Comprehensive Transcriptome Analyses Reveal that Potato Spindle Tuber Viroid Triggers Genome-Wide Changes in Alternative Splicing, Inducible trans -Acting Activity of Phased Secondary Small Interfering RNAs, and Immune Responses

Abstract

Many pathogens express noncoding RNAs (ncRNAs) during infection processes. In the most extreme case, pathogenic ncRNAs alone (such as viroids) can infect eukaryotic organisms, leading to diseases. While a few pathogenic ncRNAs have been implicated in regulating gene expression, the functions of most pathogenic ncRNAs in host-pathogen interactions remain unclear. Here, we employ potato spindle tuber viroid (PSTVd) infecting tomato as a system to dissect host interactions with pathogenic ncRNAs, using comprehensive transcriptome analyses. We uncover various new activities in regulating gene expression during PSTVd infection, such as genome-wide alteration in alternative splicing of host protein-coding genes, enhanced guided-cleavage activities of a host microRNA, and induction of the -acting function of phased secondary small interfering RNAs. Furthermore, we reveal that PSTVd infection massively activates genes involved in plant immune responses, mainly those in the calcium-dependent protein kinase and mitogen-activated protein kinase cascades, as well as prominent genes involved in hypersensitive responses, cell wall fortification, and hormone signaling. Intriguingly, our data support a notion that plant immune systems can respond to pathogenic ncRNAs, which has broad implications for providing new opportunities for understanding the complexity of immune systems in differentiating "self" and "nonself," as well as lay the foundation for resolving the long-standing question regarding the pathogenesis mechanisms of viroids and perhaps other infectious RNAs. Numerous pathogens, including viruses, express pathogenic noncoding transcripts during infection. In the most extreme case, pathogenic noncoding RNAs alone (i.e., viroids) can cause disease in plants. While some work has demonstrated that pathogenic noncoding RNAs interact with host factors for function, the biological significance of pathogenic noncoding RNAs in host-pathogen interactions remains largely unclear. Here, we apply comprehensive genome-wide analyses of plant-viroid interactions and discover several novel molecular activities underlying nuclear-replicating viroid infection processes in plants, including effects on the expression and function of host noncoding transcripts, as well as the alternative splicing of host protein-coding genes. Importantly, we show that plant immunity is activated upon infection of a nuclear-replicating viroid, which is a new concept that helps to understand viroid-based pathogenesis. Our finding has broad implications for understanding the complexity of host immune systems and the diverse functions of noncoding RNAs.

Deep RNA Sequencing Reveals a Repertoire of Human Fibroblast Circular RNAs Associated with Cellular Responses to Herpes Simplex Virus 1 Infection

“…This remodeling effect of the virus on the host transcriptome is a common strategy exploited by the virus in hostvirus interactions and has been observed in various viruses [48][49][50]. Notably, a recent study showed that HSV-1 infection could not only result in changes in gene expression but also in alternative polyadenylation and splicing in the host transcriptome by influencing the host RNA processing [51]. However, several concerns about the alteration of RNA transcripts at the whole-transcriptome level, as a result of HSV-1 infection, especially the circular RNA transcriptome, have not yet been elucidated.…”

Transcriptomic Analysis Reveals Cu/Zn SODs Acting as Hub Genes of SODs in Hylocereus undatus Induced by Trypsin during Storage

“…It has been confirmed that trypsin significantly impacts on the free radical scavenging activities of flavonoids [8]. Our previous results also showed that trypsin scavenges superoxide anions (O 2 • − ) and protects cells [9].In the area of phytopathology, transcriptomic analysis has been successful used on lots of plants [10][11][12][13]. However, few of transcriptomic works have been focused on the preservation of fruits.…”

Impaired expression of chloroplast HSP90C chaperone activates plant defense responses leading to a disease symptom-like phenotype

“…Exploiting the advantage in the present study, we explored the early molecular changes leading to the development of chlorosis using RNA-seq analysis. Although studies have shown the transcriptome changes in virus- and viroid-infected plants (Mochizuki et al ., 2014; Xia et al ., 2017; Zheng et al ., 2017), the strength of the present study is that we could detect any changes that precede detectable chlorosis.…”