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. 2018 Feb 28;285(1873):20172560.
doi: 10.1098/rspb.2017.2560.

Expression Profiling Across Wild and Cultivated Tomatoes Supports the Relevance of Early miR482/2118 Suppression for Phytophthora Resistance

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Free PMC article

Expression Profiling Across Wild and Cultivated Tomatoes Supports the Relevance of Early miR482/2118 Suppression for Phytophthora Resistance

Sophie de Vries et al. Proc Biol Sci. .
Free PMC article

Abstract

Plants possess a battery of specific pathogen resistance (R-)genes. Precise R-gene regulation is important in the presence and absence of a pathogen. Recently, a microRNA family, miR482/2118, was shown to regulate the expression of a major class of R-genes, nucleotide-binding site leucine-rich repeats (NBS-LRRs). Furthermore, RNA silencing suppressor proteins, secreted by pathogens, prevent the accumulation of miR482/2118, leading to an upregulation of R-genes. Despite this transcriptional release of R-genes, RNA silencing suppressors positively contribute to the virulence of some pathogens. To investigate this paradox, we analysed how the regulation of NBS-LRRs by miR482/2118 has been shaped by the coevolution between Phytophthora infestans and cultivated and wild tomatoes. We used degradome analyses and qRT-PCR to evaluate and quantify the co-expression of miR482/2118 and their NBS-LRR targets. Our data show that miR482/2118-mediated targeting contributes to the regulation of NBS-LRRs in Solanum lycopersicum. Based on miR482/2118 expression profiling in two additional tomato species-with different coevolutionary histories with P. infestans-we hypothesize that pathogen-mediated RNA silencing suppression is most effective in the interaction between S. lycopersicum and P. infestans Furthermore, an upregulation of miR482/2118 early in the infection may increase susceptibility to P. infestans.

Keywords: Solanum; evolution; miRNA signalling; plant immunity.

Conflict of interest statement

We have no competing interests.

Figures

Figure 1.
Figure 1.
Targeting of NBS-LRRs by miR482/2118 family members in S. lycopersicum. In vitro confirmation of NBS-LRR targeting by SlmiR482/2118 using 5′RLM-RACE for Solyc02g036270.2.1 targeted by SlmiR482a (a), Solyc08g075630.2.1 targeted by SlmiR482f (b) and Solyc08g076000.2.1 targeted by SlmiR482f (c). A schematic of the target gene (blue) is on the left. The predicted binding site (P-loop, orange) and its sequence is shown below. The arrows indicate the validated degradation sites. The number of clones supporting the site and the total number of clones sequenced are given above the arrows. Upper numbers indicate clones from the mock controls and lower numbers indicate those from infections. The corresponding PCR products of the 5′RLM-RACE are shown on the right.
Figure 2.
Figure 2.
Expression of miR482/2118 family members in S. lycopersicum, S. pimpinellifolium and S. arcanum. Relative expression (log2) in infected compared with mock-control plants of S. lycopersicum (a), S. pimpinellifolium (b) and S. arcanum (c) of the seven miR482/2118 family members at 6, 24, 48, 72 and 96 hpi relative to mock control. The bars represent the average relative expression of the mature miRNAs and the error bars indicate the standard error of the mean (SEM). Significant differences of the relative expression of the miRNA in infected versus mock-treated plants at a specific time-point are indicated by *(p-value < 0.05), **(p-value < 0.01), ***(p-value < 0.001) and ns (not significant).
Figure 3.
Figure 3.
Expression and co-regulation of SlmiR482/2118 and their NBS-LRR targets. Relative expression (log2) of potential NBS-LRR targets of miR482/2118 in infected compared with mock-control plants of S. lycopersicum. Bars show the mean expression and error bars indicate the SEM. Statistical differences in relative expression in infected versus mock-treated plants at a specific time-point are indicated by *(p-value < 0.05), **(p-value < 0.01), ***(p-value < 0.001) and ns (not significant). Filled circles below each gene corresponds to the miRNA(s) predicted to target each NBS-LRR. Arrow heads indicate significant up or downregulation of the members of SlmiR482/2118 at a given time-point: upward arrow heads indicate significant upregulation and downward arrow heads indicate significant downregulation of the miRNA. The arrow heads are coloured according to their respective miRNA. Vertical lines between miRNA arrow heads and the relative expression of the NBS-LRR highlight significant negative co-regulation between members of the SlmiR482/2118 family and their targets at a specific time-point.
Figure 4.
Figure 4.
Infection progress in S. arcanum in comparison to S. lycopersicum and S. pimpinellifolium. Necrotic area on the leaflets of S. lycopersicum (a), S. pimpinellifolium (b) and S. arcanum (c) for mock-treated (upper row) and infected (lower row) leaflets. Comparison of the relative necrotic area during P. infestans infection in S. arcanum (blue), S. pimpinellifolium (yellow) and S. lycopersicum (purple) (d). Statistical differences in relative necrotic area for the three species were calculated per time-point and are indicated by different letters above the boxes. The p-value cut-off was 0.05. Comparison of the number of haustoria, developing and mature sporangia of P. infestans after infection of S. arcanum (blue), S. pimpinellifolium (yellow) and S. lycopersicum (purple) (e). All data for S. pimpinellifolium and S. lycopersicum were published previously in de Vries et al. [29].

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References

    1. Whisson SC, et al. 2007. A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450, 115–118. (10.1038/nature06203) - DOI - PubMed
    1. Fabro G, et al. 2011. Multiple candidate effectors from the oomycete pathogen Hyaloperonospora arabidopsidis suppress host plant immunity. PLoS Pathog. 7, e1002348 (10.1371/journal.ppat.1002348) - DOI - PMC - PubMed
    1. Allen RL, Bittner-Eddy PD, Grenville-Briggs LJ, Meitz JC, Rose LE, Beynon JL. 2004. Host–parasite coevolutionary conflict between Arabidopsis and downy mildew. Science 306, 1957–1960. (10.1126/science.1104022) - DOI - PubMed
    1. Krasileva KV, Dahlbeck D, Staskawicz BJ. 2010. Activation of an Arabidopsis resistance protein is specified by the in planta association of its leucine-rich repeat domain with the cognate oomycete effector. Plant Cell 22, 2444–2458. (10.1105/tpc.110.075358) - DOI - PMC - PubMed
    1. Stokes TL, Kunkel BN, Richards EJ. 2002. Epigenetic variation in Arabidopsis disease resistance. Gene. Dev. 16, 171–182. (10.1101/gad.952102) - DOI - PMC - PubMed

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