Small RNA Regulators of Plant-Hemipteran Interactions: Micromanagers with Versatile Roles

Abstract

Non-coding small RNAs (sRNAs) in plants have important roles in regulating biological processes, including development, reproduction, and stress responses. Recent research indicates significant roles for sRNA-mediated gene silencing during plant-hemipteran interactions that involve all three of these biological processes. Plant responses to hemipteran feeding are determined by changes in the host transcriptome that appear to be fine-tuned by sRNAs. The role of sRNA in plant defense responses is complex. Different forms of sRNAs, with specific modes of action, regulate changes in the host transcriptome primarily through post-transcriptional gene silencing and occasionally through translational repression. Plant genetic resistance against hemipterans provides a model to explore the regulatory roles of sRNAs in plant defense. Aphid-induced sRNA expression in resistance genotypes delivers a new paradigm in understanding the regulation of R gene-mediated resistance in host plants. Unique sRNA profiles, including changes in sRNA biogenesis and expression can also provide insights into susceptibility to insect herbivores. Activation of phytohormone-mediated defense responses against insect herbivory is another hallmark of this interaction, and recent studies have shown that regulation of phytohormone signaling is under the control of sRNAs. Hemipterans feeding on resistant plants also show changes in insect sRNA profiles, possibly influencing insect development and reproduction. Changes in insect traits such as fecundity, host range, and resistance to insecticides are impacted by sRNAs and can directly contribute to the success of certain insect biotypes. In addition to causing direct damage to the host plant, hemipteran insects are often vectors of viral pathogens. Insect anti-viral RNAi machinery is activated to limit virus accumulation, suggesting a role in insect immunity. Virus-derived long sRNAs strongly resemble insect piRNAs, leading to the speculation that the piRNA pathway is induced in response to viral infection. Evidence for robust insect RNAi machinery in several hemipteran species is of immense interest and is being actively pursued as a possible tool for insect control. RNAi-induced gene silencing following uptake of exogenous dsRNA was successfully demonstrated in several hemipterans and the presence of sid-1 like genes support the concept of a systemic response in some species.

A combined microRNA and transcriptome analyses illuminates the resistance response of rice against brown planthopper

“…Few studies have reported the use of combined miRNA and mRNA expression profiles to analyze the responses of herbivore insects in plants, excluding studies on aphidinduced miRNA expression [35]. This study was the first to report the combined analysis of miRNA and mRNA expression profiles in BPH-infested rice, enhancing our understanding of the regulatory mechanisms of miRNA-mRNA in rice after BPH attack.…”

Identification and analysis of brown planthopper-responsive microRNAs in resistant and susceptible rice plants

“…Evidence is accumulating for a role of miRNAs in the plant responses to biotic stress 14 – 18 . In plant-insect interactions, aphid-induced small RNA expression has been studied in many plants 48 . This is the first report of the miRNA response to herbivore insect in rice.…”

RNA helicase domains of viral origin in proteins of insect retrotransposons: possible source for evolutionary advantages

“…A recently developed pathogen control strategy, which is called host-induced gene silencing (HIGS), is based on generating transgenic plants that express pathogen-specific dsRNA to trigger silencing of essential genes in insects, fungi and other pests ( Nunes & Dean, 2012 ; Koch & Kogel, 2014 ; Weiberg & Jin, 2015 ). Importantly, recent reports show that not only artificial transgenic HIGS dsRNAs, but also plant endogenous dsRNAs can be actively transported into insect cells; however, the functional consequences of consuming these dietary-derived plant dsRNAs for the insects remain to be clarified ( Ivashuta et al, 2015 ; Sattar & Thompson, 2016 ). The natural dsRNA transfer from plants to insects was reconstituted in numerous studies of insect feeding on substrates containing artificial insect-specific dsRNAs.…”