Potato Virus Y Infection Alters Small RNA Metabolism and Immune Response in Tomato

Abstract

Potato virus Y (PVY) isolate PVYC-to induces growth reduction and foliar symptoms in tomato, but new vegetation displays symptom recovery at a later stage. In order to investigate the role of micro(mi)RNA and secondary small(s)RNA-regulated mechanisms in tomato defenses against PVY, we performed sRNA sequencing from healthy and PVYC-to infected tomato plants at 21 and 30 days post-inoculation (dpi). A total of 792 miRNA sequences were obtained, among which were 123 canonical miRNA sequences, many isomiR variants, and 30 novel miRNAs. MiRNAs were mostly overexpressed in infected vs. healthy plants, whereas only a few miRNAs were underexpressed. Increased accumulation of isomiRs was correlated with viral infection. Among miRNA targets, enriched functional categories included resistance (R) gene families, transcription and hormone factors, and RNA silencing genes. Several 22-nt miRNAs were shown to target R genes and trigger the production of 21-nt phased sRNAs (phasiRNAs). Next, 500 phasiRNA-generating loci were identified, and were shown to be mostly active in PVY-infected tissues and at 21 dpi. These data demonstrate that sRNA-regulated host responses, encompassing miRNA alteration, diversification within miRNA families, and phasiRNA accumulation, regulate R and disease-responsive genes. The dynamic regulation of miRNAs and secondary sRNAs over time suggests a functional role of sRNA-mediated defenses in the recovery phenotype.

Plant Molecular Responses to Potato Virus Y: A Continuum of Outcomes from Sensitivity and Tolerance to Resistance

“…The dynamic regulation of miRNAs and secondary sRNAs was also observed in late responses of tomato to PVY C , which suggested a functional role of sRNA-mediated defenses in the recovery phenotype [112], which is an inducible form of tolerance.…”

Novel targets for engineering Physostegia chlorotic mottle and tomato brown rugose fruit virus-resistant tomatoes: in silico prediction of tomato microRNA targets

“…miR171b-3p was predicted to target SGN-E745132, an uncharacterized protein coding gene ( Feng et al, 2014 ). In PVY-infected tomato plants, miR171b-3p was also accumulated and was not detected in healthy plants ( Prigigallo et al, 2019 ).…”

“…miR168a-3p regulates the expression of the ethylene receptor (Wang et al, 2017b;Wang et al, 2017a). miR168a-3p was repressed under drought stress, up-regulated in ToLCV-resistant tomato cv LA1777 and accumulated in potato virus Y (PVY)-infected tomato plants (Liu et al, 2018;Tripathi et al, 2018;Prigigallo et al, 2019). miR171b-3p was predicted to target SGN-E745132, an uncharacterized protein coding gene (Feng et al, 2014).…”

“…miR171b-3p was predicted to target SGN-E745132, an uncharacterized protein coding gene (Feng et al, 2014). In PVY-infected tomato plants, Full-size DOI: 10.7717/peerj.10096/ fig-3 miR171b-3p was also accumulated and was not detected in healthy plants (Prigigallo et al, 2019). miR319c-3p is involved in plant development and abiotic stress response (Shi et al, 2019).…”

“…It targets members of the DCL2 family, i.e., DCL2a, DCL2b, and DCL2d (Wang et al, 2018b). It has been demonstrated that miR6026 is also up-regulated in PVY-infected plants (Prigigallo et al, 2019). Moreover, miR6026 is also up-regulated in tomato roots inoculated with P. chlamydosporia endophytic hyphomycetes (Pentimone et al, 2018).…”