Primary Metabolism, Phenylpropanoids and Antioxidant Pathways Are Regulated in Potato as a Response to Potato virus Y Infection (original) (raw)
Related papers
BMC Genomics, 2015
Background: Potato virus Y (PVY) is a major pathogen that causes substantial economic losses in worldwide potato production. Different potato cultivars differ in resistance to PVY, from severe susceptibility, through tolerance, to complete resistance. The aim of this study was to better define the mechanisms underlying tolerant responses of potato to infection by the particularly aggressive PVY NTN strain. We focused on the dynamics of the primary metabolism-related processes during PVY NTN infection. Results: A comprehensive analysis of the dynamic changes in primary metabolism was performed, which included whole transcriptome analysis, nontargeted proteomics, and photosynthetic activity measurements in potato cv. Désirée and its transgenic counterpart depleted for accumulation of salicylic acid (NahG-Désirée). Faster multiplication of virus occurred in the NahG-Désirée, with these plants developing strong disease symptoms. We show that while the dynamics of responses at the transcriptional level are extensive and bimodal, this is only partially translated to the protein level, and to the final functional outcome. Photosynthesis-related genes are transiently induced before viral multiplication is detected and it is down-regulated later on. This is reflected as a deficiency of the photosynthetic apparatus at the onset of viral multiplication only. Interestingly, specific and constant up-regulation of some RuBisCO transcripts was detected in Désirée plants, which might be important, as these proteins have been shown to interact with viral proteins. In SA-deficient and more sensitive NahG-Désirée plants, consistent down-regulation of photosynthesis-related genes was detected. A constant reduction in the photochemical efficiency from the onset of viral multiplication was identified; in nontransgenic plants this decrease was only transient. The transient reduction in net photosynthetic rate occurred in both genotypes with the same timing, and coincided with changes in stomatal conductivity. Conclusions: Down-regulation of photosynthesis-related gene expression and decreased photosynthetic activity is in line with other studies that have reported the effects of biotic stress on photosynthesis. Here, we additionally detected induction of light-reaction components in the early stages of PVY NTN infection of tolerant interaction. As some of these components have already been shown to interact with viral proteins, their overproduction might contribute to the absence of symptoms in cv. Désirée.
Proteomes
Plant diseases caused by viral infection are affecting all major crops. Being an obligate intracellular organisms, chemical control of these pathogens is so far not applied in the field except to control the insect vectors of the viruses. Understanding of molecular responses of plant immunity is therefore economically important, guiding the enforcement of crop resistance. To disentangle complex regulatory mechanisms of the plant immune responses, understanding system as a whole is a must. However, integrating data from different molecular analysis (transcriptomics, proteomics, metabolomics, smallRNA regulation etc.) is not straightforward. We evaluated the response of potato (Solanum tuberosum L.) following the infection with potato virus Y (PVY). The response has been analyzed on two molecular levels, with microarray transcriptome analysis and mass spectroscopy-based proteomics. Within this report, we performed detailed analysis of the results on both levels and compared two different approaches for analysis of proteomic data (spectral count versus MaxQuant). To link the data on different molecular levels, each protein was mapped to the corresponding potato transcript according to StNIB paralogue grouping. Only 33% of the proteins mapped to microarray probes in a one-to-one relation and additionally many showed discordance in detected levels of proteins with corresponding transcripts. We discussed functional importance of true biological differences between both levels and showed that the reason for the discordance between transcript and protein abundance lies partly in complexity and structure of biological regulation of proteome and transcriptome and partly in technical issues contributing to it.
Potato virus Y induced changes in the gene expression of potato ( Solanum tuberosum L
Physiological and Molecular Plant Pathology, 2005
The tuber necrotic strain of Potato virus Y (PVY NTN ) causes potato tuber necrotic ringspot disease in sensitive potato cultivars. Gene expression in the disease response of the susceptible potato (Solanum tuberosum L.) cultivar Igor was investigated at different times after infection, using subtractive hybridization, cDNA microarrays and real-time PCR. The most pronounced change in the expression pattern of functionally diverse groups of genes was detected in systemically infected leaves 14 days after inoculation, and in leaves of plants grown from infected tubers. The expression of several stress-related genes during the infection process, including those for heat shock proteins, catalase 1, b-1,3-glucanase, wound inducing gene, and genes involved in photosynthesis, suggests their role in the susceptible potato-PVY NTN interaction. q
Plant Pathology, 2010
Differences in the early responses of two potato cultivars, Igor and Nadine, to two isolates of Potato virus Y (PVY), the aggressive PVY NTN and the mild PVY N , were monitored. Microarray and quantitative real-time PCR analyses were carried out to identify differentially expressed genes after inoculation with each virus isolate. Additionally, symptom severity and development was observed and the amount of virus isolate accumulated in systemically infected leaves was evaluated, where a significantly higher amount of PVY NTN was detected. Microarray analysis revealed 572, 1288 and 1706 differentially expressed genes at 0AE5, 12 and 48 h post-inoculation, respectively in cv. Igor, with a similar pattern observed in cv. Nadine. Microarray and quantitative real-time PCR results implied an earlier accumulation of sugars and lower photosynthesis in leaves inoculated with the aggressive isolate than in leaves inoculated with the mild isolate. The PVY NTN isolate did not activate early differential expression of the Fe-superoxide dismutase and pectin methylesterase inhibitor (PMEI) genes, indicating a delay in plant response relative to that following PVY N inoculation. Differences in the expression of the b-glucanase-I gene were also observed in early plant responses to inoculation with each virus isolate.
Regulation of carbohydrate partitioning during the interaction of potato virus Y with tobacco
Molecular Plant Pathology, 2000
To test whether carbohydrates may play a signalling function during plant pathogenesis, we investigated the interaction between tobacco and potato virus Y (PVY N ). Four days after PVY N infection, leaves started to accumulate soluble sugars and leaf photosynthesis decreased. The accumulation of soluble sugars was accompanied by an induction of cell wall invertase and a gradual decrease in the sucrose-to-hexose ratio. In parallel to changes in carbohydrate metabolism and photosynthesis, transcripts encoding PR-proteins accumulated. Based on this coincidence, it was hypothesized that elevated hexose levels may enhance the expression of defence-related functions and might possibly explain the phenomenon of high sugar resistance in plants. This notion has been supported by the fact that cell wall invertase-expressing transgenic tobacco plants were found to be resistant against PVY N (Herbers et al. , 1996b). To exclude the possibility that salicylate, which accumulates in plants expressing invertase, may be responsible for the observed resistance, these transgenic plants were crossed with salicylate hydroxylase-expressing plants ( nahG ). The progeny were selected for high levels of sugar and low levels of salicylate. Necrotic lesions also developed, typically formed on the leaves of plants expressing invertase, and transcripts encoding PR-Q accumulated in the absence of salicylate. On the other hand, accumulation of PR-1b transcripts decreased, indicating that sugars are not sufficient for PR-1b induction. Infection experiments using these plants as hosts revealed resistance towards PVY N . Thus, the mechanism of apoplastic invertase induced virus resistance is salicylate independent and most likely sugar mediated.
Journal of Experimental Botany, 2014
The purpose of the study was to investigate the role of salicylic acid (SA) signalling in Ny-1-mediated hypersensitive resistance (HR) of potato (Solanum tuberosum L.) to Potato virus Y (PVY). The responses of the Ny-1 allele in the Rywal potato cultivar and transgenic NahG-Rywal potato plants that do not accumulate SA were characterized at the cytological, biochemical, transcriptome, and proteome levels. Analysis of noninoculated and inoculated leaves revealed that HR lesions started to develop from 3 d post inoculation and completely restricted the virus spread. At the cytological level, features of programmed cell death in combination with reactive oxygen species burst were observed. In response to PVY infection, SA was synthesized de novo. The lack of SA accumulation in the NahG plants led to the disease phenotype due to unrestricted viral spreading. Grafting experiments show that SA has a critical role in the inhibition of PVY spreading in parenchymal tissue, but not in vascular veins. The whole transcriptome analysis confirmed the central role of SA in orchestrating Ny-1-mediated responses and showed that the absence of SA leads to significant changes at the transcriptome level, including a delay in activation of expression of genes known to participate in defence responses. Moreover, perturbations in the expression of hormonal signalling genes were detected, shown as a switch from SA to jasmonic acid/ethylene signalling. Viral multiplication in the NahG plants was accompanied by downregulation of photosynthesis genes and activation of multiple energy-producing pathways.
Plant Breeding, 2019
Potato as an essential root crop plays a fundamental role in sustenance security of the world. Viruses are among the most critical pathogens that can decrease the quality of products such as potato and their potential yield. Understanding plant responses to various stresses is an economically important subject in global food security, which is seriously threatened by climate changes. One of the effective methodologies to expand the resistance of potato against various stresses can be identified as the natural defence-related genes. Microarray meta-analysis was used for finding common patterns in microarray data sets. The results were filtered out by comparing the resistant and susceptible host data sets in combination with the data derived from biotic and abiotic stress experiments. A total of 42 candidate resistance genes were selected, which were specifically regulated during the potato-virus interaction. Also, 265 genes were recognized to respond to virus infection or other stresses. Integration of transcriptome data sets from various microarray studies gives new insight into the potato-stress interactions. Moreover, the selected genes can be used as candidates to enhance potato resistance against viruses.
Molecular Plant Pathology
Host gene expression changes in the early response to potato virus Y NTN interaction were compared in two differently sensitive potato cultivars: the resistant cultivar Santé and the sensitive cultivar Igor. Hybridization of potato TIGR cDNA microarrays allowed us to monitor the expression of approximately 10 000 genes simultaneously at 0.5 and 12 h post-inoculation (hpi). Microarray data, analysed by statistics and data mining, were complemented by subtraction library construction and sequence analysis to validate the findings. The expression profiles of the two cultivars were similar and faint at 0.5 hpi, but they differed substantially at 12 hpi. Although, at 0.5 hpi, cv. Santé responded by the differential expression of a greater number of genes, at 12 hpi the number was higher in cv. Igor. The majority of genes in this cultivar were down-regulated at 12 hpi, indicating a host gene shut-off. Suites of genes that exhibited altered transcript abundance in response to the virus were identified, and included genes involved in the processes of photosynthesis, perception, signalling and defence responses. The expression of the considerable number of genes associated with photosynthesis was surprisingly up-regulated as early as 0.5 hpi and down-regulated at 12 hpi in both cultivars. The expression of genes involved in perception and signalling was increased in the sensitive cultivar at 12 hpi. By contrast, a simultaneous strong defence response at the transcriptional level was evident in the resistant cultivar, as shown by the up-regulation of genes involved in brassinosteroid, polyamine and secondary metabolite biosynthesis, and of genes coding for pathogenesis-related proteins.
Metabolomics, 2014
In order to understand resistance to Tomato yellow leaf curl virus (TYLCV) we have performed a combined analysis of the metabolome and transcriptome of resistant (R) and susceptible (S) tomato plants both prior to and following TYLCV infection. Metabolites detected by gas chromatography-mass spectrometry (GC-MS) and liquid chromatography-mass spectrometry analysis, in leaves of R and S plants, at 1, 3, 7 and 14 days post infection and control plants, were used for the reconstruction of four independent metabolic networks. Measuring the network parameters revealed distinctive systemic metabolic responses to TYLCV infection between the R and S plants. Notably, the GC-MS metabolic network indicated that, following infection, the R plant exhibited tight coordination of the metabolome than the S plant. Clear differences in the level of specialized metabolites between the S and R plants were revealed; among them, substantial alteration in the abundance of amino acids and polyamines, phenolic and indolic metabolites, all leading to the synthesis of defense compounds. Integrating metabolome and transcriptome data highlighted differently regulated pathways in the R and S plants in response to TYLCV, including the phenylpropanoid, tryptophan/nicotinate and urea/polyamine pathways. Salicylic acid biosynthesis was additionally distinctively activated in R plants upon infection. Comparing the expression of genes of the urea and phenylpropanoid pathways in S, R and Solanum habrochaites, the resistance genitor wild species tomato, indicated a time-shift in the expression patterns, before and following infection, which on one hand reflected the genetic similarity between these plants, and on the other hand demonstrated that the resistant phenotype is intermediate between that of S and S. habrochaites.
Virology Journal
Background: Potato virus Y (PVY) is one of the most economically important pathogen of potato that is present as biologically distinct strains. The virus-derived small interfering RNAs (vsiRNAs) from potato cv. Russet Burbank individually infected with PVY-N, PVY-NTN and PVY-O strains were recently characterized. Plant defense RNA-silencing mechanisms deployed against viruses produce vsiRNAs to degrade homologous viral transcripts. Based on sequence complementarity, the vsiRNAs can potentially degrade host RNA transcripts raising the prospect of vsiRNAs as pathogenicity determinants in virus-host interactions. This study investigated the global effects of PVY vsiRNAs on the host potato transcriptome. Methods: The strain-specific vsiRNAs of PVY, expressed in high copy number, were analyzed in silico for their proclivity to target potato coding and non-coding RNAs using psRobot and psRNATarget algorithms. Functional annotation of target coding transcripts was carried out to predict physiological effects of the vsiRNAs on the potato cv. Russet Burbank. The downregulation of selected target coding transcripts was further validated using qRT-PCR. Results: The vsiRNAs derived from biologically distinct strains of PVY displayed diversity in terms of absolute number, copy number and hotspots for siRNAs on their respective genomes. The vsiRNAs populations were derived with a high frequency from 6 K1, P1 and Hc-Pro for PVY-N, P1, Hc-Pro and P3 for PVY-NTN, and P1, 3′ UTR and NIa for PVY-O genomic regions. The number of vsiRNAs that displayed interaction with potato coding transcripts and number of putative coding target transcripts were comparable between PVY-N and PVY-O, and were relatively higher for PVY-NTN. The most abundant target non-coding RNA transcripts for the strain specific PVY-derived vsiRNAs were found to be MIR821, 28S rRNA,18S rRNA, snoR71, tRNA-Met and U5. Functional annotation and qRT-PCR validation suggested that the vsiRNAs target genes involved in plant hormone signaling, genetic information processing, plant-pathogen interactions, plant defense and stress response processes in potato.