Comprehensive Transcriptome Analyses Reveal that Potato Spindle Tuber Viroid Triggers Genome-Wide Changes in Alternative Splicing, Inducibletrans-Acting Activity of Phased Secondary Small Interfering RNAs, and Immune Responses.
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 thetrans-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.IMPORTANCENumerous 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.
Boyce Thompson Institute, Cornell University, Ithaca, New York, USA.
Yi
Y
Zheng
Department of Molecular Genetics, The Ohio State University, Columbus, Ohio, USA wang@biology.msstate.edu zf25@cornell.edu.|Department of Biological Sciences, Mississippi State University, Mississippi State, Mississippi, USA.
Ying
http://orcid.org/0000-0002-9659-977X
Y
Wang
Department of Molecular Genetics, The Ohio State University, Columbus, Ohio, USA.
Biao
B
Ding
Boyce Thompson Institute, Cornell University, Ithaca, New York, USA wang@biology.msstate.edu zf25@cornell.edu.|USDA Robert W. Holley Center for Agriculture and Health, Ithaca, New York, USA.
Zhangjun
http://orcid.org/0000-0001-9684-1450
Z
Fei
D017398:Alternative Splicing; D020869:Gene Expression Profiling; D005786:Gene Expression Regulation; D016679:Genome, Viral; D006728:Hormones / Q000378:metabolism; D054884:Host-Pathogen Interactions / Q000276:immunology; D018551:Solanum lycopersicum / Q000276:immunology / Q000502:physiology / Q000821:virology*; D035683:MicroRNAs; D020928:Mitogen-Activated Protein Kinases / Q000235:genetics; D010935:Plant Diseases / Q000276:immunology* / Q000821:virology; D018515:Plant Leaves / Q000821:virology; D011494:Protein Kinases / Q000235:genetics; D034741:RNA, Small Interfering / Q000235:genetics*; D012367:RNA, Viral / Q000235:genetics; D015398:Signal Transduction; D011198:Solanum tuberosum / Q000821:virology; D014772:Viroids / Q000235:genetics*; D017871:Calcium-Calmodulin-Dependent Protein Kinases
D006728:Hormones; D035683:MicroRNAs; D020928:Mitogen-Activated Protein Kinases; D011494:Protein Kinases; D034741:RNA, Small Interfering; D012367:RNA, Viral; D017871:Calcium-Calmodulin-Dependent Protein Kinases
Viroid; alternative splicing; immune responses; inducible phasiRNA; noncoding RNA