Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: December 18, 2011
Publication Date: April 15, 2012
Citation: Owens, R.A., Tech, K.B., Shao, J.Y., Sano, T., Baker, C.J. 2012. Global analysis of tomato gene expression during potato spindle tuber viroid infection reveals a complex array of changes affecting hormone signaling. Molecular Plant-Microbe Interactions. 25:582-598. Interpretive Summary: Viroids are the smallest known agents of infectious disease – small, highly structured, circular RNA molecules that encode no protein yet are able to cause very serious disease symptoms in susceptible crop plant species. How viroids are able to do this is unknown, but a phenomenon known as “RNA silencing” is believed to play an important role. In these studies we have monitored the levels of two types of host RNA in tomato plants infected by potato spindle tuber viroid (PSTVd), namely the messenger RNAs that are translated into proteins and small, regulatory RNAs known as “mi(cro)RNAs”. Our results show that i) PSTVd infection has a dramatic effect on many different aspects of tomato metabolism including hormone signaling and ii) changes in host miRNA levels associated with infection may explain the differences in disease severity observed in different tomato varieties. Plant breeders currently lack known sources of resistance that can be used to protect crops against the diseases caused by viroids. Our studies provide the first detailed insight into how viroids cause disease, thereby suggesting possible ways in which breeders might possibly create novel sources of resistance by altering one (or more) of the host pathways involved in the disease process. As currently presented, our results will be of greatest interest to researchers in the plant pathology and plant molecular biology research communities.
Technical Abstract: Viroids are the smallest known agents of infectious disease – small, single-stranded, highly structured, circular RNAs that lack detectable messenger RNA activity yet are able to replicate autonomously in susceptible plant species. Potato spindle tuber viroid (PSTVd) infection in tomato is accompanied by a wide variety of symptoms indicative of altered hormone metabolism, but just how these non-coding RNAs induce such a strong host response is unclear. To better understand what role RNA silencing may play in PSTVd pathogenicity we have used a combination of microarray analysis and large-scale RNA sequence analysis to compare the changes in tomato gene expression and miRNA levels associated with PSTVd infection in two cultivars plus a transformed line expressing small PSTVd siRNAs in the absence of viroid replication. The changes in mRNA levels detected were extensive, involving as many as one quarter of the ca. 10,000 genes present on the array for the sensitive cultivar Rutgers. Stimulation of ubiquitin-mediated protein catabolism and inhibition of chloroplast biogenesis was observed in both sensitive and tolerant cultivars; ribosome synthesis, in contrast, increased only in the infected Rutgers plants. Effects on several hormone signaling pathways were also detected and varied with host genotype. PSTVd infection was also shown to be accompanied by dramatic, cultivar-specific changes in levels of several host miRNAs. MiR159 is a known homeostatic regulator of gibberellin signaling, and it seems possible that accumulation of this (or other) miRNAs in tolerant tomato cultivars following PSTVd infection may block the appearance of disease symptoms such as stunting observed in sensitive cultivars.