Overexpression of the PAP1 transcription factor reveals a complex regulation of flavonoid and phenylpropanoid metabolism in nicotiana tabacum plants attacked by Spodoptera litura

Tomoko Mitsunami, Masahiro Nishihara, Ivan Galis, Kabir Md Alamgir, Yuko Hojo, Kohei Fujita, Nobuhiro Sasaki, Keichiro Nemoto, Tatsuya Sawasaki, Gen Ichiro Arimura

Research output: Contribution to journalArticle

15 Citations (Scopus)

Abstract

Anthocyanin pigments and associated flavonoids have demonstrated antioxidant properties and benefits for human health. Consequently, current plant bioengineers have focused on how to modify flavonoid metabolism in plants. Most of that research, however, does not consider the role of natural biotic stresses (e.g., herbivore attack). To understand the influence of herbivore attack on the metabolic engineering of flavonoids, we examined tobacco plants overexpressing the Arabidopsis PAP1 gene (encoding an MYB transcription factor), which accumulated anthocyanin pigments and other flavonoids/ phenylpropanoids. In comparison to wild-type and control plants, transgenic plants exhibited greater resistance to Spodoptera Iitura. Moreover, herbivory suppressed the PAP1 -induced increase of transcripts of flavonoid/phenylpropanoid biosynthetic genes (e.g., F3H) and the subsequent accumulation of these genes' metabolites, despite the unaltered PAP1 mRNA levels after herbivory. The instances of down-regulation were independent of the signaling pathways mediated by defense-related jasmonates but were relevant to the levels of PAP1-induced and herbivory-suppressed transcription factors, Anla and Ani b. Although initially F3H transcripts were suppressed by herbivory, after the 5. Iitura feeding was interrupted, F3H transcripts increased. We hypothesize that in transgenic plants responding to herbivory, there is a complex mechanism regulating enriched flavonoid/phenylpropanoid compounds, via biotic stress signals.

Original languageEnglish
Article numbere108849
JournalPLoS One
Volume9
Issue number9
DOIs
Publication statusPublished - Sep 30 2014

Fingerprint

Spodoptera
Spodoptera litura
Herbivory
phenylpropanoids
Flavonoids
Metabolism
Nicotiana tabacum
Tobacco
Transcription Factors
herbivores
flavonoids
transcription factors
metabolism
Anthocyanins
Genetically Modified Plants
Pigments
biotic stress
Genes
anthocyanins
transgenic plants

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Overexpression of the PAP1 transcription factor reveals a complex regulation of flavonoid and phenylpropanoid metabolism in nicotiana tabacum plants attacked by Spodoptera litura. / Mitsunami, Tomoko; Nishihara, Masahiro; Galis, Ivan; Alamgir, Kabir Md; Hojo, Yuko; Fujita, Kohei; Sasaki, Nobuhiro; Nemoto, Keichiro; Sawasaki, Tatsuya; Arimura, Gen Ichiro.

In: PLoS One, Vol. 9, No. 9, e108849, 30.09.2014.

Research output: Contribution to journalArticle

Mitsunami, Tomoko ; Nishihara, Masahiro ; Galis, Ivan ; Alamgir, Kabir Md ; Hojo, Yuko ; Fujita, Kohei ; Sasaki, Nobuhiro ; Nemoto, Keichiro ; Sawasaki, Tatsuya ; Arimura, Gen Ichiro. / Overexpression of the PAP1 transcription factor reveals a complex regulation of flavonoid and phenylpropanoid metabolism in nicotiana tabacum plants attacked by Spodoptera litura. In: PLoS One. 2014 ; Vol. 9, No. 9.
@article{e8bcf68e314248c69f64b7a35e8fd949,
title = "Overexpression of the PAP1 transcription factor reveals a complex regulation of flavonoid and phenylpropanoid metabolism in nicotiana tabacum plants attacked by Spodoptera litura",
abstract = "Anthocyanin pigments and associated flavonoids have demonstrated antioxidant properties and benefits for human health. Consequently, current plant bioengineers have focused on how to modify flavonoid metabolism in plants. Most of that research, however, does not consider the role of natural biotic stresses (e.g., herbivore attack). To understand the influence of herbivore attack on the metabolic engineering of flavonoids, we examined tobacco plants overexpressing the Arabidopsis PAP1 gene (encoding an MYB transcription factor), which accumulated anthocyanin pigments and other flavonoids/ phenylpropanoids. In comparison to wild-type and control plants, transgenic plants exhibited greater resistance to Spodoptera Iitura. Moreover, herbivory suppressed the PAP1 -induced increase of transcripts of flavonoid/phenylpropanoid biosynthetic genes (e.g., F3H) and the subsequent accumulation of these genes' metabolites, despite the unaltered PAP1 mRNA levels after herbivory. The instances of down-regulation were independent of the signaling pathways mediated by defense-related jasmonates but were relevant to the levels of PAP1-induced and herbivory-suppressed transcription factors, Anla and Ani b. Although initially F3H transcripts were suppressed by herbivory, after the 5. Iitura feeding was interrupted, F3H transcripts increased. We hypothesize that in transgenic plants responding to herbivory, there is a complex mechanism regulating enriched flavonoid/phenylpropanoid compounds, via biotic stress signals.",
author = "Tomoko Mitsunami and Masahiro Nishihara and Ivan Galis and Alamgir, {Kabir Md} and Yuko Hojo and Kohei Fujita and Nobuhiro Sasaki and Keichiro Nemoto and Tatsuya Sawasaki and Arimura, {Gen Ichiro}",
year = "2014",
month = "9",
day = "30",
doi = "10.1371/journal.pone.0108849",
language = "English",
volume = "9",
journal = "PLoS One",
issn = "1932-6203",
publisher = "Public Library of Science",
number = "9",

}

TY - JOUR

T1 - Overexpression of the PAP1 transcription factor reveals a complex regulation of flavonoid and phenylpropanoid metabolism in nicotiana tabacum plants attacked by Spodoptera litura

AU - Mitsunami, Tomoko

AU - Nishihara, Masahiro

AU - Galis, Ivan

AU - Alamgir, Kabir Md

AU - Hojo, Yuko

AU - Fujita, Kohei

AU - Sasaki, Nobuhiro

AU - Nemoto, Keichiro

AU - Sawasaki, Tatsuya

AU - Arimura, Gen Ichiro

PY - 2014/9/30

Y1 - 2014/9/30

N2 - Anthocyanin pigments and associated flavonoids have demonstrated antioxidant properties and benefits for human health. Consequently, current plant bioengineers have focused on how to modify flavonoid metabolism in plants. Most of that research, however, does not consider the role of natural biotic stresses (e.g., herbivore attack). To understand the influence of herbivore attack on the metabolic engineering of flavonoids, we examined tobacco plants overexpressing the Arabidopsis PAP1 gene (encoding an MYB transcription factor), which accumulated anthocyanin pigments and other flavonoids/ phenylpropanoids. In comparison to wild-type and control plants, transgenic plants exhibited greater resistance to Spodoptera Iitura. Moreover, herbivory suppressed the PAP1 -induced increase of transcripts of flavonoid/phenylpropanoid biosynthetic genes (e.g., F3H) and the subsequent accumulation of these genes' metabolites, despite the unaltered PAP1 mRNA levels after herbivory. The instances of down-regulation were independent of the signaling pathways mediated by defense-related jasmonates but were relevant to the levels of PAP1-induced and herbivory-suppressed transcription factors, Anla and Ani b. Although initially F3H transcripts were suppressed by herbivory, after the 5. Iitura feeding was interrupted, F3H transcripts increased. We hypothesize that in transgenic plants responding to herbivory, there is a complex mechanism regulating enriched flavonoid/phenylpropanoid compounds, via biotic stress signals.

AB - Anthocyanin pigments and associated flavonoids have demonstrated antioxidant properties and benefits for human health. Consequently, current plant bioengineers have focused on how to modify flavonoid metabolism in plants. Most of that research, however, does not consider the role of natural biotic stresses (e.g., herbivore attack). To understand the influence of herbivore attack on the metabolic engineering of flavonoids, we examined tobacco plants overexpressing the Arabidopsis PAP1 gene (encoding an MYB transcription factor), which accumulated anthocyanin pigments and other flavonoids/ phenylpropanoids. In comparison to wild-type and control plants, transgenic plants exhibited greater resistance to Spodoptera Iitura. Moreover, herbivory suppressed the PAP1 -induced increase of transcripts of flavonoid/phenylpropanoid biosynthetic genes (e.g., F3H) and the subsequent accumulation of these genes' metabolites, despite the unaltered PAP1 mRNA levels after herbivory. The instances of down-regulation were independent of the signaling pathways mediated by defense-related jasmonates but were relevant to the levels of PAP1-induced and herbivory-suppressed transcription factors, Anla and Ani b. Although initially F3H transcripts were suppressed by herbivory, after the 5. Iitura feeding was interrupted, F3H transcripts increased. We hypothesize that in transgenic plants responding to herbivory, there is a complex mechanism regulating enriched flavonoid/phenylpropanoid compounds, via biotic stress signals.

UR - http://www.scopus.com/inward/record.url?scp=84907487411&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84907487411&partnerID=8YFLogxK

U2 - 10.1371/journal.pone.0108849

DO - 10.1371/journal.pone.0108849

M3 - Article

C2 - 25268129

AN - SCOPUS:84907487411

VL - 9

JO - PLoS One

JF - PLoS One

SN - 1932-6203

IS - 9

M1 - e108849

ER -