Global transcriptome analyses reveal that infection with chrysanthemum stunt viroid (CSVd) affects gene expression profile of chrysanthemum plants, but the genes involved in plant hormone metabolism and signaling may not be silencing target of CSVd-siRNAs

Hiroki Takino, Sakihito Kitajima, Saki Hirano, Mariko Oka, Takakazu Matsuura, Yoko Ikeda, Mikiko Kojima, Yumiko Takebayashi, Hitoshi Sakakibara, Masanobu Mino

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

Chrysanthemum stunt viroid (CSVd) is a pathogen that induces stunted plant growth as a typical disease symptom in infected chrysanthemum plants. Because of its simple RNA genomic structure, the mechanism of how CSVd provokes pathogenicity in host plants remains elusive. Since small RNAs generated from CSVd genomic RNA accumulated in infected plants (Tsuro et al., 2013), it has been suggested that forced gene silencing against intrinsic genes by CSVd-small interfering (si)RNAs is involved in its pathogenicity. In this study, we revealed that CSVd infection induced global fluctuation of gene expression in plants. Hypothetical CSVd-siRNAs (22 nucleotides long) from (+) and (−) strands of the CSVd RNA genome were surveyed to examine if they could target the down-regulated gene sequences. Six genes were identified as target candidates, but the causal link between their functions and disease symptoms was remained unclear. In contrast, the expression levels of genes involved in the biosynthesis of gibberellic acid (GA) and cytokinin (CK), indole-3-acetic acid (IAA) transport and cell wall growth in infected plants were down-regulated, but mRNAs of those genes were not found as possible target sequences of CSVd-siRNAs. On the other hand, endogenous levels of GA, CK, IAA, and abscisic acid and the rate of IAA movement in the stem were not different between healthy and infected plants. Growth promotion of infected plants by GA treatment was poorer than that of healthy plants, suggesting that CSVd infection suppressed the GA-signaling pathway. This was further supported by the findings of a reduced response of GA-regulated genes to GA treatment and up-regulation of the DELLA-protein gene, a negative regulator of GA-signaling, in infected plants. Thus, the down-regulation of GA responsiveness and inhibition of cell wall expansion are major causes of the stunted growth of CSVd-infected chrysanthemum plants.

Original languageEnglish
Article number100181
JournalPlant Gene
Volume18
DOIs
Publication statusPublished - Jun 1 2019

Fingerprint

Chrysanthemum stunt viroid
Viroids
Chrysanthemum
hormone metabolism
Plant Genes
Plant Growth Regulators
Gene Expression Profiling
Transcriptome
Metabolism
Gene expression
transcriptome
plant hormones
gibberellic acid
Genes
gene expression
Infection
infection
genes
RNA
Cytokinins

Keywords

  • Chyrsanthemum stunt viroid (CSVd)
  • GA signaling
  • Plant hormones
  • RNA-seq analysis
  • Small interfering RNA

ASJC Scopus subject areas

  • Biotechnology
  • Biochemistry
  • Genetics
  • Plant Science

Cite this

Global transcriptome analyses reveal that infection with chrysanthemum stunt viroid (CSVd) affects gene expression profile of chrysanthemum plants, but the genes involved in plant hormone metabolism and signaling may not be silencing target of CSVd-siRNAs. / Takino, Hiroki; Kitajima, Sakihito; Hirano, Saki; Oka, Mariko; Matsuura, Takakazu; Ikeda, Yoko; Kojima, Mikiko; Takebayashi, Yumiko; Sakakibara, Hitoshi; Mino, Masanobu.

In: Plant Gene, Vol. 18, 100181, 01.06.2019.

Research output: Contribution to journalArticle

Takino, Hiroki ; Kitajima, Sakihito ; Hirano, Saki ; Oka, Mariko ; Matsuura, Takakazu ; Ikeda, Yoko ; Kojima, Mikiko ; Takebayashi, Yumiko ; Sakakibara, Hitoshi ; Mino, Masanobu. / Global transcriptome analyses reveal that infection with chrysanthemum stunt viroid (CSVd) affects gene expression profile of chrysanthemum plants, but the genes involved in plant hormone metabolism and signaling may not be silencing target of CSVd-siRNAs. In: Plant Gene. 2019 ; Vol. 18.
@article{8272126a82a341d795e23c44fde813b4,
title = "Global transcriptome analyses reveal that infection with chrysanthemum stunt viroid (CSVd) affects gene expression profile of chrysanthemum plants, but the genes involved in plant hormone metabolism and signaling may not be silencing target of CSVd-siRNAs",
abstract = "Chrysanthemum stunt viroid (CSVd) is a pathogen that induces stunted plant growth as a typical disease symptom in infected chrysanthemum plants. Because of its simple RNA genomic structure, the mechanism of how CSVd provokes pathogenicity in host plants remains elusive. Since small RNAs generated from CSVd genomic RNA accumulated in infected plants (Tsuro et al., 2013), it has been suggested that forced gene silencing against intrinsic genes by CSVd-small interfering (si)RNAs is involved in its pathogenicity. In this study, we revealed that CSVd infection induced global fluctuation of gene expression in plants. Hypothetical CSVd-siRNAs (22 nucleotides long) from (+) and (−) strands of the CSVd RNA genome were surveyed to examine if they could target the down-regulated gene sequences. Six genes were identified as target candidates, but the causal link between their functions and disease symptoms was remained unclear. In contrast, the expression levels of genes involved in the biosynthesis of gibberellic acid (GA) and cytokinin (CK), indole-3-acetic acid (IAA) transport and cell wall growth in infected plants were down-regulated, but mRNAs of those genes were not found as possible target sequences of CSVd-siRNAs. On the other hand, endogenous levels of GA, CK, IAA, and abscisic acid and the rate of IAA movement in the stem were not different between healthy and infected plants. Growth promotion of infected plants by GA treatment was poorer than that of healthy plants, suggesting that CSVd infection suppressed the GA-signaling pathway. This was further supported by the findings of a reduced response of GA-regulated genes to GA treatment and up-regulation of the DELLA-protein gene, a negative regulator of GA-signaling, in infected plants. Thus, the down-regulation of GA responsiveness and inhibition of cell wall expansion are major causes of the stunted growth of CSVd-infected chrysanthemum plants.",
keywords = "Chyrsanthemum stunt viroid (CSVd), GA signaling, Plant hormones, RNA-seq analysis, Small interfering RNA",
author = "Hiroki Takino and Sakihito Kitajima and Saki Hirano and Mariko Oka and Takakazu Matsuura and Yoko Ikeda and Mikiko Kojima and Yumiko Takebayashi and Hitoshi Sakakibara and Masanobu Mino",
year = "2019",
month = "6",
day = "1",
doi = "10.1016/j.plgene.2019.100181",
language = "English",
volume = "18",
journal = "Plant Gene",
issn = "2352-4073",
publisher = "Elsevier BV",

}

TY - JOUR

T1 - Global transcriptome analyses reveal that infection with chrysanthemum stunt viroid (CSVd) affects gene expression profile of chrysanthemum plants, but the genes involved in plant hormone metabolism and signaling may not be silencing target of CSVd-siRNAs

AU - Takino, Hiroki

AU - Kitajima, Sakihito

AU - Hirano, Saki

AU - Oka, Mariko

AU - Matsuura, Takakazu

AU - Ikeda, Yoko

AU - Kojima, Mikiko

AU - Takebayashi, Yumiko

AU - Sakakibara, Hitoshi

AU - Mino, Masanobu

PY - 2019/6/1

Y1 - 2019/6/1

N2 - Chrysanthemum stunt viroid (CSVd) is a pathogen that induces stunted plant growth as a typical disease symptom in infected chrysanthemum plants. Because of its simple RNA genomic structure, the mechanism of how CSVd provokes pathogenicity in host plants remains elusive. Since small RNAs generated from CSVd genomic RNA accumulated in infected plants (Tsuro et al., 2013), it has been suggested that forced gene silencing against intrinsic genes by CSVd-small interfering (si)RNAs is involved in its pathogenicity. In this study, we revealed that CSVd infection induced global fluctuation of gene expression in plants. Hypothetical CSVd-siRNAs (22 nucleotides long) from (+) and (−) strands of the CSVd RNA genome were surveyed to examine if they could target the down-regulated gene sequences. Six genes were identified as target candidates, but the causal link between their functions and disease symptoms was remained unclear. In contrast, the expression levels of genes involved in the biosynthesis of gibberellic acid (GA) and cytokinin (CK), indole-3-acetic acid (IAA) transport and cell wall growth in infected plants were down-regulated, but mRNAs of those genes were not found as possible target sequences of CSVd-siRNAs. On the other hand, endogenous levels of GA, CK, IAA, and abscisic acid and the rate of IAA movement in the stem were not different between healthy and infected plants. Growth promotion of infected plants by GA treatment was poorer than that of healthy plants, suggesting that CSVd infection suppressed the GA-signaling pathway. This was further supported by the findings of a reduced response of GA-regulated genes to GA treatment and up-regulation of the DELLA-protein gene, a negative regulator of GA-signaling, in infected plants. Thus, the down-regulation of GA responsiveness and inhibition of cell wall expansion are major causes of the stunted growth of CSVd-infected chrysanthemum plants.

AB - Chrysanthemum stunt viroid (CSVd) is a pathogen that induces stunted plant growth as a typical disease symptom in infected chrysanthemum plants. Because of its simple RNA genomic structure, the mechanism of how CSVd provokes pathogenicity in host plants remains elusive. Since small RNAs generated from CSVd genomic RNA accumulated in infected plants (Tsuro et al., 2013), it has been suggested that forced gene silencing against intrinsic genes by CSVd-small interfering (si)RNAs is involved in its pathogenicity. In this study, we revealed that CSVd infection induced global fluctuation of gene expression in plants. Hypothetical CSVd-siRNAs (22 nucleotides long) from (+) and (−) strands of the CSVd RNA genome were surveyed to examine if they could target the down-regulated gene sequences. Six genes were identified as target candidates, but the causal link between their functions and disease symptoms was remained unclear. In contrast, the expression levels of genes involved in the biosynthesis of gibberellic acid (GA) and cytokinin (CK), indole-3-acetic acid (IAA) transport and cell wall growth in infected plants were down-regulated, but mRNAs of those genes were not found as possible target sequences of CSVd-siRNAs. On the other hand, endogenous levels of GA, CK, IAA, and abscisic acid and the rate of IAA movement in the stem were not different between healthy and infected plants. Growth promotion of infected plants by GA treatment was poorer than that of healthy plants, suggesting that CSVd infection suppressed the GA-signaling pathway. This was further supported by the findings of a reduced response of GA-regulated genes to GA treatment and up-regulation of the DELLA-protein gene, a negative regulator of GA-signaling, in infected plants. Thus, the down-regulation of GA responsiveness and inhibition of cell wall expansion are major causes of the stunted growth of CSVd-infected chrysanthemum plants.

KW - Chyrsanthemum stunt viroid (CSVd)

KW - GA signaling

KW - Plant hormones

KW - RNA-seq analysis

KW - Small interfering RNA

UR - http://www.scopus.com/inward/record.url?scp=85064541258&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85064541258&partnerID=8YFLogxK

U2 - 10.1016/j.plgene.2019.100181

DO - 10.1016/j.plgene.2019.100181

M3 - Article

AN - SCOPUS:85064541258

VL - 18

JO - Plant Gene

JF - Plant Gene

SN - 2352-4073

M1 - 100181

ER -