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A remarkable synergistic effect at the transcriptomic level in peach fruits doubly infected by prunus necrotic ringspot virus and peach latent mosaic viroid.

Herranz MC, Niehl A, Rosales M, Fiore N, Zamorano A, Granell A, Pallas V - Virol. J. (2013)

Bottom Line: Our results identify a novel synergistic effect of PLMVd and PNRSV on the transcriptome of peach fruits.We demonstrate that mixed infections, which occur frequently in field conditions, result in a more complex transcriptional response than that observed in single infections.These field studies can help to fully understand plant-pathogen interactions and to develop appropriate crop protection strategies.

View Article: PubMed Central - HTML - PubMed

Affiliation: Instituto de Biología Molecular y Celular de Plantas, Universidad Politécnica de Valencia-Consejo Superior de Investigaciones Científicas, Valencia 46022, Spain. carhergor@gmail.com

ABSTRACT

Background: Microarray profiling is a powerful technique to investigate expression changes of large amounts of genes in response to specific environmental conditions. The majority of the studies investigating gene expression changes in virus-infected plants are limited to interactions between a virus and a model host plant, which usually is Arabidopsis thaliana or Nicotiana benthamiana. In the present work, we performed microarray profiling to explore changes in the expression profile of field-grown Prunus persica (peach) originating from Chile upon single and double infection with Prunus necrotic ringspot virus (PNRSV) and Peach latent mosaic viroid (PLMVd), worldwide natural pathogens of peach trees.

Results: Upon single PLMVd or PNRSV infection, the number of statistically significant gene expression changes was relatively low. By contrast, doubly-infected fruits presented a high number of differentially regulated genes. Among these, down-regulated genes were prevalent. Functional categorization of the gene expression changes upon double PLMVd and PNRSV infection revealed protein modification and degradation as the functional category with the highest percentage of repressed genes whereas induced genes encoded mainly proteins related to phosphate, C-compound and carbohydrate metabolism and also protein modification. Overrepresentation analysis upon double infection with PLMVd and PNRSV revealed specific functional categories over- and underrepresented among the repressed genes indicating active counter-defense mechanisms of the pathogens during infection.

Conclusions: Our results identify a novel synergistic effect of PLMVd and PNRSV on the transcriptome of peach fruits. We demonstrate that mixed infections, which occur frequently in field conditions, result in a more complex transcriptional response than that observed in single infections. Thus, our data demonstrate for the first time that the simultaneous infection of a viroid and a plant virus synergistically affect the host transcriptome in infected peach fruits. These field studies can help to fully understand plant-pathogen interactions and to develop appropriate crop protection strategies.

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Venn diagrams displaying the overlap in differentially regulated genes upon single or double infection with PLMVd or PNRSV. Overlap in differentially induced (a) and repressed (b) gene sets upon infection with PNRSV, PLMVd or both. Numbers shown in the nonintersecting segments represent the number of genes with statistically significant expression changes unique to each infected sample whereas numbers within intersections represent the number of genes with statistically significant expression changes occurring in common upon infection with PLMVd, PNRSV, or double infection.
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Figure 4: Venn diagrams displaying the overlap in differentially regulated genes upon single or double infection with PLMVd or PNRSV. Overlap in differentially induced (a) and repressed (b) gene sets upon infection with PNRSV, PLMVd or both. Numbers shown in the nonintersecting segments represent the number of genes with statistically significant expression changes unique to each infected sample whereas numbers within intersections represent the number of genes with statistically significant expression changes occurring in common upon infection with PLMVd, PNRSV, or double infection.

Mentions: Microarray analysis of the samples was performed using the ChillPeach array containing 4,261 peach unigenes. The number of genes with statistically significant expression changes of at least 1.5 fold relative to healthy plants was 16 and 82 for fruits infected with PLMVd and PNRSV, respectively (Figure 3a). Out of these genes, 13 and 66 have orthologs in A. thaliana. Interestingly, fruits simultaneously infected with both pathogens presented a significantly higher number of differentially regulated genes (685, out of which 602 have orthologs in A. thaliana). The majority of differentially regulated genes exhibited fold changes between 1.5 and 2.0 (Figure 3b) upon infection, however, in contrast to singly, doubly infected fruits displayed a considerable number of genes with fold changes above 2. Comparison of induced and repressed genes revealed similar results as the analysis of the total number of genes (Figure 3c and d). Moreover, this analysis revealed that virus, viroid, and double infection with both pathogens mainly lead to the repression of host gene expression. In detail, approximately 70% of genes differentially regulated upon PNRSV, PLMVd, or double infection, respectively were downregulated, while the remaining 30% were induced (Figure 3c and d). Out of the genes with orthologs in Arabidopsis only a few were induced in PNRSV (4 genes) and PLMVd (9 genes) infected fruits whereas 202 genes exhibited increased expression levels compared to the healthy control in peaches infected with both pathogens (Figure 4a and Additional file 2: Table S1). 400, 62 and 4 genes with orthologs in Arabidopis displayed significantly reduced expression upon infection, in doubly, PNRSV and PLMVd infected samples, respectively (Figure 4b and Additional file 2: Table S1). Interestingly 70% (44 genes) of the PNRSV infected genes were found in PNRSV-PLMVd double infection (meaning 10% for double infected peaches), thus indicating that PNRSV and PNRSV-PLMVd infection deregulate a largely similar set of genes.


A remarkable synergistic effect at the transcriptomic level in peach fruits doubly infected by prunus necrotic ringspot virus and peach latent mosaic viroid.

Herranz MC, Niehl A, Rosales M, Fiore N, Zamorano A, Granell A, Pallas V - Virol. J. (2013)

Venn diagrams displaying the overlap in differentially regulated genes upon single or double infection with PLMVd or PNRSV. Overlap in differentially induced (a) and repressed (b) gene sets upon infection with PNRSV, PLMVd or both. Numbers shown in the nonintersecting segments represent the number of genes with statistically significant expression changes unique to each infected sample whereas numbers within intersections represent the number of genes with statistically significant expression changes occurring in common upon infection with PLMVd, PNRSV, or double infection.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3672095&req=5

Figure 4: Venn diagrams displaying the overlap in differentially regulated genes upon single or double infection with PLMVd or PNRSV. Overlap in differentially induced (a) and repressed (b) gene sets upon infection with PNRSV, PLMVd or both. Numbers shown in the nonintersecting segments represent the number of genes with statistically significant expression changes unique to each infected sample whereas numbers within intersections represent the number of genes with statistically significant expression changes occurring in common upon infection with PLMVd, PNRSV, or double infection.
Mentions: Microarray analysis of the samples was performed using the ChillPeach array containing 4,261 peach unigenes. The number of genes with statistically significant expression changes of at least 1.5 fold relative to healthy plants was 16 and 82 for fruits infected with PLMVd and PNRSV, respectively (Figure 3a). Out of these genes, 13 and 66 have orthologs in A. thaliana. Interestingly, fruits simultaneously infected with both pathogens presented a significantly higher number of differentially regulated genes (685, out of which 602 have orthologs in A. thaliana). The majority of differentially regulated genes exhibited fold changes between 1.5 and 2.0 (Figure 3b) upon infection, however, in contrast to singly, doubly infected fruits displayed a considerable number of genes with fold changes above 2. Comparison of induced and repressed genes revealed similar results as the analysis of the total number of genes (Figure 3c and d). Moreover, this analysis revealed that virus, viroid, and double infection with both pathogens mainly lead to the repression of host gene expression. In detail, approximately 70% of genes differentially regulated upon PNRSV, PLMVd, or double infection, respectively were downregulated, while the remaining 30% were induced (Figure 3c and d). Out of the genes with orthologs in Arabidopsis only a few were induced in PNRSV (4 genes) and PLMVd (9 genes) infected fruits whereas 202 genes exhibited increased expression levels compared to the healthy control in peaches infected with both pathogens (Figure 4a and Additional file 2: Table S1). 400, 62 and 4 genes with orthologs in Arabidopis displayed significantly reduced expression upon infection, in doubly, PNRSV and PLMVd infected samples, respectively (Figure 4b and Additional file 2: Table S1). Interestingly 70% (44 genes) of the PNRSV infected genes were found in PNRSV-PLMVd double infection (meaning 10% for double infected peaches), thus indicating that PNRSV and PNRSV-PLMVd infection deregulate a largely similar set of genes.

Bottom Line: Our results identify a novel synergistic effect of PLMVd and PNRSV on the transcriptome of peach fruits.We demonstrate that mixed infections, which occur frequently in field conditions, result in a more complex transcriptional response than that observed in single infections.These field studies can help to fully understand plant-pathogen interactions and to develop appropriate crop protection strategies.

View Article: PubMed Central - HTML - PubMed

Affiliation: Instituto de Biología Molecular y Celular de Plantas, Universidad Politécnica de Valencia-Consejo Superior de Investigaciones Científicas, Valencia 46022, Spain. carhergor@gmail.com

ABSTRACT

Background: Microarray profiling is a powerful technique to investigate expression changes of large amounts of genes in response to specific environmental conditions. The majority of the studies investigating gene expression changes in virus-infected plants are limited to interactions between a virus and a model host plant, which usually is Arabidopsis thaliana or Nicotiana benthamiana. In the present work, we performed microarray profiling to explore changes in the expression profile of field-grown Prunus persica (peach) originating from Chile upon single and double infection with Prunus necrotic ringspot virus (PNRSV) and Peach latent mosaic viroid (PLMVd), worldwide natural pathogens of peach trees.

Results: Upon single PLMVd or PNRSV infection, the number of statistically significant gene expression changes was relatively low. By contrast, doubly-infected fruits presented a high number of differentially regulated genes. Among these, down-regulated genes were prevalent. Functional categorization of the gene expression changes upon double PLMVd and PNRSV infection revealed protein modification and degradation as the functional category with the highest percentage of repressed genes whereas induced genes encoded mainly proteins related to phosphate, C-compound and carbohydrate metabolism and also protein modification. Overrepresentation analysis upon double infection with PLMVd and PNRSV revealed specific functional categories over- and underrepresented among the repressed genes indicating active counter-defense mechanisms of the pathogens during infection.

Conclusions: Our results identify a novel synergistic effect of PLMVd and PNRSV on the transcriptome of peach fruits. We demonstrate that mixed infections, which occur frequently in field conditions, result in a more complex transcriptional response than that observed in single infections. Thus, our data demonstrate for the first time that the simultaneous infection of a viroid and a plant virus synergistically affect the host transcriptome in infected peach fruits. These field studies can help to fully understand plant-pathogen interactions and to develop appropriate crop protection strategies.

Show MeSH
Related in: MedlinePlus