MBLicence: CC BY-NC-ND

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title = "Aphid feeding induces the relaxation of epigenetic control and the associated regulation of the defense response in Arabidopsis",

abstract = "Environmentally induced changes in the epigenome help individuals to quickly adapt to fluctuations in the conditions of their habitats. We explored those changes in Arabidopsis thaliana plants subjected to multiple biotic and abiotic stresses, and identified transposable element (TE) activation in plants infested with the green peach aphid, Myzus persicae. We performed a genome-wide analysis mRNA expression, small RNA accumulation and DNA methylation Our results demonstrate that aphid feeding induces loss of methylation of hundreds of loci, mainly TEs. This loss of methylation has the potential to regulate gene expression and we found evidence that it is involved in the control of plant immunity genes. Accordingly, mutant plants deficient in DNA and H3K9 methylation (kyp) showed increased resistance to M. persicae infestation. Collectively, our results show that changes in DNA methylation play a significant role in the regulation of the plant transcriptional response and induction of defense response against aphid feeding.",

keywords = "Arabidopsis, aphids, defense response, epigenetics, transcriptional regulation, transposable elements",

author = "Annacondia, \{Maria Luz\} and Dimitrije Markovic and Reig-Valiente, \{Juan Luis\} and Vassilis Scaltsoyiannes and Pieterse, \{Corn{\'e} M J\} and Velemir Ninkovic and Slotkin, \{R Keith\} and German Martinez",

note = "Funding Information: Research in the Martinez group is supported by SLU, the Carl Tryggers Foundation and the Swedish Research Council (VR 2016‐05410). Sequencing was performed by the SNP\&SEQ Technology Platform in Uppsala. The facility is part of the National Genomics Infrastructure (NGI) Sweden and Science for Life Laboratory. The SNP\&SEQ Platform is also supported by the Swedish Research Council and the Knut and Alice Wallenberg Foundation. Publisher Copyright: {\textcopyright} 2021 The Authors New Phytologist {\textcopyright}2021 New Phytologist Foundation",

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month = may,

doi = "10.1111/nph.17226",

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AU - Annacondia, Maria Luz

AU - Markovic, Dimitrije

AU - Reig-Valiente, Juan Luis

AU - Scaltsoyiannes, Vassilis

AU - Pieterse, Corné M J

AU - Ninkovic, Velemir

AU - Slotkin, R Keith

AU - Martinez, German

N1 - Funding Information: Research in the Martinez group is supported by SLU, the Carl Tryggers Foundation and the Swedish Research Council (VR 2016‐05410). Sequencing was performed by the SNP&SEQ Technology Platform in Uppsala. The facility is part of the National Genomics Infrastructure (NGI) Sweden and Science for Life Laboratory. The SNP&SEQ Platform is also supported by the Swedish Research Council and the Knut and Alice Wallenberg Foundation. Publisher Copyright: © 2021 The Authors New Phytologist ©2021 New Phytologist Foundation

PY - 2021/5

Y1 - 2021/5

N2 - Environmentally induced changes in the epigenome help individuals to quickly adapt to fluctuations in the conditions of their habitats. We explored those changes in Arabidopsis thaliana plants subjected to multiple biotic and abiotic stresses, and identified transposable element (TE) activation in plants infested with the green peach aphid, Myzus persicae. We performed a genome-wide analysis mRNA expression, small RNA accumulation and DNA methylation Our results demonstrate that aphid feeding induces loss of methylation of hundreds of loci, mainly TEs. This loss of methylation has the potential to regulate gene expression and we found evidence that it is involved in the control of plant immunity genes. Accordingly, mutant plants deficient in DNA and H3K9 methylation (kyp) showed increased resistance to M. persicae infestation. Collectively, our results show that changes in DNA methylation play a significant role in the regulation of the plant transcriptional response and induction of defense response against aphid feeding.

AB - Environmentally induced changes in the epigenome help individuals to quickly adapt to fluctuations in the conditions of their habitats. We explored those changes in Arabidopsis thaliana plants subjected to multiple biotic and abiotic stresses, and identified transposable element (TE) activation in plants infested with the green peach aphid, Myzus persicae. We performed a genome-wide analysis mRNA expression, small RNA accumulation and DNA methylation Our results demonstrate that aphid feeding induces loss of methylation of hundreds of loci, mainly TEs. This loss of methylation has the potential to regulate gene expression and we found evidence that it is involved in the control of plant immunity genes. Accordingly, mutant plants deficient in DNA and H3K9 methylation (kyp) showed increased resistance to M. persicae infestation. Collectively, our results show that changes in DNA methylation play a significant role in the regulation of the plant transcriptional response and induction of defense response against aphid feeding.

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KW - epigenetics

KW - transcriptional regulation

KW - transposable elements

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JO - New Phytologist

JF - New Phytologist

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ER -

Aphid feeding induces the relaxation of epigenetic control and the associated regulation of the defense response in Arabidopsis

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