Abstract
BackgroundThe 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 FindingsThirty 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/SignificanceSPCSV 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.
Highlights
Sweet potato chlorotic stunt virus (SPCSV; genus Crinivirus; family Closteroviridae) is a phloem-limited virus [1], semipersistently transmitted by whiteflies [2,3] and known to occur in most areas where sweetpotatoes (Ipomoea batatas Lam.) are grown
Natural occurrence of SPCSV in wild species has not been reported, but under experimental conditions, the West African’ (WA) strain of SPCSV is able to infect two of the species
Similar observations have been made for Sweet potato mild mottle virus (SPMMV; genus Ipomovirus; Potyviridae) [35] and Sweet potato feathery mottle virus (SPFMV) [29] in the wild species of Convolvulaceae and cultivated sweetpotatoes in Uganda, Rice yellow mottle virus (RYMV; genus Sobemovirus) in cultivated rice and wild graminaceous species in East, Central and West Africa [36], and African cassava mosaic virus and East African cassava mosaic cameroon virus in cassava and various wild hosts in west Africa [37]
Summary
Sweet potato chlorotic stunt virus (SPCSV; genus Crinivirus; family Closteroviridae) is a phloem-limited virus [1], semipersistently transmitted by whiteflies [2,3] and known to occur in most areas where sweetpotatoes (Ipomoea batatas Lam.) are grown. 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. SPCSV isolates lacking p22 synergized with Sweet potato feathery mottle virus (SPFMV, genus potyvirus; Potyviridae) and caused severe symptoms in co-infected sweetpotato plants. A new whiteflytransmitted virus (KML33b) encoding an RNase homolog (
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