Bimodal dynamics of primary metabolism-related responses in tolerant potato-Potato virus Y interaction

Abstract

BackgroundPotato 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 PVYNTN strain. We focused on the dynamics of the primary metabolism-related processes during PVYNTN infection.ResultsA 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.ConclusionsDown-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 PVYNTN 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1925-2) contains supplementary material, which is available to authorized users.

Salicylic acid mitigates physiological and proteomic changes induced by the SPCP1 strain of Potato virus X in tomato plants

“…Plant responses from secondary metabolism have been intensively studied for decades, but less is known about the effect of phytopathogens on plant primary metabolism [69]. Recently, interest in this aspect of plant viral interactions has been increasing as, for instance, in the potyviruses [59,68].…”

Salicylic acid perturbs sRNA-gibberellin regulatory network in immune response of potato toPotato virus Yinfection

“…We further compared miRNA expression profiles of PVY NTN -infected versus mock inoculated leaves in early stages of virus infection (3 dpi, 1 day before detectable viral multiplication; [5,7]). In total, 57 unique miRNAs were found to be significantly differentially expressed in early stages of PVY NTN infection (3 dpi) of Désirée plants.…”

“…Hence, the tolerant phenotype is likely to be more durable than resistance [6]. Until now, studies on Désirée-PVY NTN interactions have focused on the detection of changes in the plant transcriptome and proteome, particularly those related to plant hormonal signaling [5,7]. Salicylic acid (SA) was found to be the crucial component for attenuation of the disease symptoms [5].…”

Achievements and prospects of applying high-throughput sequencing techniques to potato genetics and breeding

“…ncbi.nlm.nih.gov/geo/) -это база данных, в которой собра ны результаты высокопроизводительного секвенирования транскриптомов (RNAseq) и анализа экспрессии генов с использованием микрочипов, в том числе для S. tuberosum (Rensink et al, 2005;Carvallo et al, 2011;Evers et al, 2012;Zhang et al, 2013;Stare et al, 2015;Gálvez et al, 2016). База данных GEO включает несколько разделов, в том числе DataSets, который содержит описание эксперимен тов по секвенированию транскриптомов.…”

“…В этом разделе суммированы данные 1 583 экспериментов, посвященных анализу транскриптома картофеля. Результаты транс криптомных экспериментов в БД GEO представлены в 30 публикациях, в число которых входят исследования по изменению транскриптома картофеля в ответ на за ражение вирусами Petek et al, 2014;Stare et al, 2015), на воздействие факторами абиотического стресса (Gálvez et al, 2016), различия в уровне экспрессии генов miRNA в зависимости от стадии развития (Lakhotia et al, 2014). Первичные данные секвенирования транс криптомов в экспериментах RNAseq представлены в базе данных NCBI SRA (Sequence Read Archive), основном мировом архиве результатов высокопроизводительного секвенирования нуклеотидных последовательностей.…”