A simple, rapid and inexpensive method for localization of Tomato yellow leaf curl virus and Potato leafroll virus in plant and insect vectors

Ghanim, Murad; Brumin, Marina; Popovski, Smadar

doi:10.1016/j.jviromet.2009.04.017

Cited by 58 publications

(46 citation statements)

References 17 publications

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“…Short oligonucleotide probes for TYLCCNV and mTYLCCNV (5=-Cy3-GGGACGTCAGGGCTTCTGTA-3=) and for TYLCV and mTYLCV (5=-Cy3-GGAACATCAGGGCTTCG ATA-3=) were used to localize virions in dissected whitefly MGs and PSGs (41). Whiteflies were sampled using the method mentioned above.…”

Section: Methodsmentioning

confidence: 99%

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Specific Cells in the Primary Salivary Glands of the Whitefly Bemisia tabaci Control Retention and Transmission of Begomoviruses

Wei

Zhao

Zhang

et al. 2014

J Virol

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The majority of plant viruses are vectored by arthropods via persistent-circulative or noncirculative transmission. Previous studies have shown that specific binding sites for noncirculative viruses reside within the stylet or foregut of insect vectors, whereas the transmission mechanisms of circulative viruses remain ambiguous. Here we report the critical roles of whitefly primary salivary glands (PSGs) in the circulative transmission of two begomoviruses. The Middle East Asia Minor 1 (MEAM1) species of the whitefly Bemisia tabaci complex efficiently transmits both Tomato yellow leaf curl China virus (TYLCCNV) and Tomato yellow leaf curl virus (TYLCV), whereas the Mediterranean (MED) species transmits TYLCV but not TYLCCNV. PCR and fluorescence in situ hybridization experiments showed that TYLCCNV efficiently penetrates the PSGs of MEAM1 but not MED whiteflies. When a fragment of the coat protein of TYLCCNV was exchanged with that of TYLCV, mutated TYLCCNV accumulated in the PSGs of MED whiteflies, while mutant TYLCV was nearly undetectable. Confocal microscopy revealed that virion transport in PSGs follows specific paths to reach secretory cells in the central region, and the accumulation of virions in the secretory region of PSGs was correlated with successful virus transmission. Our findings demonstrate that whitefly PSGs, in particular the cells around the secretory region, control the specificity of begomovirus transmission. IMPORTANCEOver 75% of plant viruses are transmitted by insects. However, the mechanisms of virus transmission by insect vectors remain largely unknown. Begomoviruses and whiteflies are a complex of viruses and vectors which threaten many crops worldwide. We investigated the transmission of two begomoviruses by two whitefly species. We show that specific cells of the whitefly primary salivary glands control viral transmission specificity and that virion transport in the glands follows specific paths to reach secretory cells in the central region and then to reach the salivary duct. Our results indicate that the secretory cells in the central region of primary salivary glands determine the recognition and transmission of begomoviruses. These findings set a foundation for future research not only on circulative plant virus transmission but also on other human and animal viruses transmitted by arthropod vectors.

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Section: Methodsmentioning

confidence: 99%

“…Twenty MGs and PSGs were dissected from viruliferous MEAM1 and MED adults. Dissected organs were used for fluorescence in situ hybridization (FISH) analyses as described by Ghanim et al (41). In addition, no probe and nonviruliferous whiteflies were used as controls.…”

Section: Methodsmentioning

confidence: 99%

Specific Cells in the Primary Salivary Glands of the Whitefly Bemisia tabaci Control Retention and Transmission of Begomoviruses

Wei

Zhao

Zhang

et al. 2014

J Virol

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“…The FISH procedure generally followed Gottlieb et al [22] and Ghanim et al [35] (with slight modifications). Specimens were collected directly into Carnoy's fixative (chloroform : ethanol : glacial acetic acid, 6 : 3 : 1) and fixed overnight.…”

Section: Methodsmentioning

confidence: 99%

Horizontal transmission of the insect symbiont Rickettsia is plant-mediated

et al. 2011

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Bacteria in the genus Rickettsia, best known as vertebrate pathogens vectored by blood-feeding arthropods, can also be found in phytophagous insects. The presence of closely related bacterial symbionts in evolutionarily distant arthropod hosts presupposes a means of horizontal transmission, but no mechanism for this transmission has been described. Using a combination of experiments with live insects, molecular analyses and microscopy, we found that Rickettsia were transferred from an insect host (the whitefly Bemisia tabaci) to a plant, moved inside the phloem, and could be acquired by other whiteflies. In one experiment, Rickettsia was transferred from the whitefly host to leaves of cotton, basil and black nightshade, where the bacteria were restricted to the phloem cells of the plant. In another experiment, Rickettsia-free adult whiteflies, physically segregated but sharing a cotton leaf with Rickettsia-plus individuals, acquired the Rickettsia at a high rate. Plants can serve as a reservoir for horizontal transmission of Rickettsia, a mechanism which may explain the occurrence of phylogenetically similar symbionts among unrelated phytophagous insect species. This plant-mediated transmission route may also exist in other insect -symbiont systems and, since symbionts may play a critical role in the ecology and evolution of their hosts, serve as an immediate and powerful tool for accelerated evolution.

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“…The first tissue through which virions can translocate to the hemocoel is a modification of the digestive system called the filter chamber (10). Based on extensive TYLCV localization studies using fluorescence in situ hybridization (FISH) and transmission electron microscopy, most TYLCV virions have been observed in the filter chamber, suggesting that it is the main site for viral particle translocation to the hemocoel (11)(12)(13). Virions are transported through the cytoplasm of the filter chamber epithelial cells in vesicles that fuse with the basal plasma membrane, releasing particles between the membrane and the basal lamina (10,14,15).…”

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confidence: 99%

“…Virions are transported through the cytoplasm of the filter chamber epithelial cells in vesicles that fuse with the basal plasma membrane, releasing particles between the membrane and the basal lamina (10,14,15). In contrast to the family Luteoviridae, TYLCV is localized in midgut epithelial cells but not in the hindgut (11,16). Once they cross the midgut cells, the virions take up temporary residence in the hemocoel and then enter the salivary system, from which they are transmitted to plants during feeding (9,14,15).…”

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confidence: 99%

Replication of Tomato Yellow Leaf Curl Virus in Its Whitefly Vector, Bemisia tabaci

Pakkianathan

Kontsedalov

Lebedev

et al. 2015

J Virol

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Tomato yellow leaf curl virus (TYLCV) is a begomovirus transmitted exclusively by the whitefly Bemisia tabaci in a persistent, circulative manner. Replication of TYLCV in its vector remains controversial, and thus far, the virus has been considered to be nonpropagative. Following 8 h of acquisition on TYLCV-infected tomato plants or purified virions and then transfer to non-TYLCV-host cotton plants, the amounts of virus inside whitefly adults significantly increased (>2-fold) during the first few days and then continuously decreased, as measured by the amounts of genes on both virus DNA strands. Reported alterations in insect immune and defense responses upon virus retention led us to hypothesize a role for the immune response in suppressing virus replication. After virus acquisition, stress conditions were imposed on whiteflies, and the levels of three viral gene sequences were measured over time. When whiteflies were exposed to TYLCV and treatment with two different pesticides, the virus levels continuously increased. Upon exposure to heat stress, the virus levels gradually decreased, without any initial accumulation. Switching of whiteflies between pesticide, heat stress, and control treatments caused fluctuating increases and decreases in virus levels. Fluorescence in situ hybridization analysis confirmed these results and showed virus signals inside midgut epithelial cell nuclei. Combining the pesticide and heat treatments with virus acquisition had significant effects on fecundity. Altogether, our results demonstrate for the first time that a single-stranded DNA plant virus can replicate in its hemipteran vector. IMPORTANCEPlant viruses in agricultural crops are of great concern worldwide. Many of them are transmitted from infected to healthy plants by insects. Persistently transmitted viruses often have a complex association with their vectors; however, most are believed not to replicate within these vectors. Such replication is important, as it contributes to the virus's spread and can impact vector biology. Tomato yellow leaf curl virus (TYLCV) is a devastating begomovirus that infects tomatoes. It is persistently transmitted by the whitefly Bemisia tabaci but is believed not to replicate in the insect. To demonstrate that TYLCV is, in fact, propagative (i.e., it replicates in its insect host), we hypothesized that insect defenses play a role in suppressing virus replication. We thus exposed whitefly to pesticide and heat stress conditions to manipulate its physiology, and we showed that under such conditions, the virus is able to replicate and significantly influence the insect's fecundity. (Begomovirus, Geminiviridae) is the name given to a complex of single-stranded DNA (ssDNA) plant viruses that cause tremendous losses of tomato crops worldwide (1). Begomoviruses are transmitted by several biotypes of the whitefly Bemisia tabaci (2, 3). Begomoviruses have either a single (monopartite) or two (bipartite) circular ssDNA genomes of ϳ2,700 nucleotides each. Each genome is encapsidated in an ϳ25...

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A simple, rapid and inexpensive method for localization of Tomato yellow leaf curl virus and Potato leafroll virus in plant and insect vectors

Cited by 58 publications

References 17 publications

Specific Cells in the Primary Salivary Glands of the Whitefly Bemisia tabaci Control Retention and Transmission of Begomoviruses

Specific Cells in the Primary Salivary Glands of the Whitefly Bemisia tabaci Control Retention and Transmission of Begomoviruses

Horizontal transmission of the insect symbiont Rickettsia is plant-mediated

Replication of Tomato Yellow Leaf Curl Virus in Its Whitefly Vector, Bemisia tabaci

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