A Land Plant-Specific Transcription Factor Directly Enhances Transcription of a Pathogenic Noncoding RNA Template by DNA-Dependent RNA Polymerase II

Wang, Ying; Qu, Jie; Ji, Shaoyi; Wallace, Andrew; Wu, Jian; Li, Yang; Gopalan, Venkat; Ding, Biao

doi:10.1105/tpc.16.00100

Cited by 63 publications

(112 citation statements)

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“…Their RNAs form rod-shaped secondary structures but likely lack ribozyme activities (2,16). Potato spindle tuber viroid (PSTVd) requires a unique splicing variant of transcription factor IIIA (TFIIIA-7ZF) to replicate by Pol II (17) and optimizes expression of TFIIIA-7ZF through a direct interaction with a TFIIIA splicing regulator (ribosomal protein L5, a negative regulator of viroid replication) (18). The molecular basis of viroid pathogenicity is not fully understood, although some mechanisms have been suggested, including the down-regulation of host gene expression via RNA silencing-mediated degradation guided by viroid-derived small RNAs (19)(20)(21).…”

mentioning

confidence: 99%

Symptomatic plant viroid infections in phytopathogenic fungi

Wei

Bian

Andika

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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Viroids are pathogenic agents that have a small, circular noncoding RNA genome. They have been found only in plant species; therefore, their infectivity and pathogenicity in other organisms remain largely unexplored. In this study, we investigate whether plant viroids can replicate and induce symptoms in filamentous fungi. Seven plant viroids representing viroid groups that replicate in either the nucleus or chloroplast of plant cells were inoculated to three plant pathogenic fungi, Cryphonectria parasitica, Valsa mali, and Fusarium graminearum. By transfection of fungal spheroplasts with viroid RNA transcripts, each of the three, hop stunt viroid (HSVd), iresine 1 viroid, and avocado sunblotch viroid, can stably replicate in at least one of those fungi. The viroids are horizontally transmitted through hyphal anastomosis and vertically through conidia. HSVd infection severely debilitates the growth of V. mali but not that of the other two fungi, while in F. graminearum and C. parasitica, with deletion of dicer-like genes, the primary components of the RNA-silencing pathway, HSVd accumulation increases. We further demonstrate that HSVd can be bidirectionally transferred between F. graminearum and plants during infection. The viroids also efficiently infect fungi and induce disease symptoms when the viroid RNAs are exogenously applied to the fungal mycelia. These findings enhance our understanding of viroid replication, host range, and pathogenicity, and of their potential spread to other organisms in nature.plant viroid | fungus | transmission | pathogenicity V iroids are infectious pathogenic agents possessing small, nonencapsidated, circular single-stranded RNAs that, to date, have been found to naturally infect only plants (1, 2). Viroids infect a wide variety of higher plant species, causing devastating diseases in many crops, particularly vegetables, fruits, and ornamental plants (3). In crop plants, viroids are known to spread by vegetative propagation; by mechanical agricultural practices; and, in certain cases, through seeds, pollen, and insect transmission (3, 4). As viroids do not encode any proteins and do not require a helper agent for their multiplication and survival, the biological activities of viroids are entirely dependent on direct interactions of their RNA genome or its derivatives with cellular host components (5-9). Viroid replication or processing of its RNAs in the yeast, Saccharomyces cerevisiae, and cyanobacterium, Nostoc (Nostocales), have been demonstrated (10-12).Currently, at least 34 viroid species have been identified and are classified into two families, Avsunviroidae and Pospiviroidae (13-15). The members of Avsunviroidae (type species: Avocado sunblotch viroid) replicate in the chloroplasts or plastids through symmetric rolling-circle replication using the host nuclear-encoded polymerase. Their RNAs form highly branched secondary structures and have ribozyme activities. Members of Pospiviroidae (type species: Potato spindle tuber viroid) replicate and accumulate in the nucleus th...

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mentioning

confidence: 99%

Symptomatic plant viroid infections in phytopathogenic fungi

Wei

Bian

Andika

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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“…Viroids are circular noncoding RNAs that infect crop plants, often leading to plant disease (Ding, 2009, Flores et al, 2014. As infectious noncoding RNAs, viroids have been a productive model to dissect plant defense mechanisms against invasive RNAs (Itaya et al, 2007, St-Pierre et al, 2009, Zheng et al, 2017, the role of RNA three-dimensional motifs in regulating RNA systemic trafficking (Ding, 2009, and RNA-templated RNA replication by DNA-dependent RNA polymerase II (Pol II) (Rackwitz et al, 1981, Wang et al, 2016. Recent progress has begun to elucidate how viroids co-opt cellular factors to effectively propagate themselves (Flores et al, 2005, Ding, 2009, Nohales et al, 2012a, Nohales et al, 2012b, Minoia et al, 2014, Katsarou et al, 2016, Wang et al, 2016, Dissanayaka Mudiyanselage et al, 2018, Jiang et al, 2018.…”

Section: Discussionmentioning

confidence: 99%

“…PSTVd, and viroids in family Pospiviroidae, employ Pol II for transcription (Rackwitz et al, 1981). A splicing variant of TFIIIA (TFIIIA-7ZF) facilitates Pol II-catalyzed transcription using PSTVd RNA template (Wang et al, 2016). Interestingly, the splicing of TFIIIA transcripts is regulated through a direct interaction between PSTVd and ribosomal protein L5 (RPL5), which results in optimal expression of TFIIIA-7ZF favoring PSTVd transcription (Jiang et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

A simple method to co-purify genomic DNA, RNA, and proteins for functional studies

Jiang

et al. 2018

Preprint

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Understanding the regulation of gene expression, from the epigenetic modifications on genomes to posttranscriptional and translational controls, are critical for elucidating molecular mechanisms underlying distinct phenotypes in biology. With the rapid development of Multi-Omics analyses, it is desirable to minimize sample variations by using DNA, RNA, and proteins co-purified from the same samples. Currently, most of the co-purification protocols rely on Tri Reagent (Trizol as a common representative) and require protein precipitation and dissolving steps, which render difficulties in experimental handling and high-throughput analyses. Here, we established a simple and robust method to minimize the precipitation steps and yield ready-to-use RNA and protein in solutions.This method can be applied to samples in small quantity, such as protoplasts. We demonstrated that the protoplast system equipped with this method may facilitate studies on viroid biogenesis. Given the ease and the robustness of this new method, it will have broad applications for plant research and other disciplines in molecular biology. 42 31 24 15 Kda FL RIPA Su RIPA 11 93 72 53 42 31 24 15 Kda

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“…This is further supported by the findings where N. benthamiana canonical 9‐zinc finger (ZF) Transcription Factor IIIA (TFIIIA‐9ZF) and its variant TFIIIA‐7ZF interacted with (+) strand of PSTVd whereas only TFIIIA‐7ZF found to interact with (−) strand of PSTVd. In planta experiments revealed that the expression of TFIIIA‐7ZF directly correlates with PSTVd replication (Wang et al, ). More recently, in vitro and in vivo studies revealed that, PSTVd favor the expression of TFIIIA‐7ZF, thereby promoting its replication by directly interacting with a splicing regulator, RPL5 with CCR, which is critical for PSTVd replication (Dissanayaka Mudiyanselage, Qu, Tian, Jiang, & Wang, ; Jiang et al, ).…”

Section: Viroid Pathogenicity and Host Componentsmentioning

confidence: 99%

Current overview on viroid–host interactions

Adkar-Purushothama

Perreault

2019

WIREs RNA

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Viroids are one of the most enigmatic highly structured, circular, single‐stranded RNA phytopathogens. Although they are not known to code for any peptide, viroids induce visible symptoms in susceptible host plants that resemble those associated with many plant viruses. It is known that viroids induce disease symptoms by direct interaction with host factors; however, the precise mechanism by which this occurs remains poorly understood. Studies on the host's responses to viroid infection, host susceptibility and nonhost resistance have been underway for several years, but much remains to be done in order to fully understand the complex nature of viroid–host interactions. Recent progress using molecular biology techniques combined with computational algorithms, in particular evidence of the role of viroid‐derived small RNAs in the RNA silencing pathways of a disease network, has widened the knowledge of viroid pathogenicity. The complexity of viroid–host interactions has been revealed in the past decades to include, but not be limited to, the involvement of host factors, viroid structural complexity, and viroid‐induced ribosomal stress, which is further boosted by the discovery of long noncoding RNAs (lncRNAs). In this review, the current understanding of the viroid–host interaction has been summarized with the goal of simplifying the complexity of viroid biology for future research. This article is categorized under: RNA in Disease and Development > RNA in Disease

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A Land Plant-Specific Transcription Factor Directly Enhances Transcription of a Pathogenic Noncoding RNA Template by DNA-Dependent RNA Polymerase II

Cited by 63 publications

References 57 publications

Symptomatic plant viroid infections in phytopathogenic fungi

Symptomatic plant viroid infections in phytopathogenic fungi

A simple method to co-purify genomic DNA, RNA, and proteins for functional studies

Current overview on viroid–host interactions

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