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Prof. Jeanmarie Verchot
Plant Virology, Texas A&M AgriLife Research, Dallas, TX, USA

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0 Protein–membrane interactions
0 Potexvirus
0 Potyvirus
0 ER stress regulation
0 Cellular interactions

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Potexvirus

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Review
Published: 06 May 2021 in Viruses
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Negative-strand (-) RNA viruses (NSVs) comprise a large and diverse group of viruses that are generally divided in those with non-segmented and those with segmented genomes. Whereas most NSVs infect animals and humans, the smaller group of the plant-infecting counterparts is expanding, with many causing devastating diseases worldwide, affecting a large number of major bulk and high-value food crops. In 2018, the taxonomy of segmented NSVs faced a major reorganization with the establishment of the order Bunyavirales. This article overviews the major plant viruses that are part of the order, i.e., orthospoviruses (Tospoviridae), tenuiviruses (Phenuiviridae), and emaraviruses (Fimoviridae), and provides updates on the more recent ongoing research. Features shared with the animal-infecting counterparts are mentioned, however, special attention is given to their adaptation to plant hosts and vector transmission, including intra/intercellular trafficking and viral counter defense to antiviral RNAi.

ACS Style

Richard Kormelink; Jeanmarie Verchot; Xiaorong Tao; Cecile Desbiez. The Bunyavirales: The Plant-Infecting Counterparts. Viruses 2021, 13, 842 .

AMA Style

Richard Kormelink, Jeanmarie Verchot, Xiaorong Tao, Cecile Desbiez. The Bunyavirales: The Plant-Infecting Counterparts. Viruses. 2021; 13 (5):842.

Chicago/Turabian Style

Richard Kormelink; Jeanmarie Verchot; Xiaorong Tao; Cecile Desbiez. 2021. "The Bunyavirales: The Plant-Infecting Counterparts." Viruses 13, no. 5: 842.

Journal article
Published: 11 March 2021 in International Journal of Molecular Sciences
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Potato virus X (PVX) belongs to genus Potexvirus. This study characterizes the cellular transcriptome responses to PVX infection in Russet potato at 2 and 3 days post infection (dpi). Among the 1242 differentially expressed genes (DEGs), 268 genes were upregulated, and 37 genes were downregulated at 2 dpi while 677 genes were upregulated, and 265 genes were downregulated at 3 dpi. DEGs related to signal transduction, stress response, and redox processes. Key stress related transcription factors were identified. Twenty-five pathogen resistance gene analogs linked to effector triggered immunity or pathogen-associated molecular pattern (PAMP)-triggered immunity were identified. Comparative analysis with Arabidopsis unfolded protein response (UPR) induced DEGs revealed genes associated with UPR and plasmodesmata transport that are likely needed to establish infection. In conclusion, this study provides an insight on major transcriptional regulatory networked involved in early response to PVX infection and establishment.

ACS Style

Venura Herath; Jeanmarie Verchot. Transcriptional Regulatory Networks Associate with Early Stages of Potato Virus X Infection of Solanum tuberosum. International Journal of Molecular Sciences 2021, 22, 2837 .

AMA Style

Venura Herath, Jeanmarie Verchot. Transcriptional Regulatory Networks Associate with Early Stages of Potato Virus X Infection of Solanum tuberosum. International Journal of Molecular Sciences. 2021; 22 (6):2837.

Chicago/Turabian Style

Venura Herath; Jeanmarie Verchot. 2021. "Transcriptional Regulatory Networks Associate with Early Stages of Potato Virus X Infection of Solanum tuberosum." International Journal of Molecular Sciences 22, no. 6: 2837.

Editorial
Published: 08 January 2021 in Viruses
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It is with great sadness and sympathy for his family and the plant virology community that we convey the passing of Michael Goodin unexpectedly in December 2020

ACS Style

Jeanmarie Verchot; Andrew O. Jackson; Anne E. Simon. In Tribute to Michael Goodin. Viruses 2021, 13, 78 .

AMA Style

Jeanmarie Verchot, Andrew O. Jackson, Anne E. Simon. In Tribute to Michael Goodin. Viruses. 2021; 13 (1):78.

Chicago/Turabian Style

Jeanmarie Verchot; Andrew O. Jackson; Anne E. Simon. 2021. "In Tribute to Michael Goodin." Viruses 13, no. 1: 78.

Editorial
Published: 01 January 2021 in Viruses
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We are pleased to present in this Special Issue a series of reviews and research studies on the topic of “Plant Virus Emergence”

ACS Style

Michael Goodin; Jeanmarie Verchot. Introduction to Special Issue of Plant Virus Emergence. Viruses 2021, 13, 55 .

AMA Style

Michael Goodin, Jeanmarie Verchot. Introduction to Special Issue of Plant Virus Emergence. Viruses. 2021; 13 (1):55.

Chicago/Turabian Style

Michael Goodin; Jeanmarie Verchot. 2021. "Introduction to Special Issue of Plant Virus Emergence." Viruses 13, no. 1: 55.

Journal article
Published: 29 December 2020 in International Journal of Molecular Sciences
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The basic region-leucine zipper (bZIP) transcription factors (TFs) form homodimers and heterodimers via the coil–coil region. The bZIP dimerization network influences gene expression across plant development and in response to a range of environmental stresses. The recent release of the most comprehensive potato reference genome was used to identify 80 StbZIP genes and to characterize their gene structure, phylogenetic relationships, and gene expression profiles. The StbZIP genes have undergone 22 segmental and one tandem duplication events. Ka/Ks analysis suggested that most duplications experienced purifying selection. Amino acid sequence alignments and phylogenetic comparisons made with the Arabidopsis bZIP family were used to assign the StbZIP genes to functional groups based on the Arabidopsis orthologs. The patterns of introns and exons were conserved within the assigned functional groups which are supportive of the phylogeny and evidence of a common progenitor. Inspection of the leucine repeat heptads within the bZIP domains identified a pattern of attractive pairs favoring homodimerization, and repulsive pairs favoring heterodimerization. These patterns of attractive and repulsive heptads were similar within each functional group for Arabidopsis and S. tuberosum orthologs. High-throughput RNA-seq data indicated the most highly expressed and repressed genes that might play significant roles in tissue growth and development, abiotic stress response, and response to pathogens including Potato virus X. These data provide useful information for further functional analysis of the StbZIP gene family and their potential applications in crop improvement.

ACS Style

Venura Herath; Jeanmarie Verchot. Insight into the bZIP Gene Family in Solanum tuberosum: Genome and Transcriptome Analysis to Understand the Roles of Gene Diversification in Spatiotemporal Gene Expression and Function. International Journal of Molecular Sciences 2020, 22, 253 .

AMA Style

Venura Herath, Jeanmarie Verchot. Insight into the bZIP Gene Family in Solanum tuberosum: Genome and Transcriptome Analysis to Understand the Roles of Gene Diversification in Spatiotemporal Gene Expression and Function. International Journal of Molecular Sciences. 2020; 22 (1):253.

Chicago/Turabian Style

Venura Herath; Jeanmarie Verchot. 2020. "Insight into the bZIP Gene Family in Solanum tuberosum: Genome and Transcriptome Analysis to Understand the Roles of Gene Diversification in Spatiotemporal Gene Expression and Function." International Journal of Molecular Sciences 22, no. 1: 253.

Review article
Published: 22 December 2020 in Current Opinion in Virology
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In recent years there have been significant advances in our understanding of the ER stress responses in plants that are associated with virus infection, as well as bacterial and fungal diseases. In plants, ER stress induced by virus infection includes several signaling pathways that include the unfolded protein response (UPR) to promote the expression of chaperone proteins for proper protein folding. Understanding how facets of ER stress signaling broadly engage in pathogen responses, as well as those that are specific to virus infection is important to distinguishing features essential for broad cellular defenses and processes that may be specifically linked to viral infectivity and disease.

ACS Style

Jeanmarie Verchot; Karolina M Pajerowska-Mukhtar. UPR signaling at the nexus of plant viral, bacterial, and fungal defenses. Current Opinion in Virology 2020, 47, 9 -17.

AMA Style

Jeanmarie Verchot, Karolina M Pajerowska-Mukhtar. UPR signaling at the nexus of plant viral, bacterial, and fungal defenses. Current Opinion in Virology. 2020; 47 ():9-17.

Chicago/Turabian Style

Jeanmarie Verchot; Karolina M Pajerowska-Mukhtar. 2020. "UPR signaling at the nexus of plant viral, bacterial, and fungal defenses." Current Opinion in Virology 47, no. : 9-17.

Research article
Published: 01 October 2020 in Molecular Plant-Microbe Interactions®
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Rose rosette virus (RRV) is a negative-sense RNA virus with a seven-segmented genome that is enclosed by a double membrane. We constructed an unconventional minireplicon system encoding the antigenomic (ag)RNA1 (encoding the viral RNA-dependent RNA polymerase [RdRp]), agRNA3 (encoding the nucleocapsid protein [N]), and a modified agRNA5 containing the coding sequence for the iLOV protein in place of the P5 open reading frame (R5-iLOV). iLOV expression from the R5-iLOV template was amplified by activities of the RdRp and N proteins in Nicotiana benthamiana leaves. A mutation was introduced into the RdRp catalytic domain and iLOV expression was eliminated, indicating RNA1-encoded polymerase activity drives iLOV expression from the R5-iLOV template. Fluorescence from the replicon was highest at 3 days postinoculation (dpi) and declined at 7 and 13 dpi. Addition of the tomato bushy stunt virus (TBSV) P19 silencing-suppressor protein prolonged expression until 7 dpi. A full-length infectious clone system was constructed of seven binary plasmids encoding each of the seven genome segments. Agro-delivery of constructs encoding RRV RNAs 1 through 4 or RNAs 1 through 7 to N. benthamiana plants produced systemic infection. Finally, agro-delivery of the full-length RRV infectious clone including all segments produced systemic infection within 60 dpi. This advance opens new opportunities for studying RRV infection biology.

ACS Style

Jeanmarie Verchot; Venura Herath; Cesar D. Urrutia; Mathieu Gayral; Kelsey Lyle; Madalyn K. Shires; Kevin Ong; David Byrne. Development of a Reverse Genetic System for Studying Rose Rosette Virus in Whole Plants. Molecular Plant-Microbe Interactions® 2020, 33, 1209 -1221.

AMA Style

Jeanmarie Verchot, Venura Herath, Cesar D. Urrutia, Mathieu Gayral, Kelsey Lyle, Madalyn K. Shires, Kevin Ong, David Byrne. Development of a Reverse Genetic System for Studying Rose Rosette Virus in Whole Plants. Molecular Plant-Microbe Interactions®. 2020; 33 (10):1209-1221.

Chicago/Turabian Style

Jeanmarie Verchot; Venura Herath; Cesar D. Urrutia; Mathieu Gayral; Kelsey Lyle; Madalyn K. Shires; Kevin Ong; David Byrne. 2020. "Development of a Reverse Genetic System for Studying Rose Rosette Virus in Whole Plants." Molecular Plant-Microbe Interactions® 33, no. 10: 1209-1221.

Journal article
Published: 10 September 2020 in Viruses
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Bunyavirales are negative-sense segmented RNA viruses infecting arthropods, protozoans, plants, and animals. This study examines the phylogenetic relationships of plant viruses within this order, many of which are recently classified species. Comprehensive phylogenetic analyses of the viral RNA dependent RNA polymerase (RdRp), precursor glycoprotein (preGP), the nucleocapsid (N) proteins point toward common progenitor viruses. The RdRp of Fimoviridae and Tospoviridae show a close evolutional relationship while the preGP of Fimoviridae and Phenuiviridae show a closed relationship. The N proteins of Fimoviridae were closer to the Phasmaviridae, the Tospoviridae were close to some Phenuiviridae members and the Peribunyaviridae. The plant viral movement proteins of species within the Tospoviridae and Phenuiviridae were more closely related to each other than to members of the Fimoviridae. Interestingly, distal ends of 3′ and 5′ untranslated regions of species within the Fimoviridae shared similarity to arthropod and vertebrate infecting members of the Cruliviridae and Peribunyaviridae compared to other plant virus families. Co-phylogeny analysis of the plant infecting viruses indicates that duplication and host switching were more common than co-divergence with a host species.

ACS Style

Venura Herath; Gustavo Romay; Cesar D. Urrutia; Jeanmarie Verchot. Family Level Phylogenies Reveal Relationships of Plant Viruses within the Order Bunyavirales. Viruses 2020, 12, 1010 .

AMA Style

Venura Herath, Gustavo Romay, Cesar D. Urrutia, Jeanmarie Verchot. Family Level Phylogenies Reveal Relationships of Plant Viruses within the Order Bunyavirales. Viruses. 2020; 12 (9):1010.

Chicago/Turabian Style

Venura Herath; Gustavo Romay; Cesar D. Urrutia; Jeanmarie Verchot. 2020. "Family Level Phylogenies Reveal Relationships of Plant Viruses within the Order Bunyavirales." Viruses 12, no. 9: 1010.

Mini review
Published: 15 August 2020 in Plant Signaling & Behavior
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Plant potexvirus and potyvirus infection can trigger endoplasmic reticulum (ER) stress. ER stress signaling increases the expression of cytoprotective ER-chaperones, especially the BiP chaperones which contribute to pro-survival functions when plants are subjected to infection. The inositol requiring enzyme (IRE1) is one ER stress sensor that is activated to splice the bZIP60 mRNA which produces a truncated transcription factor that activates gene expression in the nucleus. The IRE1/bZIP60 pathway is associated with restricting potyvirus and potexvirus infection. Recent data also identified the IRE1-independent UPR pathways led by bZIP28 and bZIP17 contribute to potexvirus and potyvirus infection. These three bZIP pathways recognize cis-regulatory elements in the BiP promoters to enhance gene expression. BiP is part of a negative feedback loop that regulates the activities of the ER stress transducers IRE1, bZIP28, and bZIP17 to block their activation. We discuss a model in which bZIP60 and bZIP17 synergistically induce BiP and other genes restricting Plantago asiatica mosaic virus (PlAMV; a potexvirus) infection while bZIP60 and bZIP28 independently induce genes supporting PlAMV infection. Regarding Turnip mosiac virus (TuMV, a potyvirus) infection, bZIP60 and bZIP28 serve to repress local and systemic infection. Finally, tauroursodeoxycholic acid treatments were used to demonstrate that the protein folding capacity significantly influences PlAMV accumulation.

ACS Style

Venura Herath; Mathieu Gayral; Rita K. Miller; Jeanmarie Verchot. BIP and the unfolded protein response are important for potyvirus and potexvirus infection. Plant Signaling & Behavior 2020, 15, 1 .

AMA Style

Venura Herath, Mathieu Gayral, Rita K. Miller, Jeanmarie Verchot. BIP and the unfolded protein response are important for potyvirus and potexvirus infection. Plant Signaling & Behavior. 2020; 15 (11):1.

Chicago/Turabian Style

Venura Herath; Mathieu Gayral; Rita K. Miller; Jeanmarie Verchot. 2020. "BIP and the unfolded protein response are important for potyvirus and potexvirus infection." Plant Signaling & Behavior 15, no. 11: 1.

Journal article
Published: 09 July 2020 in Scientific Reports
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The endoplasmic reticulum (ER) immunoglobulin binding proteins (BiPs) are molecular chaperones involved in normal protein maturation and refolding malformed proteins through the unfolded protein response (UPR). Plant BiPs belong to a multi-gene family contributing to development, immunity, and responses to environmental stresses. This study identified three BiP homologs in the Solanum tuberosum (potato) genome using phylogenetic, amino acid sequence, 3-D protein modeling, and gene structure analysis. These analyses revealed that StBiP1 and StBiP2 grouped with AtBiP2, whereas StBiP3 grouped with AtBiP3. While the protein sequences and folding structures are highly similar, these StBiPs are distinguishable by their expression patterns in different tissues and in response to environmental stressors such as treatment with heat, chemicals, or virus elicitors of UPR. Ab initio promoter analysis revealed that potato and Arabidopsis BiP1 and BiP2 promoters were highly enriched with cis-regulatory elements (CREs) linked to developmental processes, whereas BiP3 promoters were enriched with stress related CREs. The frequency and linear distribution of these CREs produced two phylogenetic branches that further resolve the groups identified through gene phylogeny and exon/intron phase analysis. These data reveal that the CRE architecture of BiP promoters potentially define their spatio-temporal expression patterns under developmental and stress related cues.

ACS Style

Venura Herath; Mathieu Gayral; Nirakar Adhikari; Rita Miller; Jeanmarie Verchot. Genome-wide identification and characterization of Solanum tuberosum BiP genes reveal the role of the promoter architecture in BiP gene diversity. Scientific Reports 2020, 10, 1 -14.

AMA Style

Venura Herath, Mathieu Gayral, Nirakar Adhikari, Rita Miller, Jeanmarie Verchot. Genome-wide identification and characterization of Solanum tuberosum BiP genes reveal the role of the promoter architecture in BiP gene diversity. Scientific Reports. 2020; 10 (1):1-14.

Chicago/Turabian Style

Venura Herath; Mathieu Gayral; Nirakar Adhikari; Rita Miller; Jeanmarie Verchot. 2020. "Genome-wide identification and characterization of Solanum tuberosum BiP genes reveal the role of the promoter architecture in BiP gene diversity." Scientific Reports 10, no. 1: 1-14.

Preprint content
Published: 16 May 2020
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The endoplasmic reticulum (ER) immunoglobulin binding proteins (BiPs) are molecular chaperones involved in normal protein maturation and refolding malformed proteins through the unfolded protein response (UPR). Plants BiPs belong to a multi-gene family contributing to development, immunity, and responses to environmental stresses. This study identified three BiP homologues in the Solanum tuberosum (potato) genome using phylogenetic, amino acid sequence, 3-D protein modeling and gene structure analysis. These analyses revealed that StBiP1 and StBiP2 grouped with AtBiP2, whereas StBiP3 grouped with AtBiP3. While the protein sequences and folding structures are highly similar, these StBiPs are distinguishable by their expression patterns in different tissues and in response to environmental stressors such as treatment with heat, chemicals, or virus elicitors of UPR. Ab initio promoter analysis revealed that potato and Arabidopsis BiP1 and BiP2 promoters were highly enriched with cis regulatory elements (CREs) linked to developmental processes, whereas BiP3 promoters were enriched with stress-related CREs. The frequency and linear distribution of these CREs produced two phylogenetic branches that further resolve the groups identified through gene phylogeny and exon/intron phase analysis. These data reveal that the CRE architecture of BiP promoters potentially define their spatio -temporal expression patterns under developmental and stress related cues.

ACS Style

Venura Herath; Mathieu Gayral; Nirakar Adhikari; Rita Miller; Jeanmarie Verchot. Genome-wide identification and characterization of Solanum tuberosum BiP genes reveals the role of the promoter architecture in BiP gene diversity. 2020, 1 .

AMA Style

Venura Herath, Mathieu Gayral, Nirakar Adhikari, Rita Miller, Jeanmarie Verchot. Genome-wide identification and characterization of Solanum tuberosum BiP genes reveals the role of the promoter architecture in BiP gene diversity. . 2020; ():1.

Chicago/Turabian Style

Venura Herath; Mathieu Gayral; Nirakar Adhikari; Rita Miller; Jeanmarie Verchot. 2020. "Genome-wide identification and characterization of Solanum tuberosum BiP genes reveals the role of the promoter architecture in BiP gene diversity." , no. : 1.

Original article
Published: 11 May 2020 in The Plant Journal
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Pathogens and other adverse environmental conditions can trigger endoplasmic reticulum (ER) stress. ER stress signaling increases the expression of cytoprotective ER‐chaperones. The inositol requiring enzyme (IRE1) is one ER stress sensor that is activated to splice the bZIP60 mRNA which produces a truncated transcription factor that activates gene expression in the nucleus. The IRE1/bZIP60 pathway is associated with restricting potyvirus and potexvirus infection. This study shows that the Plantago asiatica mosaic virus (PlAMV) triple gene block 3 (TGB3) and the Turnip mosaic virus (TuMV) 6K2 proteins activate alternative transcription pathways involving the bZIP17, bZIP28, BAG7, NAC089, and NAC103 factors in Arabidopsis thaliana. Using the corresponding knock‐ out mutant lines, we show that bZIP17, bZIP60, BAG7 and NAC089 are factors in reducing PlAMV infection whereas bZIP28 and bZIP60 are factors in reducing TuMV infection. We propose a model in which bZIP60 and bZIP17 synergistically induce genes restricting PlAMV infection while bZIP60 and bZIP28 independently induce genes supporting PlAMV infection. Regarding TuMV‐GFP infection, bZIP60 and bZIP28 serve to repress local and systemic infection. Finally, tauroursodeoxycholic acid treatments were used to demonstrate that the protein folding capacity significantly influences PlAMV accumulation.

ACS Style

Mathieu Gayral; Omar Arias Gaguancela; Evelyn Vasquez; Venura Herath; Francisco Javier Flores; Martin B. Dickman; Jeanmarie Verchot. Multiple ER‐to‐nucleus stress signaling pathways are activated during Plantago asiatica mosaic virus and Turnip mosaic virus infection in Arabidopsis thaliana. The Plant Journal 2020, 103, 1233 -1245.

AMA Style

Mathieu Gayral, Omar Arias Gaguancela, Evelyn Vasquez, Venura Herath, Francisco Javier Flores, Martin B. Dickman, Jeanmarie Verchot. Multiple ER‐to‐nucleus stress signaling pathways are activated during Plantago asiatica mosaic virus and Turnip mosaic virus infection in Arabidopsis thaliana. The Plant Journal. 2020; 103 (3):1233-1245.

Chicago/Turabian Style

Mathieu Gayral; Omar Arias Gaguancela; Evelyn Vasquez; Venura Herath; Francisco Javier Flores; Martin B. Dickman; Jeanmarie Verchot. 2020. "Multiple ER‐to‐nucleus stress signaling pathways are activated during Plantago asiatica mosaic virus and Turnip mosaic virus infection in Arabidopsis thaliana." The Plant Journal 103, no. 3: 1233-1245.

Preprint content
Published: 30 September 2019
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Summary Endoplasmic reticulum (ER) stress due to biotic or abiotic stress activates the unfolded protein response (UPR) to restore ER homeostasis. The UPR relies on multiple ER-to-nucleus signaling factors which mainly induce the expression of cytoprotective ER-chaperones. The inositol requiring enzyme (IRE1) along with its splicing target, bZIP60, restrict potyvirus, and potexvirus accumulation. Until now, the involvement of the alternative UPR pathways and the role of UPR to limit virus accumulation have remained elusive. Here, we used the Plantago asiatica mosaic virus (PlAMV) and the Turnip mosaic virus (TuMV) to demonstrate that the potexvirus triple gene block 3 (TGB3) protein and the potyvirus 6K2 protein activate the bZIP17, bZIP28, bZIP60, BAG7, NAC089 and NAC103 signaling in Arabidopsis thaliana. Using the corresponding knock-out mutant lines, we demonstrated that these factors differentially restrict local and systemic virus accumulation. We show that bZIP17, bZIP60, BAG7, and NAC089 are factors in PlAMV infection, whereas bZIP28 and bZIP60 are factors in TuMV infection. TGB3 and 6K2 transient expression in leave reveal that these alternative pathways induce BiPs expression. Finally, using dithiothreitol (DTT) and tauroursodeoxycholic acid (TUDCA) treatment, we demonstrated that the protein folding capacity significantly influences PlAMV accumulation. Together, these results indicate that multiple ER-to-nucleus signaling pathways are activated during virus infection and restrict virus accumulation through increasing protein folding capacity. Significance statement The IRE1/bZIP60 pathway of unfolded protein response (UPR) is activated by potyviruses and potexviruses, limiting their infection, but the role of alternative UPR pathways is unknown. This study reveals the activation of multiple ER-to-nucleus signaling pathways by the Plantago asiatica mosaic virus and the Turnip mosaic virus. We identify additional signaling pathways serve to restrict virus accumulation through increased protein folding capacity.

ACS Style

Mathieu Gayral; Omar Arias Gaguancela; Evelyn Vasquez; Venura Herath; Mingxiong Pang; Francisco Javier Florez; Martin B Dickman; Jeanmarie Verchot. Multiple ER-to-nucleus stress signaling pathways become active during Plantago asiatica mosaic virus and Turnip mosaic virus infection in Arabidopsis thaliana. 2019, 786137 .

AMA Style

Mathieu Gayral, Omar Arias Gaguancela, Evelyn Vasquez, Venura Herath, Mingxiong Pang, Francisco Javier Florez, Martin B Dickman, Jeanmarie Verchot. Multiple ER-to-nucleus stress signaling pathways become active during Plantago asiatica mosaic virus and Turnip mosaic virus infection in Arabidopsis thaliana. . 2019; ():786137.

Chicago/Turabian Style

Mathieu Gayral; Omar Arias Gaguancela; Evelyn Vasquez; Venura Herath; Mingxiong Pang; Francisco Javier Florez; Martin B Dickman; Jeanmarie Verchot. 2019. "Multiple ER-to-nucleus stress signaling pathways become active during Plantago asiatica mosaic virus and Turnip mosaic virus infection in Arabidopsis thaliana." , no. : 786137.

Preprint
Published: 23 July 2019
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Rose rosette virus (RRV) is an Emaravirus, a negative-sense RNA virus with a 7-segmented genome that is enclosed by a double membrane. While the genome sequences of many emaraviruses are reported, there is negligible information concerning virus replication and movement in host plants. Computational methods determined that RNA1 encoded the RNA dependent RNA polymerase (RdRp), RNA2 encoded glycoprotein precursor, and the RNA3 encoded the nucleocapsid (N), all share significant homologies with similar proteins of the Orthobunyavirus family. The RRV terminal UTR sequences are complementary and share significant identity with the UTR sequences of Bunyamwera virus. We report a minireplicon system and a full length infectious clone of RRV, which are the first for any emaravirus species. The photoreversible fluorescent iLOV protein was used to replace the RNA5 open reading frame (R5-iLOV). We demonstrate that agro-infiltration of Nicotiana benthamiana leaves to deliver RNA1, RNA3, and R5-iLOV cDNAs led to iLOV expression. A mutation was introduced into the RdRp active site and iLOV expression was eliminated. Delivery of four segments or seven segments of the RRV infectious clone produced systemic infection in N. benthamiana and rose plants. iLOV was also fused to the glycoprotein precursor (R2-iLOV). Using confocal microscopy, the R2-iLOV was seen in spherical bodies along membrane strands inside N. benthamiana epidermal cells. This new technology will enable future research to functionally characterize the RRV proteins, to study the virus-host interactions governing local and systemic infection, and examine the subcellular functions of the Gc.IMPORTANCERRV has emerged as a severe threat to cultivated roses, causing millions of dollars in losses to commercial producers. The majority of the viral gene products have not been researched or characterized until now. We constructed a minireplicon system and an infectious clone of the seven-segmented RRV genome that is contained in a binary vector and delivered by Agrobacterium. This technology has been slow to develop for viruses with negative-strand RNA genomes. It has been especially tricky for plant viruses with multicomponent negative-strand RNA genomes. We report the first reverse genetic system for a member of the genus Emaravirus, Rose rosette virus (RRV). We introduced the iLOV fluorescent protein as a fusion to the Gc protein and as a replacement for the open reading frame in genome segment 5. This game-changing reverse genetic system creates new opportunities for studying negative-strand RNA viruses in plants.

ACS Style

Jeanmarie Verchot; Venura Herath; Cesar D. Urrutia; Mathieu Gayral; Kelsey Lyle; Madalyn K. Shires; Kevin Ong; David Byrne; Mingxiong Pang. Characterization of Rose rosette virus and development of reverse genetic system for studying virus accumulation and movement in whole plants. 2019, 712000 .

AMA Style

Jeanmarie Verchot, Venura Herath, Cesar D. Urrutia, Mathieu Gayral, Kelsey Lyle, Madalyn K. Shires, Kevin Ong, David Byrne, Mingxiong Pang. Characterization of Rose rosette virus and development of reverse genetic system for studying virus accumulation and movement in whole plants. . 2019; ():712000.

Chicago/Turabian Style

Jeanmarie Verchot; Venura Herath; Cesar D. Urrutia; Mathieu Gayral; Kelsey Lyle; Madalyn K. Shires; Kevin Ong; David Byrne; Mingxiong Pang. 2019. "Characterization of Rose rosette virus and development of reverse genetic system for studying virus accumulation and movement in whole plants." , no. : 712000.

Editorial
Published: 08 July 2019 in Molecular Plant Pathology
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ACS Style

Miguel A. Aranda; Kristiina Mäkinen; Jeanmarie Verchot. Introduction to Special Issue of Molecular Plant Pathology ‐ “Extracellular and intracellular perception of plant viruses”. Molecular Plant Pathology 2019, 20, 1183 -1184.

AMA Style

Miguel A. Aranda, Kristiina Mäkinen, Jeanmarie Verchot. Introduction to Special Issue of Molecular Plant Pathology ‐ “Extracellular and intracellular perception of plant viruses”. Molecular Plant Pathology. 2019; 20 (9):1183-1184.

Chicago/Turabian Style

Miguel A. Aranda; Kristiina Mäkinen; Jeanmarie Verchot. 2019. "Introduction to Special Issue of Molecular Plant Pathology ‐ “Extracellular and intracellular perception of plant viruses”." Molecular Plant Pathology 20, no. 9: 1183-1184.

Journal article
Published: 27 July 2018 in Journal of Visualized Experiments
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This metagenome approach is used to identify plant viruses with circular DNA genomes and their transcripts. Often plant DNA viruses that occur in low titers in their host or cannot be mechanically inoculated to another host are difficult to propagate to achieve a greater titer of infectious material. Infected leaves are ground in a mild buffer with optimal pH and ionic composition recommended for purifying most bacilliform Para retroviruses. Urea is used to break up inclusion bodies that trap virions and to dissolve cellular components. Differential centrifugation provides further separation of virions from plant contaminants. Then proteinase K treatment removes the capsids. Then the viral DNA is concentrated and used for next-generation sequencing (NGS). The NGS data are used to assemble contigs which are submitted to NCBI-BLASTn to identify a subset of virus sequences in the generated dataset. In a parallel pipeline, RNA is isolated from infected leaves using a standard column-based RNA extraction method. Then ribosome depletion is carried out to enrich for a subset of mRNA and virus transcripts. Assembled sequences derived from RNA sequencing (RNA-seq) were submitted to NCBI-BLASTn to identify a subset of virus sequences in this dataset. In our study, we identified two related full-length badnavirus genomes in the two datasets. This method is preferred to another common approach which extracts the aggregate population of small RNA sequences to reconstitute plant virus genomic sequences. This latter metagenomic pipeline recovers virus related sequences that are retro-transcribing elements inserted into the plant genome. This is coupled to biochemical or molecular assays to further discern the actively infectious agents. The approach documented in this study, recovers sequences representative of replicating viruses that likely indicate active virus infection.

ACS Style

Jeanmarie Verchot; Aastha Thapa; Dulanjani Wijayasekara; Peter R. Hoyt. Combining Analysis of DNA in a Crude Virion Extraction with the Analysis of RNA from Infected Leaves to Discover New Virus Genomes. Journal of Visualized Experiments 2018, e57855 -e57855.

AMA Style

Jeanmarie Verchot, Aastha Thapa, Dulanjani Wijayasekara, Peter R. Hoyt. Combining Analysis of DNA in a Crude Virion Extraction with the Analysis of RNA from Infected Leaves to Discover New Virus Genomes. Journal of Visualized Experiments. 2018; (137):e57855-e57855.

Chicago/Turabian Style

Jeanmarie Verchot; Aastha Thapa; Dulanjani Wijayasekara; Peter R. Hoyt. 2018. "Combining Analysis of DNA in a Crude Virion Extraction with the Analysis of RNA from Infected Leaves to Discover New Virus Genomes." Journal of Visualized Experiments , no. 137: e57855-e57855.

Journal article
Published: 01 January 2018 in Virus Research
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Members of the genus Badnavirus have a single non-covalently closed circular double-stranded DNA genome of 7.2-9.2kb. The genome encodes three open reading frames (ORFs) on the positive DNA strand. Canna yellow mottle virus (CaYMV) is a badnavirus that has been described as the etiological cause of yellow mottle disease in canna, although only a 565bp fragment of the genome has been previously reported from cannas. In this report, concentrated virions were recovered from infected canna plants and nucleic acids were extracted. Two full-length sequences represent two badnavirus genomes were recovered and were determined to be 6966bp and 7385bp in length. These DNAs represent a virus strain belonging to Canna yellow mottle virus and a novel species tentatively termed Canna yellow mottle associated virus. Phylogenetic analysis indicates that these two viruses are closely related to sugarcane bacilliform GD virus, pineapple bacilliform comosus virus, banana streak MY virus, and cycad leaf necrosis virus. We also showed naturally grown canna plants to be frequently co-infected by these two badnaviruses along with a potyvirus, Canna yellow streak virus.

ACS Style

Dulanjani Wijayasekara; Peter Hoyt; Austin Gimondo; Bruce Dunn; Aastha Thapa; Hannah Jones; Jeanmarie Verchot. Molecular characterization of two badnavirus genomes associated with Canna yellow mottle disease. Virus Research 2018, 243, 19 -24.

AMA Style

Dulanjani Wijayasekara, Peter Hoyt, Austin Gimondo, Bruce Dunn, Aastha Thapa, Hannah Jones, Jeanmarie Verchot. Molecular characterization of two badnavirus genomes associated with Canna yellow mottle disease. Virus Research. 2018; 243 ():19-24.

Chicago/Turabian Style

Dulanjani Wijayasekara; Peter Hoyt; Austin Gimondo; Bruce Dunn; Aastha Thapa; Hannah Jones; Jeanmarie Verchot. 2018. "Molecular characterization of two badnavirus genomes associated with Canna yellow mottle disease." Virus Research 243, no. : 19-24.

Review
Published: 19 November 2016 in Viruses
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The endoplasmic reticulum (ER) is central to plant virus replication, translation, maturation, and egress. Ubiquitin modification of ER associated cellular and viral proteins, alongside the actions of the 26S proteasome, are vital for the regulation of infection. Viruses can arrogate ER associated ubiquitination as well as cytosolic ubiquitin ligases with the purpose of directing the ubiquitin proteasome system (UPS) to new targets. Such targets include necessary modification of viral proteins which may stabilize certain complexes, or modification of Argonaute to suppress gene silencing. The UPS machinery also contributes to the regulation of effector triggered immunity pattern recognition receptor immunity. Combining the results of unrelated studies, many positive strand RNA plant viruses appear to interact with cytosolic Ub-ligases to provide novel avenues for controlling the deleterious consequences of disease. Viral interactions with the UPS serve to regulate virus infection in a manner that promotes replication and movement, but also modulates the levels of RNA accumulation to ensure successful biotrophic interactions. In other instances, the UPS plays a central role in cellular immunity. These opposing roles are made evident by contrasting studies where knockout mutations in the UPS can either hamper viruses or lead to more aggressive diseases. Understanding how viruses manipulate ER associated post-translational machineries to better manage virus–host interactions will provide new targets for crop improvement.

ACS Style

Jeanmarie Verchot. Plant Virus Infection and the Ubiquitin Proteasome Machinery: Arms Race along the Endoplasmic Reticulum. Viruses 2016, 8, 314 .

AMA Style

Jeanmarie Verchot. Plant Virus Infection and the Ubiquitin Proteasome Machinery: Arms Race along the Endoplasmic Reticulum. Viruses. 2016; 8 (11):314.

Chicago/Turabian Style

Jeanmarie Verchot. 2016. "Plant Virus Infection and the Ubiquitin Proteasome Machinery: Arms Race along the Endoplasmic Reticulum." Viruses 8, no. 11: 314.

Research article
Published: 01 October 2016 in Molecular Plant-Microbe Interactions®
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The inositol requiring enzyme (IRE1) is an endoplasmic reticulum (ER) stress sensor. When activated, it splices the bZIP60 mRNA, producing a truncated transcription factor that upregulates genes involved in the unfolded protein response. Bax inhibitor 1 (BI-1) is another ER stress sensor that regulates cell death in response to environmental assaults. The potyvirus 6K2 and potexvirus TGB3 proteins are known to reside in the ER, serving, respectively, as anchors for the viral replicase and movement protein complex. This study used green fluorescent protein (GFP)-tagged Turnip mosaic virus (TuMV), Plantago asiatica mosaic virus (PlAMV), Potato virus Y (PVY), and Potato virus X (PVX) to determine that the IRE1/bZIP60 pathway and BI-1 machinery are induced early in virus infection in Arabidopsis thaliana, Nicotiana benthamiana, and Solanum tuberosum. Agrodelivery of only the potyvirus 6K2 or TGB3 genes into plant cells activated bZIP60 and BI-1 expression in Arabidopsis thaliana, N. benthamiana, and S. tuberosum. Homozygous ire1a-2, ire1b-4, and ire1a-2/ire1b-4 mutant Arabidopsis plants were inoculated with TuMV-GFP or PlAMV-GFP. PlAMV accumulates to a higher level in ire1a-2 or ire1a-2/ire1b-4 mutant plants than in ire1b-4 or wild-type plants. TuMV-GFP accumulates to a higher level in ire1a-2, ire1b-4, or ire1a-2/ire1b-4 compared with wild-type plants, suggesting that both isoforms contribute to TuMV-GFP infection. Gene silencing was used to knock down bZIP60 and BI-1 expression in N. benthamiana. PVX-GFP and PVY-GFP accumulation was significantly elevated in these silenced plants compared with control plants. This study demonstrates that two ER stress pathways, namely IRE1/bZIP60 and the BI-1 pathway, limit systemic accumulation of potyvirus and potexvirus infection. Silencing BI-1 expression also resulted in systemic necrosis. These data suggest that ER stress–activated pathways, led by IRE1 and BI-1, respond to invading potyvirus and potexviruses to restrict virus infection and enable physiological changes enabling plants to tolerate virus assault.

ACS Style

Omar Arias Gaguancela; Lizbeth Peña Zúñiga; Alexis Vela Arias; Dennis Halterman; Francisco Flores; Ida Elisabeth Johansen; Aiming Wang; Yasuyuki Yamaji; Jeanmarie Verchot. The IRE1/bZIP60 Pathway and Bax Inhibitor 1 Suppress Systemic Accumulation of Potyviruses and Potexviruses in Arabidopsis and Nicotiana benthamiana Plants. Molecular Plant-Microbe Interactions® 2016, 29, 750 -766.

AMA Style

Omar Arias Gaguancela, Lizbeth Peña Zúñiga, Alexis Vela Arias, Dennis Halterman, Francisco Flores, Ida Elisabeth Johansen, Aiming Wang, Yasuyuki Yamaji, Jeanmarie Verchot. The IRE1/bZIP60 Pathway and Bax Inhibitor 1 Suppress Systemic Accumulation of Potyviruses and Potexviruses in Arabidopsis and Nicotiana benthamiana Plants. Molecular Plant-Microbe Interactions®. 2016; 29 (10):750-766.

Chicago/Turabian Style

Omar Arias Gaguancela; Lizbeth Peña Zúñiga; Alexis Vela Arias; Dennis Halterman; Francisco Flores; Ida Elisabeth Johansen; Aiming Wang; Yasuyuki Yamaji; Jeanmarie Verchot. 2016. "The IRE1/bZIP60 Pathway and Bax Inhibitor 1 Suppress Systemic Accumulation of Potyviruses and Potexviruses in Arabidopsis and Nicotiana benthamiana Plants." Molecular Plant-Microbe Interactions® 29, no. 10: 750-766.

Review
Published: 01 April 2016 in Current Opinion in Virology
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The endoplasmic reticulum and Golgi network (ERGN) is vital to most cellular biosynthetic processes. Many positive strand RNA viruses depend upon the ERGN for replication, maturation, and egress. Viruses induce changes in ER architecture and stimulate fatty acid synthesis to create environments that can scaffold replication complexes, plant virus movement complexes, or virion maturation. Potato virus X (PVX) and Turnip mosaic virus (TuMV) each encode small membrane binding proteins that embed in the ERGN and activate the unfolded protein response (UPR). The UPR ensures ERGN homeostasis in the face of environmental assaults that could negatively impact the biosynthetic functions of the ERGN. This article explores the relationship between ER stress, the UPR, and membrane synthesis occurring during virus infection.

ACS Style

Jeanmarie Verchot. How does the stressed out ER find relief during virus infection? Current Opinion in Virology 2016, 17, 74 -79.

AMA Style

Jeanmarie Verchot. How does the stressed out ER find relief during virus infection? Current Opinion in Virology. 2016; 17 ():74-79.

Chicago/Turabian Style

Jeanmarie Verchot. 2016. "How does the stressed out ER find relief during virus infection?" Current Opinion in Virology 17, no. : 74-79.