Repressed expression of nucleoporins and importins impairs plant defense against an infectious noncoding RNA
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Viroids are a group of infectious noncoding RNAs that cause substantial crop diseases. Previous studies showed that both RNA silencing and plant immunity play defense roles against viroid infection. However, viroids can still achieve successful systemic infection in hosts. The underlying mechanism remains elusive. Through comparing proteomics profiles from mock and infected tomato samples, we unexpectedly observed a systematic reduction of proteins factors involved in nuclear pore complex and nuclear transport receptors. This fortuitous observation was confirmed in subsequent analyses and led us to discover the impaired NPR1 (NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1) nuclear import in infected samples. Transgenically increasing NPR1 expression in tomato plants or exogenously application of salicylic acid analog repressed potato spindle tuber viroid (PSTVd) infection. Altogether, our finding pinpoints the repressed expression of host nuclear transport receptors and nucleoporins as the mechanism limiting the effectiveness of plant defense against viroid, which significantly advances the understanding of plant-pathogen interactions.
Significance Statement
Viroids represent a mysterious group of pathogens. Plant-viroid interactions have not been well understood. Here, we report a fortuitous observation of a wide range of protein level reductions in nucleoporins and nuclear transport receptors upon potato spindle tuber viroid (PSTVd) infection. This reduction impairs the nuclear import of a key immune factor, NPR1. Based on this finding, we increased the expression of NPR1 protein in plants or used a salicylic acid analog (acibenzolar-S-methyl/ASM) to elevate NPR1 activity, both of which limited the infection potato spindle tuber viroid. Notably, spraying ASM to prevent PSTVd infection provides the first practical measure against this internationally controlled agent.
