Small Talk: On the Possible Role of Trans-Kingdom Small RNAs during Plant–Virus–Vector Tritrophic Communication

Small RNAs (sRNAs) are the hallmark and main effectors of RNA silencing and therefore are involved in major biological processes in plants, such as regulation of gene expression, antiviral defense, and plant genome integrity. The mechanisms of sRNA amplification as well as their mobile nature and rapid generation suggest sRNAs as potential key modulators of intercellular and interspecies communication in plant-pathogen–pest interactions. Plant endogenous sRNAs can act in cis to regulate plant innate immunity against pathogens, or in trans to silence pathogens’ messenger RNAs (mRNAs) and impair virulence. Likewise, pathogen-derived sRNAs can act in cis to regulate expression of their own genes and increase virulence towards a plant host, or in trans to silence plant mRNAs and interfere with host defense. In plant viral diseases, virus infection alters the composition and abundance of sRNAs in plant cells, not only by triggering and interfering with the plant RNA silencing antiviral response, which accumulates virus-derived small interfering RNAs (vsiRNAs), but also by modulating plant endogenous sRNAs. Here, we review the current knowledge on the nature and activity of virus-responsive sRNAs during virus–plant interactions and discuss their role in trans-kingdom modulation of virus vectors for the benefit of virus dissemination.