Transcriptomic changes in<i>Nicotiana benthamiana</i>plants inoculated with the wild‐type or an attenuated mutant of<i>Tobacco vein banding mosaic virus</i>

Geng, Chao; Wang, Hongyan; Liu, Jin; Yan, Zhi‐Yong; Tian, Yanping; Yuan, Xuefeng; Gao, Rui; Li, Xiangdong

doi:10.1111/mpp.12471

Cited by 21 publications

(16 citation statements)

References 53 publications

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“…genes involved in the RNA silencing pathway, the JA signaling pathway, and the auxin signaling transduction68 .Altogether, the results reported in this study illustrate the complex interaction between viruses and their native host plants, and how the outcome of this interaction, in terms of viral replication and accumulation, correlates with the expression of host genes(Fig. 8A).…”

supporting

confidence: 65%

“…In this case, the more virulent strain mainly altered stress responses and transport functions compared to the mild one 67 . In a recent study, the transcriptomic alterations induced in Nicotiana benthamiana plants infected either with a wild-type tobacco vein banding mosaic potyvirus (TVBMV) or a genotype deficient in VSR protein HC-Pro were compared 68 . Both transcriptomes differed in many aspects, including repression of photosynthesis-related genes,…”

Section: Discussionmentioning

confidence: 99%

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Viral fitness predicts the magnitude and direction of perturbations in the infected host transcriptome

Cervera

Ambrós

Bernet

et al. 2017

Preprint

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Overall, these results reveal the high information content of viral fitness, and suggest its potential use to predict differences in genomic profiles of infected hosts.. CC-BY-NC-ND 4.0 International license not peer-reviewed) is the author/funder. It is made available under aThe copyright holder for this preprint (which was . http://dx.doi.org/10.1101/206789 doi: bioRxiv preprint first posted online 3 Fitness is a complex parameter often used by evolutionary biologists and ecologists to quantitatively describe the reproductive ability and evolutionary potential of an organism into a particular environment 1,2 . Despite this apparently simple definition, measuring fitness is difficult and most studies only measure one or more fitness components (e.g., survival to maturity, fecundity, number of mates, or number of offspring produced) as proxies to total fitness 1,2 . In the field of virology, it has become standard to measure fitness by growth-competition experiments in mixed infections with a reference strain 3,4 . With this experimental set up, fitness is just the relative ability of a viral strain to produce stable infectious progeny in a given host (cell type, organ, individual, or species) when the available resources have to be shared with a competitor 5 .Regardless its limitations, at least, this approach provides a metric for ranking viral strains according to their performance in a particular environment/host. Such a fitness measure has been pivotal for quantitatively understanding many virus evolution processes: the effect of genetic bottlenecks and accumulation of deleterious mutations in RNA virus populations 6-8 , the rates and dynamics of adaptive evolution into novel hosts 9, , the pleiotropic cost of host range expansion [10][11][12] , the cost of genome complexity 13,14 , the cost of antiviral escape mutations [15][16][17] , the topography of adaptive fitness landscapes [18][19][20] , and the role of robustness in virus evolution [21][22][23] .But differences in viral fitness should also matter in genome wide studies seeking to understand the mode of action of the viruses (i.e., the precise way they interact with their hosts).Even though it has been argued that an integrative systems biology approach to viral pathogenesis would result in a better understanding of pathogenesis and in the identification of common targets for different viruses, therefore serving as a guide to a more rational design of therapeutic drugs [24][25][26][27][28][29][30] , pioneering studies have ignored the high genetic variability of viruses and subsequent differences in fitness and in mode of action. Experimental evidences support that even single nucleotide substitutions have significant effects on viral fitness, regardless they are synonymous or nonsynonymous, or they affect coding or non-coding genomic regions [31][32][33][34][35][36][37] . A common trend among all these studies is that, whenever fitness is evaluated in the standard host, the distribution of mutational effects is highly skewed towards deleterious...

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supporting

confidence: 65%

Section: Discussionmentioning

confidence: 99%

Viral fitness predicts the magnitude and direction of perturbations in the infected host transcriptome

Cervera

Ambrós

Bernet

et al. 2017

Preprint

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“…2015 ). In a recent study, the transcriptomic alterations induced in Nicotiana benthamiana plants infected either with a WT tobacco vein banding mosaic potyvirus or a genotype deficient in the VSR were compared ( Geng et al. 2017 ).…”

Section: Resultsmentioning

confidence: 99%

Viral Fitness Correlates with the Magnitude and Direction of the Perturbation Induced in the Host’s Transcriptome: The Tobacco Etch Potyvirus—Tobacco Case Study

Cervera

Ambrós

Bernet

et al. 2018

Molecular Biology and Evolution

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Determining the fitness of viral genotypes has become a standard practice in virology as it is essential to evaluate their evolutionary potential. Darwinian fitness, defined as the advantage of a given genotype with respect to a reference one, is a complex property that captures, in a single figure, differences in performance at every stage of viral infection. To what extent does viral fitness result from specific molecular interactions with host factors and regulatory networks during infection? Can we identify host genes in functional classes whose expression depends on viral fitness? Here, we compared the transcriptomes of tobacco plants infected with seven genotypes of tobacco etch potyvirus that differ in fitness. We found that the larger the fitness differences among genotypes, the more dissimilar the transcriptomic profiles are. Consistently, two different mutations, one in the viral RNA polymerase and another in the viral suppressor of RNA silencing, resulted in significantly similar gene expression profiles. Moreover, we identified host genes whose expression showed a significant correlation, positive or negative, with the virus' fitness. Differentially expressed genes which were positively correlated with viral fitness activate hormone- and RNA silencing-mediated pathways of plant defense. In contrast, those that were negatively correlated with fitness affect metabolism, reducing growth, and development. Overall, these results reveal the high information content of viral fitness and suggest its potential use to predict differences in genomic profiles of infected hosts.

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“…Time-course studies have also allowed monitoring symptomatic and asymptomatic phases of infection associated with symptom recovery or with delayed symptom induction ( Allie et al, 2014 ; Madronero et al, 2018 ). Finally, transcriptomes or proteomes have been compared in susceptible, resistant or tolerant cultivars infected with the same virus strain ( Allie et al, 2014 ; Wang et al, 2016b ) or in plants infected with virulent or mild virus strains ( Kogovsek et al, 2016 ; Geng et al, 2017 ). Not surprisingly, these studies have highlighted both similarities and differences in the transcriptome changes induced by viruses in susceptible, tolerant, and resistant interactions.…”

Section: Insights In the Complexity Of Tolerant Plant–virus Interactimentioning

confidence: 99%

Exploring the Diversity of Mechanisms Associated With Plant Tolerance to Virus Infection

Paudel

Sanfaçon

2018

Front. Plant Sci.

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Tolerance is defined as an interaction in which viruses accumulate to some degree without causing significant loss of vigor or fitness to their hosts. Tolerance can be described as a stable equilibrium between the virus and its host, an interaction in which each partner not only accommodate trade-offs for survival but also receive some benefits (e.g., protection of the plant against super-infection by virulent viruses; virus invasion of meristem tissues allowing vertical transmission). This equilibrium, which would be associated with little selective pressure for the emergence of severe viral strains, is common in wild ecosystems and has important implications for the management of viral diseases in the field. Plant viruses are obligatory intracellular parasites that divert the host cellular machinery to complete their infection cycle. Highjacking/modification of plant factors can affect plant vigor and fitness. In addition, the toxic effects of viral proteins and the deployment of plant defense responses contribute to the induction of symptoms ranging in severity from tissue discoloration to malformation or tissue necrosis. The impact of viral infection is also influenced by the virulence of the specific virus strain (or strains for mixed infections), the host genotype and environmental conditions. Although plant resistance mechanisms that restrict virus accumulation or movement have received much attention, molecular mechanisms associated with tolerance are less well-understood. We review the experimental evidence that supports the concept that tolerance can be achieved by reaching the proper balance between plant defense responses and virus counter-defenses. We also discuss plant translation repression mechanisms, plant protein degradation or modification pathways and viral self-attenuation strategies that regulate the accumulation or activity of viral proteins to mitigate their impact on the host. Finally, we discuss current progress and future opportunities toward the application of various tolerance mechanisms in the field.

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Transcriptomic changes inNicotiana benthamianaplants inoculated with the wild‐type or an attenuated mutant ofTobacco vein banding mosaic virus

Cited by 21 publications

References 53 publications

Viral fitness predicts the magnitude and direction of perturbations in the infected host transcriptome

Viral fitness predicts the magnitude and direction of perturbations in the infected host transcriptome

Viral Fitness Correlates with the Magnitude and Direction of the Perturbation Induced in the Host’s Transcriptome: The Tobacco Etch Potyvirus—Tobacco Case Study

Exploring the Diversity of Mechanisms Associated With Plant Tolerance to Virus Infection

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