Abstract
Plant microRNAs (miRNAs) have recently been reported to be involved in the cross-kingdom regulation of specific cellular and physiological processes in animals. However, little of this phenomenon is known for the communication between host plant and insect herbivore. In this study, the plant-derived miRNAs in the hemolymph of a cruciferous specialist Plutella xylostella were identified by small RNAs sequencing. A total of 39 miRNAs with typical characteristics of plant miRNAs were detected, of which 24 had read counts ≥ 2 in each library. Three plant-derived miRNAs with the highest read counts were validated, and all of them were predicted to target the hemocyanin domains-containing genes of P. xylostella. The luciferase assays in the Drosophila S2 cell demonstrated that miR159a and novel-7703-5p could target BJHSP1 and PPO2 respectively, possibly in an incomplete complementary pairing mode. We further found that treatment with agomir-7703-5p significantly influenced the pupal development and egg-hatching rate when reared on the artificial diet. The developments of both pupae and adults were severely affected upon their transfer to Arabidopsis thaliana, but this might be independent of the cross-kingdom regulation of the three plant-derived miRNAs on their target genes in P. xylostella, based on expression analysis. Taken together, our work reveals that the plant-derived miRNAs could break the barrier of the insect mid-gut to enter the circulatory system, and potentially regulate the development of P. xylostella. Our findings provide new insights into the co-evolution of insect herbivore and host plant, and novel direction for pest control using plant-derived miRNAs.
Highlights
MicroRNAs are small non-coding RNAs of 19–24 nucleotides [1]
A total of 39 miRNAs, including 33 previously-reported and 6 novel sequences from the larval hemolymph of P. xylostella were well aligned to the genome of Arabidopsis thaliana (Table 1)
The results showed that the levels of miR159a, miR166a-3p and novel-7703-5p strain, except for BJHSP1, which was expressed at a higher level in the 4th instar larvae of the G88 strain in leaves damaged by P. xylostella were significantly reduced as compared with that of fresh intact (Figure 7B–D)
Summary
MicroRNAs (miRNAs) are small non-coding RNAs of 19–24 nucleotides [1]. In both animals and plants, miRNAs play an important role in post-transcriptional regulation by interacting with target mRNAs involved in cell differentiation, apoptosis, metabolism and response to environmental stress [2]. Proteins participating in the biogenesis of miRNAs differ between plants and animals [4,5] with 20 -O-methylation at 30 end by the methyltransferase Hua enhancer 1 (HEN1) being involved in plants [6]. It has been reported that plant miRNAs are able to pass through the strict gastrointestinal barrier of animals when ingested, circulating in the blood, and eventually exerting biological functions by regulating gene expression in various tissues or cells [8,9,10,11]. MiRNA-mediated cross-kingdom communication has been first reported in mammalian liver, where rice-derived miR168a alters the physiological status of mice via its regulating of the low-density lipoprotein receptor adapter protein 1
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