Paper · 2012 · BMC Plant Biology

Expression of geminiviral AC2 RNA silencing suppressor changes sugar and jasmonate responsive gene expression in transgenic tobacco plants

Arto J Soitamo; Balaji Jada; Kirsi Lehto

12
claims
24
verbatim quotes
45
citations
4
research areas
✓
Open access

Abstract

BACKGROUND: RNA-silencing is a conserved gene regulation and surveillance machinery, which in plants, is also used as major defence mechanism against viruses. Various virus-specific dsRNA structures are recognized by the silencing machinery leading to degradation of the viral RNAs or, as in case of begomoviruses, to methylation of their DNA genomes. Viruses produce specific RNA silencing suppressor (RSS) proteins to prevent these host defence mechanisms, and as these interfere with the silencing machinery they also disturb the endogenous silencing reactions. In this paper, we describe how expression of AC2 RSS, derived from African cassava mosaic geminivirus changes transcription profile in tobacco (Nicotiana tabacum) leaves and in flowers. RESULTS: Expression of AC2 RSS in transgenic tobacco plants induced clear phenotypic changes both in leaves and in flowers. Transcriptomes of these plants were strongly altered, with total of 1118 and 251 differentially expressed genes in leaves and flowers, respectively. The three most up-regulated transcript groups were related to stress, cell wall modifications and signalling, whereas the three most down-regulated groups were related to translation, photosynthesis and transcription. It appears that many of the gene expression alterations appeared to be related to enhanced biosynthesis of jasmonate and ethylene, and consequent enhancement of the genes and pathways that are regulated by these hormones, or to the retrograde signalling caused by the reduced photosynthetic activity and sugar metabolism. Comparison of these results to a previous transcriptional profiling of HC-Pro RSS-expressing plants revealed that some of same genes were induced by both RSSs, but their expression levels were typically higher in AC2 than in HC-Pro RSS expressing plants. All in all, a large number of transcript alterations were found to be specific to each of the RSS expressing transgenic plants. CONCLUSIONS: AC2 RSS in transgenic tobacco plants interferes with the silencing machinery. It causes stress and defence reactions for instance via induction of the jasmonate and ethylene biosynthesis, and by consequent gene expression alteration regulated by these hormones. The changed sugar metabolism may cause significant down-regulation of genes encoding ribosomal proteins, thus reducing the general translation level.

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Claims 12

Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

AC2 expression induced clear leaf and flower phenotypic changes in tobacco.

Organ / stage
leavese0
Treatment
Expression of AC2 RSSe0
Gene
AC2 RSSe0
Outcome
clear phenotypic changese0

Not reportedComparatorDirection

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Nicotiana tabacum
Nicotiana tabacum · TaxonJom / Joachim Müllerchen · CC BY 2.5 · Wikimedia Commons ↗

Verbatim

e0

“Expression of AC2 RSS in transgenic tobacco plants induced clear phenotypic changes both in leaves and in flowers.”

✓ located verbatim in the source · abstract, characters 760–874 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

AC2-expressing tobacco leaves had 1118 differentially expressed genes.

Organ / stage
leavese0
Treatment
Expression of AC2 RSSe1
Outcome
differentially expressed genese0
Value
1118e0

Not reportedComparatorDirection

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Nicotiana tabacum
Nicotiana tabacum · TaxonJom / Joachim Müllerchen · CC BY 2.5 · Wikimedia Commons ↗

Verbatim

e0

“Transcriptomes of these plants were strongly altered, with total of 1118 and 251 differentially expressed genes in leaves and flowers, respectively.”

✓ located verbatim in the source · abstract, characters 875–1023 · show in text ↑
t0

“transgenic tobacco plants”

✓ located verbatim in the source · title, characters 113–138 · show in text ↑
e1

“Expression of AC2 RSS in transgenic tobacco plants”

✓ located verbatim in the source · abstract, characters 760–810 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

AC2-expressing tobacco flowers had 251 differentially expressed genes.

Organ / stage
flowerse0
Treatment
Expression of AC2 RSSe1
Outcome
differentially expressed genese0
Value
251e0

Not reportedComparatorDirection

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Nicotiana tabacum
Nicotiana tabacum · TaxonJom / Joachim Müllerchen · CC BY 2.5 · Wikimedia Commons ↗

Verbatim

e0

“Transcriptomes of these plants were strongly altered, with total of 1118 and 251 differentially expressed genes in leaves and flowers, respectively.”

✓ located verbatim in the source · abstract, characters 875–1023 · show in text ↑
t0

“transgenic tobacco plants”

✓ located verbatim in the source · title, characters 113–138 · show in text ↑
e1

“Expression of AC2 RSS in transgenic tobacco plants”

✓ located verbatim in the source · abstract, characters 760–810 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

The most up-regulated tobacco transcript groups related to stress, cell-wall modifications and signalling.

Outcome
transcript groupse0
Direction
up-regulatede0
Qualifier
stress, cell wall modifications and signallinge0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Nicotiana tabacum
Nicotiana tabacum · TaxonJom / Joachim Müllerchen · CC BY 2.5 · Wikimedia Commons ↗

Verbatim

e0

“The three most up-regulated transcript groups were related to stress, cell wall modifications and signalling”

✓ located verbatim in the source · abstract, characters 1024–1132 · show in text ↑
t0

“tobacco”

✓ located verbatim in the source · title, characters 124–131 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

The most down-regulated tobacco transcript groups related to translation, photosynthesis and transcription.

Outcome
groupse0
Direction
down-regulatede0
Qualifier
translation, photosynthesis and transcriptione0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Nicotiana tabacum
Nicotiana tabacum · TaxonJom / Joachim Müllerchen · CC BY 2.5 · Wikimedia Commons ↗

Verbatim

e0

“the three most down-regulated groups were related to translation, photosynthesis and transcription”

✓ located verbatim in the source · abstract, characters 1142–1240 · show in text ↑
t0

“tobacco”

✓ located verbatim in the source · title, characters 124–131 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

Many tobacco expression alterations appeared related to enhanced jasmonate and ethylene biosynthesis and their regulated pathways.

Compound
jasmonate and ethylenee0
Outcome
gene expression alterationse0
Qualifier
enhanced biosynthesise0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Nicotiana tabacum
Nicotiana tabacum · TaxonJom / Joachim Müllerchen · CC BY 2.5 · Wikimedia Commons ↗

Verbatim

e0

“It appears that many of the gene expression alterations appeared to be related to enhanced biosynthesis of jasmonate and ethylene, and consequent enhancement of the genes and pathways that are regulated by these hormones”

✓ located verbatim in the source · abstract, characters 1242–1462 · show in text ↑
t0

“tobacco”

✓ located verbatim in the source · title, characters 124–131 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

Expression alterations also appeared related to retrograde signalling caused by reduced photosynthetic activity and sugar metabolism.

Outcome
gene expression alterationse0
Qualifier
retrograde signalling caused by the reduced photosynthetic activity and sugar metabolisme0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Nicotiana tabacum
Nicotiana tabacum · TaxonJom / Joachim Müllerchen · CC BY 2.5 · Wikimedia Commons ↗

Verbatim

e0

“many of the gene expression alterations appeared to be related to enhanced biosynthesis of jasmonate and ethylene, and consequent enhancement of the genes and pathways that are regulated by these hormones, or to the retrograde signalling caused by the reduced photosynthetic activity and sugar metabolism”

✓ located verbatim in the source · abstract, characters 1258–1562 · show in text ↑
t0

“tobacco”

✓ located verbatim in the source · title, characters 124–131 · show in text ↑
Associationobservedoriginal resultmeasured

Claim · model-written summary

Some tobacco genes were induced by both AC2 and HC-Pro, typically at higher expression levels with AC2.

Gene
AC2e0
Outcome
expression levelse0
Direction
highere0
Qualifier
typicallye0
Comparator
HC-Proe0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Nicotiana tabacum
Nicotiana tabacum · TaxonJom / Joachim Müllerchen · CC BY 2.5 · Wikimedia Commons ↗

Verbatim

e0

“some of same genes were induced by both RSSs, but their expression levels were typically higher in AC2 than in HC-Pro RSS expressing plants”

✓ located verbatim in the source · abstract, characters 1678–1817 · show in text ↑
t0

“tobacco”

✓ located verbatim in the source · title, characters 124–131 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Many transcript alterations were specific to each RSS-expressing tobacco plant type.

Outcome
transcript alterationse0
Qualifier
specific to each of the RSS expressing transgenic plantse0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Nicotiana tabacum
Nicotiana tabacum · TaxonJom / Joachim Müllerchen · CC BY 2.5 · Wikimedia Commons ↗

Verbatim

e0

“a large number of transcript alterations were found to be specific to each of the RSS expressing transgenic plants”

✓ located verbatim in the source · abstract, characters 1831–1945 · show in text ↑
t0

“tobacco”

✓ located verbatim in the source · title, characters 124–131 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

AC2 interfered with tobacco silencing machinery.

Gene
AC2 RSSe0
Outcome
interferes with the silencing machinerye0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Nicotiana tabacum
Nicotiana tabacum · TaxonJom / Joachim Müllerchen · CC BY 2.5 · Wikimedia Commons ↗

Verbatim

e0

“AC2 RSS in transgenic tobacco plants interferes with the silencing machinery.”

✓ located verbatim in the source · abstract, characters 1960–2037 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

AC2 caused stress and defence reactions via jasmonate and ethylene biosynthesis and hormone-regulated expression changes.

Compound
jasmonate and ethylenee0
Outcome
stress and defence reactionse0
Qualifier
via induction of the jasmonate and ethylene biosynthesise0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Nicotiana tabacum
Nicotiana tabacum · TaxonJom / Joachim Müllerchen · CC BY 2.5 · Wikimedia Commons ↗

Verbatim

e0

“It causes stress and defence reactions for instance via induction of the jasmonate and ethylene biosynthesis, and by consequent gene expression alteration regulated by these hormones.”

✓ located verbatim in the source · abstract, characters 2038–2221 · show in text ↑
t0

“tobacco”

✓ located verbatim in the source · title, characters 124–131 · show in text ↑
Mechanismhypothesisoriginal resultnegativemeasured

Claim · model-written summary

Changed sugar metabolism may significantly down-regulate ribosomal-protein genes and reduce general translation in tobacco.

Gene
ribosomal proteinse0
Outcome
down-regulation of genes encoding ribosomal proteinse0
Qualifier
changed sugar metabolism may causee0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Nicotiana tabacum
Nicotiana tabacum · TaxonJom / Joachim Müllerchen · CC BY 2.5 · Wikimedia Commons ↗

Verbatim

e0

“The changed sugar metabolism may cause significant down-regulation of genes encoding ribosomal proteins, thus reducing the general translation level.”

✓ located verbatim in the source · abstract, characters 2222–2371 · show in text ↑
t0

“tobacco”

✓ located verbatim in the source · title, characters 124–131 · show in text ↑