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Open AccessArticle

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

1
Consiglio Nazionale delle Ricerche, Istituto per la Protezione Sostenibile delle Piante, G. Via Amendola 122/D, 70126 Bari, Italy
2
National Institute of Biology, Department of Biotechnology and Systems Biology, Večna pot 111, 1000 Ljubljana, Slovenia
3
Consiglio Nazionale delle Ricerche, Istituto di Bioscienze e BioRisorse, Via G. Amendola 165/A, 70126 Bari, Italy
4
Consiglio Nazionale delle Ricerche, Istituto di Tecnologie Biomediche, Via G. Amendola 122/D, 70126 Bari, Italy
*
Authors to whom correspondence should be addressed.
These authors contributed equally to this work.
Viruses 2019, 11(12), 1100; https://doi.org/10.3390/v11121100
Received: 25 October 2019 / Revised: 19 November 2019 / Accepted: 24 November 2019 / Published: 27 November 2019
(This article belongs to the Special Issue The Complexity of the Potyviral Interaction Network)
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.
Keywords: RNA silencing; plant defense response; Solanum lycopersicum; Potato virus Y; molecular plant-virus interactions; microRNA; secondary small interfering RNA; phasiRNA; small RNA sequencing RNA silencing; plant defense response; Solanum lycopersicum; Potato virus Y; molecular plant-virus interactions; microRNA; secondary small interfering RNA; phasiRNA; small RNA sequencing
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MDPI and ACS Style

Prigigallo, M.I.; Križnik, M.; Paola, D.D.; Catalano, D.; Gruden, K.; Finetti-Sialer, M.M.; Cillo, F. Potato Virus Y Infection Alters Small RNA Metabolism and Immune Response in Tomato. Viruses 2019, 11, 1100.

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