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Article ; Online: Identification of epigenetically regulated genes involved in plant-virus interaction and their role in virus-triggered induced resistance.

Corrêa, Régis L / Kutnjak, Denis / Ambrós, Silvia / Bustos, Mónica / Elena, Santiago F

2024 Volume 24, Issue 1, Page(s) 172

Abstract: Background: Plant responses to a wide range of stresses are known to be regulated by epigenetic mechanisms. Pathogen-related investigations, particularly against RNA viruses, are however scarce. It has been demonstrated that Arabidopsis thaliana plants ... ...

Abstract	Background: Plant responses to a wide range of stresses are known to be regulated by epigenetic mechanisms. Pathogen-related investigations, particularly against RNA viruses, are however scarce. It has been demonstrated that Arabidopsis thaliana plants defective in some members of the RNA-directed DNA methylation (RdDM) or histone modification pathways presented differential susceptibility to the turnip mosaic virus. In order to identify genes directly targeted by the RdDM-related RNA Polymerase V (POLV) complex and the histone demethylase protein JUMONJI14 (JMJ14) during infection, the transcriptomes of infected mutant and control plants were obtained and integrated with available chromatin occupancy data for various epigenetic proteins and marks. Results: A comprehensive list of virus-responsive gene candidates to be regulated by the two proteins was obtained. Twelve genes were selected for further characterization, confirming their dynamic regulation during the course of infection. Several epigenetic marks on their promoter sequences were found using in silico data, raising confidence that the identified genes are actually regulated by epigenetic mechanisms. The altered expression of six of these genes in mutants of the methyltransferase gene CURLY LEAF and the histone deacetylase gene HISTONE DEACETYLASE 19 suggests that some virus-responsive genes may be regulated by multiple coordinated epigenetic complexes. A temporally separated multiple plant virus infection experiment in which plants were transiently infected with one virus and then infected by a second one was designed to investigate the possible roles of the identified POLV- and JMJ14-regulated genes in wild-type (WT) plants. Plants that had previously been stimulated with viruses were found to be more resistant to subsequent virus challenge than control plants. Several POLV- and JMJ14-regulated genes were found to be regulated in virus induced resistance in WT plants, with some of them poisoned to be expressed in early infection stages. Conclusions: A set of confident candidate genes directly regulated by the POLV and JMJ14 proteins during virus infection was identified, with indications that some of them may be regulated by multiple epigenetic modules. A subset of these genes may also play a role in the tolerance of WT plants to repeated, intermittent virus infections.
MeSH term(s)	Plant Viruses ; DNA Methylation ; Arabidopsis/genetics ; Histone Deacetylases ; Virus Diseases ; Arabidopsis Proteins ; Jumonji Domain-Containing Histone Demethylases
Chemical Substances	Histone Deacetylases (EC 3.5.1.98) ; JMJ14 protein, Arabidopsis (EC 1.14.11.-) ; Arabidopsis Proteins ; Jumonji Domain-Containing Histone Demethylases (EC 1.14.11.-)
Language	English
Publishing date	2024-03-05
Publishing country	England
Document type	Journal Article
ZDB-ID	2059868-3
ISSN	1471-2229 ; 1471-2229
ISSN (online)	1471-2229
ISSN	1471-2229
DOI	10.1186/s12870-024-04866-3
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Article ; Online: On the early identification and characterization of pear blister canker viroid, apple dimple fruit viroid, peach latent mosaic viroid and chrysanthemum chlorotic mottle viroid.

Navarro, Beatriz / Ambrós, Silvia / Serio, Francesco Di / Hernández, Carmen

Virus research

2022 Volume 323, Page(s) 199012

Abstract: In the 90's, pear blister canker viroid (PBCVd), apple dimple fruit viroid (ADFVd), peach latent mosaic viroid (PLMVd) and chrysanthemum chlorotic mottle viroid (CChMVd) were identified and characterized in the Ricardo Flores' laboratory. In these ... ...

Abstract	In the 90's, pear blister canker viroid (PBCVd), apple dimple fruit viroid (ADFVd), peach latent mosaic viroid (PLMVd) and chrysanthemum chlorotic mottle viroid (CChMVd) were identified and characterized in the Ricardo Flores' laboratory. In these studies, the autonomous replication of these infectious RNAs and their involvement in the elicitation of diseases in their natural hosts were also shown. Their discovery was achieved by classical approaches based on the physical purification of the viroid RNAs from polyacrylamide gels followed by the sequencing of their genomic RNAs and by bioassays to assess their autonomous replication and the fulfillment of Koch's postulates. The molecular characterization of these four viroids, including the study of their sequence variability, contributed to the establishment of the concept of quasispecies for viroids and to the development of reliable molecular diagnostic methods that have facilitated the control of the diseases they caused. Most importantly, some of these viroids became valuable experimental model systems that are still used nowadays to study structural-functional relationships in RNAs and to dissect evolutionary and pathogenic pathways underlying plant-viroid interaction. The differences between early viroid discovery strategies, relying on biological and pathogenic issues, and the current high-throughput sequencing-based approaches, that frequently allow the discovery of new viroids and viroid-like RNAs in symptomless hosts, is also discussed, clarifying why the traditional molecular and biological studies mentioned above are still required to conclusively define the nature of any novel viroid-like RNA.
MeSH term(s)	Viroids/genetics ; Malus ; Pyrus ; Fruit ; Blister ; RNA ; Chrysanthemum
Chemical Substances	RNA (63231-63-0)
Language	English
Publishing date	2022-11-24
Publishing country	Netherlands
Document type	Journal Article
ZDB-ID	605780-9
ISSN	1872-7492 ; 0168-1702
ISSN (online)	1872-7492
ISSN	0168-1702
DOI	10.1016/j.virusres.2022.199012
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Article ; Online: Phenotypic and genomic changes during Turnip mosaic virus adaptation to Arabidopsis thaliana mutants lacking epigenetic regulatory factors.

Ambrós, Silvia / Olmo-Uceda, María J / Corrêa, Régis L / Elena, Santiago F

Evolution; international journal of organic evolution

2023 Volume 78, Issue 1, Page(s) 69–85

Abstract: In this study, we investigated how an emerging RNA virus evolves, interacts, and adapts to populations of a novel host species with defects in epigenetically controlled plant defense mechanisms. Mutations in epigenetic regulatory pathways would exert ... ...

Abstract	In this study, we investigated how an emerging RNA virus evolves, interacts, and adapts to populations of a novel host species with defects in epigenetically controlled plant defense mechanisms. Mutations in epigenetic regulatory pathways would exert different effects on defense-response genes but also induce large-scale alterations in cellular physiology and homeostasis. To test whether these effects condition the emergence and subsequent adaptation of a viral pathogen, we have evolved five independent lineages of a naive turnip mosaic virus (TuMV) strain in a set of Arabidopsis thaliana genotypes carrying mutations that influence important elements of two main epigenetic pathways and compare the results with those obtained for viral lineages evolved in wild-type plants. All evolved lineages showed adaptation to the lack of epigenetically regulated responses through significant increases in infectivity, virulence, and viral load although the magnitude of the improvements strongly depended on the plant genotype. In early passages, these traits evolved more rapidly, but the rate of evolution flattened out in later ones. Viral load was positively correlated with different measures of virulence, though the strength of the associations changed from the ancestral to the evolved viruses. High-throughput sequencing was used to evaluate the viral diversity of each lineage, as well as characterizing the nature of fixed mutations, evolutionary convergences, and potential targets of TuMV adaptation. Within each lineage, we observed a net increase in genome-wide genetic diversity, with some instances where nonsynonymous alleles experienced a transient rise in abundance before being displaced by the ancestral allele. In agreement with previous studies, viral VPg protein has been shown as a key player in the adaptation process, even though no obvious association between fixed alleles and host genotype was found.
MeSH term(s)	Arabidopsis/genetics ; Arabidopsis Proteins/genetics ; Arabidopsis Proteins/metabolism ; Host-Pathogen Interactions/genetics ; Potyvirus/genetics ; Viral Proteins/genetics ; Viral Proteins/metabolism ; Genomics ; Epigenesis, Genetic ; Plant Diseases/genetics
Chemical Substances	Arabidopsis Proteins ; Viral Proteins
Language	English
Publishing date	2023-10-25
Publishing country	United States
Document type	Journal Article
ZDB-ID	2036375-8
ISSN	1558-5646 ; 0014-3820
ISSN (online)	1558-5646
ISSN	0014-3820
DOI	10.1093/evolut/qpad192
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Article: Defects in plant immunity modulate the rates and patterns of RNA virus evolution.

Navarro, Rebeca / Ambrós, Silvia / Butković, Anamarija / Carrasco, José L / González, Rubén / Martínez, Fernando / Wu, Beilei / Elena, Santiago F

Virus evolution

2022 Volume 8, Issue 2, Page(s) veac059

Abstract: It is assumed that host genetic variability for susceptibility to infection conditions virus evolution. Differences in host susceptibility can drive a virus to diversify into strains that track different defense alleles (e.g. antigenic diversity) or to ... ...

Abstract	It is assumed that host genetic variability for susceptibility to infection conditions virus evolution. Differences in host susceptibility can drive a virus to diversify into strains that track different defense alleles (e.g. antigenic diversity) or to infect only the most susceptible genotypes. Here, we have studied how variability in host defenses determines the evolutionary fate of a plant RNA virus. We performed evolution experiments with
Language	English
Publishing date	2022-06-20
Publishing country	England
Document type	Journal Article
ZDB-ID	2818949-8
ISSN	2057-1577
ISSN	2057-1577
DOI	10.1093/ve/veac059
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Article ; Online: Engineered Functional Redundancy Relaxes Selective Constraints upon Endogenous Genes in Viral RNA Genomes.

Ambrós, Silvia / de la Iglesia, Francisca / Rosario, Sttefany M / Butkovic, Anamarija / Elena, Santiago F

Genome biology and evolution

2018 Volume 10, Issue 7, Page(s) 1823–1836

Abstract: Functional redundancy, understood as the functional overlap of different genes, is a double-edge sword. At the one side, it is thought to serve as a robustness mechanism that buffers the deleterious effect of mutations hitting one of the redundant copies, ...

Abstract	Functional redundancy, understood as the functional overlap of different genes, is a double-edge sword. At the one side, it is thought to serve as a robustness mechanism that buffers the deleterious effect of mutations hitting one of the redundant copies, thus resulting in pseudogenization. At the other side, it is considered as a source of genetic and functional innovation. In any case, genetically redundant genes are expected to show an acceleration in the rate of molecular evolution. Here, we tackle the role of functional redundancy in viral RNA genomes. To this end, we have evaluated the rates of compensatory evolution for deleterious mutations affecting an essential function, the suppression of RNA silencing plant defense, of tobacco etch potyvirus (TEV). TEV genotypes containing deleterious mutations in presence/absence of engineered functional redundancy were evolved and the pattern of fitness and pathogenicity recovery evaluated. Genetically redundant genotypes suffered less from the effect of deleterious mutations and showed relatively minor changes in fitness and pathogenicity. By contrast, nongenetically redundant genotypes had very low fitness and pathogenicity at the beginning of the evolution experiment that were fully recovered by the end. At the molecular level, the outcome depended on the combination of the actual mutations being compensated and the presence/absence of functional redundancy. Reversions to wild-type alleles were the norm in the nonredundant genotypes while redundant ones either did not fix any mutation at all or showed a higher nonsynonymous mutational load.
MeSH term(s)	Evolution, Molecular ; Genome, Viral ; Mutation ; Plant Diseases/virology ; Plants/virology ; Potyvirus/genetics ; Potyvirus/pathogenicity ; Pseudogenes ; RNA Interference ; RNA Viruses/genetics ; RNA, Viral/genetics
Chemical Substances	RNA, Viral
Language	English
Publishing date	2018-07-04
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1759-6653
ISSN (online)	1759-6653
DOI	10.1093/gbe/evy141
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Article ; Online: Viroid Diseases in Pome and Stone Fruit Trees and Koch's Postulates: A Critical Assessment.

Di Serio, Francesco / Ambrós, Silvia / Sano, Teruo / Flores, Ricardo / Navarro, Beatriz

Viruses

2018 Volume 10, Issue 11

Abstract: Composed of a naked circular non-protein-coding genomic RNA, counting only a few hundred nucleotides, viroids-the smallest infectious agents known so far-are able to replicate and move systemically in herbaceous and woody host plants, which concomitantly ...

Abstract	Composed of a naked circular non-protein-coding genomic RNA, counting only a few hundred nucleotides, viroids-the smallest infectious agents known so far-are able to replicate and move systemically in herbaceous and woody host plants, which concomitantly may develop specific diseases or remain symptomless. Several viroids have been reported to naturally infect pome and stone fruit trees, showing symptoms on leaves, fruits and/or bark. However, Koch's postulates required for establishing on firm grounds the viroid etiology of these diseases, have not been met in all instances. Here, pome and stone fruit tree diseases, conclusively proven to be caused by viroids, are reviewed, and the need to pay closer attention to fulfilling Koch's postulates is emphasized.
MeSH term(s)	Malus/virology ; Plant Diseases/virology ; Plant Viruses/physiology ; Plants/virology ; Viroids/physiology
Language	English
Publishing date	2018-11-07
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2516098-9
ISSN	1999-4915 ; 1999-4915
ISSN (online)	1999-4915
ISSN	1999-4915
DOI	10.3390/v10110612
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Article ; Online: 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, Héctor / Ambrós, Silvia / Bernet, Guillermo P / Rodrigo, Guillermo / Elena, Santiago F

Molecular biology and evolution

2018 Volume 35, Issue 7, Page(s) 1599–1615

Abstract: 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 ... ...

Abstract	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.
MeSH term(s)	Gene Expression ; Genetic Fitness ; Host-Pathogen Interactions ; Microarray Analysis ; Models, Biological ; Plant Diseases ; Potyvirus/genetics ; Real-Time Polymerase Chain Reaction ; Nicotiana/metabolism ; Nicotiana/virology ; Transcriptome
Keywords	covid19
Language	English
Publishing date	2018-03-07
Publishing country	United States
Document type	Comparative Study ; Journal Article ; Research Support, Non-U.S. Gov't ; Validation Study
ZDB-ID	998579-7
ISSN	1537-1719 ; 0737-4038
ISSN (online)	1537-1719
ISSN	0737-4038
DOI	10.1093/molbev/msy038
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Article ; Online: Molecular signatures of silencing suppression degeneracy from a complex RNA virus.

Ambrós, Silvia / Gómez-Muñoz, Neus / Giménez-Santamarina, Silvia / Sánchez-Vicente, Javier / Navarro-López, Josep / Martínez, Fernando / Daròs, José-Antonio / Rodrigo, Guillermo

PLoS computational biology

2021 Volume 17, Issue 6, Page(s) e1009166

Abstract: As genomic architectures become more complex, they begin to accumulate degenerate and redundant elements. However, analyses of the molecular mechanisms underlying these genetic architecture features remain scarce, especially in compact but sufficiently ... ...

Abstract	As genomic architectures become more complex, they begin to accumulate degenerate and redundant elements. However, analyses of the molecular mechanisms underlying these genetic architecture features remain scarce, especially in compact but sufficiently complex genomes. In the present study, we followed a proteomic approach together with a computational network analysis to reveal molecular signatures of protein function degeneracy from a plant virus (as virus-host protein-protein interactions). We employed affinity purification coupled to mass spectrometry to detect several host factors interacting with two proteins of Citrus tristeza virus (p20 and p25) that are known to function as RNA silencing suppressors, using an experimental system of transient expression in a model plant. The study was expanded by considering two different isolates of the virus, and some key interactions were confirmed by bimolecular fluorescence complementation assays. We found that p20 and p25 target a common set of plant proteins including chloroplastic proteins and translation factors. Moreover, we noted that even specific targets of each viral protein overlap in function. Notably, we identified argonaute proteins (key players in RNA silencing) as reliable targets of p20. Furthermore, we found that these viral proteins preferentially do not target hubs in the host protein interactome, but elements that can transfer information by bridging different parts of the interactome. Overall, our results demonstrate that two distinct proteins encoded in the same viral genome that overlap in function also overlap in their interactions with the cell proteome, thereby highlighting an overlooked connection from a degenerate viral system.
MeSH term(s)	Argonaute Proteins/metabolism ; Citrus/metabolism ; Citrus/virology ; Closterovirus/genetics ; Closterovirus/metabolism ; Computational Biology ; Genome, Viral ; Host Microbial Interactions/genetics ; Host Microbial Interactions/physiology ; Models, Biological ; Plant Diseases/virology ; Plant Proteins/metabolism ; Protein Interaction Maps ; Proteomics ; RNA Interference ; RNA, Viral/genetics ; Repressor Proteins/genetics ; Repressor Proteins/metabolism ; Nicotiana/metabolism ; Nicotiana/virology ; Viral Proteins/genetics ; Viral Proteins/metabolism
Chemical Substances	Argonaute Proteins ; Plant Proteins ; RNA, Viral ; Repressor Proteins ; Viral Proteins
Language	English
Publishing date	2021-06-28
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2193340-6
ISSN	1553-7358 ; 1553-734X
ISSN (online)	1553-7358
ISSN	1553-734X
DOI	10.1371/journal.pcbi.1009166
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Article ; Online: 2b or Not 2b: Experimental Evolution of Functional Exogenous Sequences in a Plant RNA Virus.

Willemsen, Anouk / Zwart, Mark P / Ambrós, Silvia / Carrasco, José L / Elena, Santiago F

Genome biology and evolution

2017 Volume 9, Issue 2, Page(s) 297–310

Abstract: Horizontal gene transfer (HGT) is pervasive in viruses and thought to be a key mechanism in their evolution. On the other hand, strong selective constraints against increasing genome size are an impediment for HGT, rapidly purging horizontally ... ...

Abstract	Horizontal gene transfer (HGT) is pervasive in viruses and thought to be a key mechanism in their evolution. On the other hand, strong selective constraints against increasing genome size are an impediment for HGT, rapidly purging horizontally transferred sequences and thereby potentially hindering evolutionary innovation. Here, we explore experimentally the evolutionary fate of viruses with simulated HGT events, using the plant RNA virus Tobacco etch virus (TEV), by separately introducing two functional, exogenous sequences to its genome. One of the events simulates the acquisition of a new function though HGT of a conserved AlkB domain, responsible for the repair of alkylation or methylation damage in many organisms. The other event simulates the acquisition of a sequence that duplicates an existing function, through HGT of the 2b RNA silencing suppressor from Cucumber mosaic virus. We then evolved these two viruses, tracked the maintenance of the horizontally transferred sequences over time, and for the final virus populations, sequenced their genome and measured viral fitness. We found that the AlkB domain was rapidly purged from the TEV genome, restoring fitness to wild-type levels. Conversely, the 2b gene was stably maintained and did not have a major impact on viral fitness. Moreover, we found that 2b is functional in TEV, as it provides a replicative advantage when the RNA silencing suppression domain of HC-Pro is mutated. These observations suggest a potentially interesting role for HGT of short functional sequences in ameliorating evolutionary constraints on viruses, through the duplication of functions.
MeSH term(s)	AlkB Enzymes/chemistry ; AlkB Enzymes/genetics ; Cucumovirus/genetics ; Evolution, Molecular ; Gene Transfer, Horizontal ; Genome, Viral ; Potyvirus/genetics ; Protein Domains ; RNA, Viral/genetics ; Nicotiana/virology
Chemical Substances	RNA, Viral ; AlkB Enzymes (EC 1.14.11.33)
Language	English
Publishing date	2017-01-30
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2495328-3
ISSN	1759-6653 ; 1759-6653
ISSN (online)	1759-6653
ISSN	1759-6653
DOI	10.1093/gbe/evw300
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Article: A new procedure for rapid evaluation of the ability of Citrus tristeza virus mild isolates to cross protect against severe isolates

Ruiz-Ruiz, Susana / Navarro-Lopez, Josep / Moreno, Pedro / Ambros, Silvia

Acta horticulturae. 2015 Jan. 20, , no. 1065

2015

Abstract: Measures to control damage caused by severe stem pitting strains (SP) of Citrus tristeza virus (CTV) include selective eradication and cross protection with mild strains (MS). Implementation of these measures needs sensitive and specific methods to ... ...

Abstract	Measures to control damage caused by severe stem pitting strains (SP) of Citrus tristeza virus (CTV) include selective eradication and cross protection with mild strains (MS). Implementation of these measures needs sensitive and specific methods to discriminate between SP and MS variants in the viral populations. We developed a quantitative real-time RT-PCR method using Taqman locked nucleic acid (LNA) probes that enabled quantification of SP and MS variants in natural CTV populations. Here we used this method to monitor the evolution of the CTV population in Pineapple sweet orange plants pre-inoculated with a MS (T32) or a SP (T318) isolate, and then challenge-inoculated with budsticks infected with a SP or a MS isolate, respectively. While control plants singly inoculated with T32 or T318 only contained the cognate CTV variant in successive flushes, the plants doubly inoculated contained the two sequence variants in tissues derived from both the receptor plant and the inoculum budstick, with no strain impairing systemic invasion by the other. The relative amount of T32 and T318 variants in the co-infected plants differed between flushes. The co-infected plants showed stem pitting symptoms similar to those of plants inoculated only with T318, whereas control plants inoculated only with T32 or non-inoculated remained symptomless. This procedure enables rapid evaluation of MS for cross protecting ability.
Keywords	Citrus tristeza virus ; control methods ; evolution ; inoculum ; nucleic acids ; oranges ; reverse transcriptase polymerase chain reaction ; tissues
Language	English
Dates of publication	2015-0120
Size	p. 799-807.
Publishing place	International Society for Horticultural Science.
Document type	Article
Note	Paper presented at the XII International Citrus Congress - International Society of Citriculture, held November 18-23, 2012, Valencia, Spain
ISSN	0567-7572
Database	NAL-Catalogue (AGRICOLA)

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