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An atypical RNA silencing suppression strategy provides a snapshot of the evolution of sweet potato-infecting potyviruses.

ABSTRACT: Plant viruses usually encode proteins with RNA silencing suppression (RSS) activity to counteract plant defenses. In Potyvirus, the largest genus in the family Potyviridae, this role is taken over by the multifunctional HCPro, also involved in aphid transmission, polyprotein processing and virion formation. Recently, the large P1 of Sweet potato feathery mottle virus (SPFMV) was characterized finding an extra ORF produced after polymerase slippage, which originates the product P1N-PISPO. Transient expression assays showed that SPFMV P1 and P1N-PISPO presented RSS activity, while HCPro did not. In this work, we analyze possible differences between HCPro of SPFMV and other potyviruses, testing HCPro RSS activity in a transient expression assay, and using a Plum pox virus-based system to test the ability of SPFMV P1N-PISPO and HCPro to serve as RNA silencing suppressors in the context of a viral infection. Our results indicate that not only P1 and P1N-PISPO, but also HCPro display RSS activity when expressed in a suitable context, stressing the importance of the selected experimental system for testing anti-silencing capacity of proteins. The presence of multiple viral silencing suppressors in SPFMV adds complexity to an already intricate RSS system, and provides insight into the hypothetical evolution of sweet potato-infecting potyvirids.

SUBMITTER: Rodamilans B

PROVIDER: S-EPMC6206096 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND:The bipartite single-stranded RNA genome of Sweet potato chlorotic stunt virus (SPCSV, genus Crinivirus; Closteroviridae) encodes a Class 1 RNase III (RNase3), a putative hydrophobic protein (p7) and a 22-kDa protein (p22) from genes located in RNA1. RNase3 and p22 suppress RNA silencing, the basal antiviral defence mechanism in plants. RNase3 is sufficient to render sweetpotato (Ipomoea batatas) virus-susceptible and predisposes it to development of severe diseases following infection with unrelated virus. The incidence, strains and gene content of SPCSV infecting wild plant species have not been studied. METHODOLOGY/PRINCIPAL FINDINGS:Thirty SPCSV isolates were characterized from 10 wild Ipomoea species, Hewittia sublobata or Lepistemon owariensis (family Convolvulaceae) in Uganda and compared with 34 local SPCSV isolates infecting sweetpotatoes. All isolates belonged to the East African (EA) strain of SPCSV and contained RNase3 and p7, but p22 was not detected in six isolates. The three genes showed only limited genetic variability and the proteins were under purifying selection. SPCSV isolates lacking p22 synergized with Sweet potato feathery mottle virus (SPFMV, genus potyvirus; Potyviridae) and caused severe symptoms in co-infected sweetpotato plants. One SPCSV isolate enhanced accumulation of SPFMV, but no severe symptoms developed. A new whitefly-transmitted virus (KML33b) encoding an RNase3 homolog (<56% identity to SPCSV RNase3) able to suppresses sense-mediated RNA silencing was detected in I. sinensis. CONCLUSIONS/SIGNIFICANCE:SPCSV isolates infecting wild species and sweetpotato in Uganda were genetically undifferentiated, suggesting inter-species transmission of SPCSV. Most isolates in Uganda contained p22, unlike SPCSV isolates characterized from other countries and continents. Enhanced accumulation of SPFMV and increased disease severity were found to be uncoupled phenotypic outcomes of RNase3-mediated viral synergism in sweetpotato. A second virus encoding an RNase3-like RNA silencing suppressor was detected. Overall, results provided many novel and important insights into evolutionary biology of SPCSV.

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An atypical RNA silencing suppression strategy provides a snapshot of the evolution of sweet potato-infecting potyviruses.

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