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

Stare et al. BMC Genomics (2015) 16:716 DOI 10.1186/s12864-015-1925-2 RESEARCH ARTICLE Open Access Bimodal dynamics of primary metabolismrelated responses in tolerant potato-Potato virus Y interaction Tjaša Stare1*, Živa Ramšak1, Andrej Blejec1, Katja Stare1, Neža Turnšek1, Wolfram Weckwerth2, Stefanie Wienkoop2, Dominik Vodnik3 and Kristina Gruden1 Abstract 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 PVYNTN strain. We focused on the dynamics of the primary metabolism-related processes during PVYNTN 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 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. Keywords: Plant-pathogen interactions, Potato virus Y, Potyviridae, Salicylic acid, Solanum tuberosum, Whole transcriptome analysis, Shot-gun proteomics, Photosynthetic parameters * Correspondence: 1 Department of Biotechnology and Systems Biology, National Institute of Biology, Vecna pot 111, Ljubljana, Slovenia Full list of author information is available at the end of the article © 2015 Stare et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Stare et al. BMC Genomics (2015) 16:716 Background Potato (Solanum tuberosum L.) is the most widely grown tuber crop in the world, and the fourth largest food crop in terms of fresh produce, after rice, wheat and tomato. Potato virus Y (PVY) is a member of the Potyviridae family, and economically, it is one of the most important potato pathogens, with a worldwide spread [1]. Several strains of PVY have been isolated that differ at the molecular and biological levels. PVYNTN is an aggressive isolate that induces severe symptoms in sensitive potato cultivars, with the development of potato tuber necrotic ringspot disease, thus resulting in major economic losses [2, 3]. Different potato cultivars show different levels of sensitivity to this particular viral strain, from susceptibility, through tolerance, to complete resistance (reviewed in [2]). Plant defenses against pathogens are regulated at the molecular level by a network of interconnecting signal transduction pathways, of which salicylic acid (SA) is an important component [4, 5]. SA has been shown to mediate resistance in many compatible plant-virus interactions and its deficiency leads to an impairment of the defense responses and susceptibility to pathogen attack [6, 7]. Depending upon the virus and the host, SA can induce inhibition of viral replication, or cell-to-cell or long distance viral movement [4, 8]. In recent years, it has become clear that plant defense responses are complex, and that they arise from crosstalk between different hormonal signaling pathways that enable specificity of responses to different pathogens and fine-tuning of defense responses [5, 9]. Pathogens that attack plants promote massive reprogramming of the plant metabolism for the synthesis of chemical defenses—a process that can be costly in terms of plant growth and fitness [10]. Plants must balance potentially competing demands for resources, to support both their defense and their requirements for cellular maintenance, growth and reproduction. Previous studies have shown that lowered plant growth rates in virusinfected plants can be attributed mainly to impaired photosynthesis, albeit experimental data that relate biotic stress and photosynthesis are often inconsistent. On the one hand, a decline in the rate of photosynthesis following attack by insects or pathogens has been documented; and on the other hand, examples of compensatory stimulation of photosynthesis have also been reported (reviewed in [11]). Most of these studies have focused on different static time points after virus infection, with very few exceptions that have followed the dynamics of targeted gene expression [12, 13]. However, to understand the reprogramming of plant metabolism, it is not sufficient to look only at a single ‘screen shoot’ of the plant status. Instead, dynamic ranges of these responses should be monitored. The potato-PVY interaction has been studied previously at both morphological and biochemical levels, as well as at the gene expression level (reviewed in [2]). Recently, we Page 2 of 17 performed a time series analysis of resp (...truncated)