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. 2019 Jul 17;93(15):e00488-19.
doi: 10.1128/JVI.00488-19. Print 2019 Aug 1.

Transmission of a New Polerovirus Infecting Pepper by the Whitefly Bemisia tabaci

Saptarshi Ghosh  1 , Surapathrudu Kanakala  1 , Galina Lebedev  1 , Svetlana Kontsedalov  1 , David Silverman  2 , Tamar Alon  2 , Neta Mor  2 , Noa Sela  3 , Neta Luria  3 , Aviv Dombrovsky  3 , Munir Mawassi  3 , Sabrina Haviv  3 , Henryk Czosnek  4 , Murad Ghanim  5
Affiliations

Transmission of a New Polerovirus Infecting Pepper by the Whitefly Bemisia tabaci

Saptarshi Ghosh et al. J Virol. .

Abstract

Many animal and plant viruses depend on arthropods for their transmission. Virus-vector interactions are highly specific, and only one vector or one of a group of vectors from the same family is able to transmit a given virus. Poleroviruses (Luteoviridae) are phloem-restricted RNA plant viruses that are exclusively transmitted by aphids. Multiple aphid-transmitted polerovirus species commonly infect pepper, causing vein yellowing, leaf rolling, and fruit discoloration. Despite low aphid populations, a recent outbreak with such severe symptoms in many bell pepper farms in Israel led to reinvestigation of the disease and its insect vector. Here we report that this outbreak was caused by a new whitefly (Bemisia tabaci)-transmitted polerovirus, which we named Pepper whitefly-borne vein yellows virus (PeWBVYV). PeWBVYV is highly (>95%) homologous to Pepper vein yellows virus (PeVYV) from Israel and Greece on its 5' end half, while it is homologous to African eggplant yellows virus (AeYV) on its 3' half. Koch's postulates were proven by constructing a PeWBVYV infectious clone causing the pepper disease, which was in turn transmitted to test pepper plants by B. tabaci but not by aphids. PeWBVYV represents the first report of a whitefly-transmitted polerovirus.IMPORTANCE The high specificity of virus-vector interactions limits the possibility of a given virus changing vectors. Our report describes a new virus from a family of viruses strictly transmitted by aphids which is now transmitted by whiteflies (Bemisia tabaci) and not by aphids. This report presents the first description of polerovirus transmission by whiteflies. Whiteflies are highly resistant to insecticides and disperse over long distances, carrying virus inoculum. Thus, the report of such unusual polerovirus transmission by a supervector has extensive implications for the epidemiology of the virus disease, with ramifications concerning the international trade of agricultural commodities.

Keywords: Bemisia tabaci; aphid; circulative; polerovirus; transmission.

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Figures

FIG 1
FIG 1
Symptoms caused by the newly identified PeWBVYV in pepper. The major damage is the discoloration of the fruits, as shown in panels B and D, compared to normal fruits (A), as well as the reduction in fruit size and change in fruit shape (D). (C) Infected plants with leaves showing yellowing and upward curling and stunted growth compared to the normal green leaves.
FIG 2
FIG 2
(A to C) Raw results of transmission of PeWBVYV as determined by RT-PCR from plants given an inoculation access period of 48 h with 10 viruliferous whiteflies per plant using clip cages in three replicates, with 15 plants each. Panels A, B, and C represent the first, second, and third replicates, respectively. “C1” and “C2” represent control plants inoculated with nonviruliferous whiteflies, while “+” and “ntc” denote positive controls and no-template controls, respectively. (D) Raw results of transmission of PeWBVYV as determined by RT-PCR from pepper plants given continuous inoculation access with ∼30 viruliferous whiteflies per plant in three replicates (8 plants each). “C1” refers to a control plant inoculated with nonviruliferous whiteflies, and “+” denotes a positive control. (E) Control experiment for testing the inability of B. tabaci to transmit PeVYV-2 after acquiring the virus for 48 h from infected plants and lifelong transmission to five healthy plants (lanes 1 to 5) compared to a positive control (+). M, molecular weight markers.
FIG 3
FIG 3
Genetic organization of PeWBVYV. (A) PeWBVYV ORFs and validation strategy using RT-PCR amplification. UTR, untranslated region. (B) Strategy for assembly of cDNA corresponding to the PeWBVYV RNA genome from overlapping fragments by overlap extension PCR. (C) PCR amplification of cDNA corresponding to the PeWBVYV RNA genome by overlap PCR.
FIG 4
FIG 4
Amino acid (aa) sequence identities of the translated proteins and nucleotide identities of the noncoding regions (NCR) of PeWBVYV with those of other closely related virus species. Blank cells and asterisks (*) indicate divergent sequences and partial sequence availability, respectively. Increasing levels of saturation of red and green denote high and low amino acid similarity, respectively.
FIG 5
FIG 5
Recombination (RDP) and genetic map of PeWBVYV showing major (AeYV) and minor (PeVYV-2) parents (top) and the transition in the genome sequence at the breakpoint (X; 2,826 bp) at ORF2 (bottom).
FIG 6
FIG 6
Northern blot analysis of N. benthamiana and pepper plants inoculated with the PeWBVYV infectious clone. (A) Lanes 1 and 2, N. benthamiana inoculated with the PeWBVYV clone; lanes 3 and 4, N. benthamiana inoculated with the binary vector pJL89 alone; lane 5, pepper inoculated with PeWBVYV clone; lane 6, pepper inoculated with the binary vector pJL89 alone; lanes 7 and 8, pepper naturally infected with whiteflies (positive control); gRNA, genomic RNA; sgRNA, subgenomic RNA. (B) RT-PCR confirmation of transmission of PeWBVYV infectious clone by B. tabaci. Lanes 1 to 12 denote pepper plants inoculated with B. tabaci after a 48-h acquisition access period on pepper plant agroinoculated with PeWBVYV. C1 and C2, pepper plants caged with B. tabaci after 48 h of rearing on virus-free pepper plants inoculated with pJL89 alone; +C, pepper plant infected with the PeWBVYV infectious clone; ntc, no-template control; M, molecular weight markers.
FIG 7
FIG 7
(A to C) Localization of PeWBVYV (red) in the phloem of naturally infected pepper plants (A) and in N. benthamiana plants agroinoculated with the PeWBVYV infectious clone (B) compared to control uninfected plant hybridized with the same probe (C). White arrowheads indicate virus (red) inside phloem sieve elements and black arrowheads indicate xylem. (D to F) Localization of PeWBVYV (red) inside midguts of B. tabaci after acquisition from naturally infected (D) and agroinfected (E) pepper plants compared to acquisition from a control uninfected plant hybridized with the same probe (F). Nuclei were stained with DAPI (4′,6-diamidino-2-phenylindole; blue).
FIG 8
FIG 8
Multiplex detection of PeWBVYV and PeVYV-2 showing single detection of each virus alone and multiplex detection of both viruses in the same reaction. ntc, no-template control; M, molecular weight markers.
FIG 9
FIG 9
Distribution of PeVYV-2 and PeWBVYV in Israel, sampled from three major pepper-growing areas (Jordan Valley, Arava Valley, and the coastal area) from January to April 2017 and 2018. Pie charts indicate the incidence of PeVYV-2 and PeWBVYV detection in two successive seasons (2017 and 2018). The total numbers of plants tested in the two seasons in each of the specified locations were as follows: for Jordan Valley, 24 and 36, respectively; for the Arava Valley area, 10 and 36, respectively; for the coastal area, 7 and 9, respectively.
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