Acquisition, Interference, and Retention of Cucurbit Leaf Curl Viruses in Whiteflies

Cohen, Shahar; Duffus, J. E.; Liu, H. Y.

doi:10.1094/phyto-79-109

Cited by 43 publications

(16 citation statements)

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“…We propose that this observation could be due to compatible early virus-aphid interactions in all cases, followed by transmission blocking at a later step for nonvectors only. For example, late barriers blocking passage across the salivary glands have been demonstrated for some luteovirus-and geminivirus-vector couples (27)(28)(29). Further investigation will be required to determine the exact step at which FBNSV is blocked within A. gossypii.…”

Section: Discussionmentioning

confidence: 99%

Circulative Nonpropagative Aphid Transmission of Nanoviruses: an Oversimplified View

Sicard

Zeddam

Yvon

et al. 2015

J Virol

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Plant virus species of the family Nanoviridae have segmented genomes with the highest known number of segments encapsidated individually. They thus likely represent the most extreme case of the so-called multipartite, or multicomponent, viruses. All species of the family are believed to be transmitted in a circulative nonpropagative manner by aphid vectors, meaning that the virus simply crosses cellular barriers within the aphid body, from the gut to the salivary glands, without replicating or even expressing any of its genes. However, this assumption is largely based on analogy with the transmission of other plant viruses, such as geminiviruses or luteoviruses, and the details of the molecular and cellular interactions between aphids and nanoviruses are poorly investigated. When comparing the relative frequencies of the eight genome segments in populations of the species Faba bean necrotic stunt virus (FBNSV) (genus Nanovirus) within host plants and within aphid vectors fed on these plants, we unexpectedly found evidence of reproducible changes in the frequencies of some specific segments. We further show that these changes occur within the gut during early stages of the virus cycle in the aphid and not later, when the virus is translocated into the salivary glands. This peculiar observation, which was similarly confirmed in three aphid vector species, Acyrthosiphon pisum, Aphis craccivora, and Myzus persicae, calls for revisiting of the mechanisms of nanovirus transmission. It reveals an unexpected intimate interaction that may not fit the canonical circulative nonpropagative transmission. IMPORTANCEA specific mode of interaction between viruses and arthropod vectors has been extensively described in plant viruses in the three families Luteoviridae, Geminiviridae, and Nanoviridae, but never in arboviruses of animals. This so-called circulative nonpropagative transmission contrasts with the classical biological transmission of animal arboviruses in that the corresponding viruses are thought to cross the vector cellular barriers, from the gut lumen to the hemolymph and to the salivary glands, without expressing any of their genes and without replicating. By monitoring the genetic composition of viral populations during the life cycle of Faba bean necrotic stunt virus (FBNSV) (genus Nanovirus), we demonstrate reproducible genetic changes during the transit of the virus within the body of the aphid vector. These changes do not fit the view that viruses simply traverse the bodies of their arthropod vectors and suggest more intimate interactions, calling into question the current understanding of circulative nonpropagative transmission. P lant viruses of the families Luteoviridae, Geminiviridae, and Nanoviridae are transmitted in a circulative (persistent) nonpropagative manner by their insect vectors (1, 2). This transmission mode is characterized by the internalization of the virus within the insect without replication or even transcription of the viral genome. After feeding on an infected plant, the virus...

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Section: Discussionmentioning

confidence: 99%

Circulative Nonpropagative Aphid Transmission of Nanoviruses: an Oversimplified View

Sicard

Zeddam

Yvon

et al. 2015

J Virol

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“…The virus may accumulate in the body of the insect and then move into the salivary glands at a rate which is much slower than the accumulation rate, as suggested by Gildow and Rochow [1981] for luteoviruses and by Cohen et al [1989] for squash leaf curl virus (SLCV) and melon leaf curl virus, two closely related geminiviruses.…”

Section: Discussionmentioning

confidence: 99%

Relationships of the Sardinian isolate of tomato yellow leaf curl geminivirus with its whitefly vectorBemisia tabaci Gen

1995

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Relationships of an Italian isolate of tomato yellow leaf curl geminivirus from Sardinia (TYLCV-S) with its whitefly vector Bemisia tabaci were studied by means of experimental transmissions from tomato to tomato plants. TYLCV-S was confirmed to be transmitted in a persistent, circulative manner. The minimum latent period in the vector was between 17 and 20 h from the beginning of the acquisition access period (AAP). The maximum retention of infectivity was 8 days from the end of the AAP. Both acquisition and inoculation feeding times influenced the detected proportion of infective insects, with patterns well described by an exponential model. Acquisition was more efficient than inoculation. Males were significantly less efficient vectors than females. Nymphs were as efficient as adults in acquiring the virus. The length of AAP influenced both the retention of infectivity, and the pattern of transmission in serial transfer transmission tests with individual females. No significant difference in transmission efficiency was detected between two colonies of B. tabaci, one inducing typical silverleaf symptoms on squash, the other inducing only mild symptoms with more than 50 whiteflies per plant. The phenomenon of periodic acquisition was not unequivocally proved for TYLCV-S.

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“…Most whitefly-transmitted viruses are ingested from the phloem sap of virus-infected plants during feeding (Duffus, 1987;Cohen et al, 1989). For successful transmission, virus must pass intact through the digestive system and ultimately enter the salivary system, from where virions are transmitted to the plant in whitefly saliva.…”

Section: Discussionmentioning

confidence: 99%

Uptake and metabolism of leaf proteins by the silverleaf whitefly

Salvucci

Rosell

Brown

1998

Arch Insect Biochem Physiol

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Acquisition, Interference, and Retention of Cucurbit Leaf Curl Viruses in Whiteflies

Cited by 43 publications

References 0 publications

Circulative Nonpropagative Aphid Transmission of Nanoviruses: an Oversimplified View

Circulative Nonpropagative Aphid Transmission of Nanoviruses: an Oversimplified View

Relationships of the Sardinian isolate of tomato yellow leaf curl geminivirus with its whitefly vectorBemisia tabaci Gen

Uptake and metabolism of leaf proteins by the silverleaf whitefly

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