Brevipalpus-transmitted viruses: parallelism beyond a common vector or convergent evolution of distantly related pathogens?

Although diseases caused by Brevipalpus-transmitted viruses (BTV) became relevant for agriculture a century ago, their causal agents have been only recently characterized and classified in two new genera of plant-infecting viruses: Cilevirus and Dichorhavirus. In this review, we highlight both similarities and differences between these viruses emphasizing their current taxonomy and historical classification, phylogeny, genomic organization, gene expression, and the latest research developments on BTVs. Additionally, we stress particular features of interactions with their mite vectors and plant hosts that support, from an evolutionary perspective, the potential convergence of both viral groups.

Virus-vector relationship in the Citrus leprosis pathosystem.

Citrus leprosis has been one of the most destructive diseases of citrus in the Americas. In the last decade important progress has been achieved such as the complete genome sequencing of its main causal agent, Citrus leprosis virus C (CiLV-C), belonging to a new genus Cilevirus. It is transmitted by Brevipalpus yothersi Baker (Acari: Tenuipalpidae), and is characterized by the localized symptoms it induces on the leaves, fruits and stems. It occurs in the American continents from Mexico to Argentina. The virus was until recently considered restricted to Citrus spp. However, it was found naturally infecting other plants species as Swinglea glutinosa Merrill and Commelina benghalensis L., and has been experimentally transmitted by B. yothersi to a large number of plant species. Despite these advances little is known about the virus-vector relationship that is a key to understanding the epidemiology of the disease. Some components of the CiLV-C/B. yothersi relationship were determined using the common bean (Phaseolus vulgaris L. cv. 'IAC Una') as a test plant. They included: (a) the virus acquisition access period was 4 h; (b) the virus inoculation access period was 2 h; (c) the latent period between acquisition and inoculation was 7 h; (d) the period of retention of the virus by a single viruliferous mite was at least 12 days; (d) the percentage of viruliferous individuals from mite colonies on infected tissues ranged from 25 to 60%. The experiments confirmed previous data that all developmental stages of B. yothersi (larva, protonymph and deutonymph, adult female and male) were able to transmit CiLV-C and that transovarial transmission of the virus did not occur. CiLV-C can be acquired from lesions on leaves, fruits and stems by B. yothersi. Based on the distribution of lesions produced by single viruliferous B. yothersi on bean leaves, it is concluded that they tend to feed in restricted areas, usually near the veins. The short latent and transmission periods during the larval stage suggest that the CiLV-C/B. yothersi relationship is of the persistent circulative type.

Transmission of grapevine Pinot gris virus by Colomerus vitis (Acari: Eriophyidae) to grapevine.

Grapevine Pinot gris virus (GPGV) is a new virus reported in Europe and several other grape-growing countries. In an attempt to identify a vector for GPGV, samples of the eriophyid mite Colomerus vitis collected from buds and erinea in GPGV-infected vines were analysed by RT-PCR, using specific primers. Molecular analysis revealed the presence of GPGV in C. vitis. Transmission trials were conducted using C. vitis collected from GPGV-infected vines. Mites were able to transmit GPGV to healthy grapevines, suggesting that C. vitis is a potential vector of this virus.

Planting Date and Variety Selection for Management of Viruses Transmitted by the Wheat Curl Mite (Acari: Eriophyidae).

Wheat is an important food grain worldwide, and it is the primary dryland crop in the western Great Plains. A complex of three viruses (Wheat streak mosaic, Wheat mosaic, and Triticum mosaic viruses) is a common cause of loss in winter wheat production in the Great Plains. All these viruses are transmitted by the wheat curl mite (Aceria tosichella Keifer). Once these viruses are established, there are no curative actions; therefore, prevention is the key to successful management. A study was designed to evaluate preventative management tactics (planting date, resistant varieties) for reducing the impact from this virus complex. The main plot treatments were three planting dates, and split-plot treatments were three wheat varieties. Varieties were planted at three different times during the fall to simulate early, recommended, and late planting dates. The varieties evaluated in this study were Mace (virus resistant), Millennium (mild tolerance), and Tomahawk (susceptible). Measurements of virus symptomology and yield were used to determine virus impact. Results consistently showed that the resistant Mace yielded more than Millennium or Tomahawk under virus pressure. In some years, delayed planting improved the yields for all varieties, regardless of their background; however, under the most severe virus pressure the combination of both management strategies was not sufficient to provide practical control of this complex. These results illustrate the importance of using a combination of management tactics for this complex, but also reinforce the importance for producers to use additional management strategies (e.g., control preharvest volunteer wheat) to manage this complex.

Dichorhavirus: a proposed new genus for Brevipalpus mite-transmitted, nuclear, bacilliform, bipartite, negative-strand RNA plant viruses.

Orchid fleck virus (OFV) is an unassigned negative-sense, single-stranded (-)ssRNA plant virus that was previously suggested to be included in the family Rhabdoviridae, order Mononegavirales. Although OFV shares some biological characteristics, including nuclear cytopathological effects, gene order, and sequence similarities, with nucleorhabdoviruses, its taxonomic status is unclear because unlike all mononegaviruses, OFV has a segmented genome and its particles are not enveloped. This article analyses the available biological, physico-chemical, and nucleotide sequence evidence that seems to indicate that OFV and several other Brevipalpus mite-transmitted short bacilliform (-)ssRNA viruses are likely related and may be classified taxonomically in novel species in a new free-floating genus Dichorhavirus.

Detection of European mountain ash ringspot-associated virus-specific RNA and protein P3 in the pear leaf blister mite Phytoptus pyri (Eriophyidae).

The means by which European mountain ash ringspot-associated virus (EMARaV), a minus-strand ssRNA virus and the type member of the genus Emaravirus, is naturally spread, is unknown. In attempts to identify an EMARaV vector, galls induced by the eriophyid mite Phytoptus pyri were frequently found on infected leaves. By immunofluorescence microscopy, the presence of EMARaV nucleocapsid protein P3 was demonstrated in P. pyri individuals collected from diseased plants. Furthermore, RT-PCR analysis of entire P. pyri individuals revealed the presence of both viral genomic ss(-)RNAs and antigenomic ss(+)RNAs, suggesting that P. pyri might be a candidate vector of EMARaV.

Detection and localisation of picorna-like virus particles in tissues of Varroa destructor, an ectoparasite of the honey bee, Apis mellifera.

Virus-like particles, 27 nm in diameter, were observed in extracts of individual Varroa destructor mites and in sections of mite tissue. Application of a purification procedure resulted in virus preparations that were used to prepare an antiserum to detect the virus in individual mites. Immunohistology studies showed that the gastric caecae were heavily infected, whereas no immunostaining could be detected in other mite tissues or organs, like the salivary glands, brain, rectum or reproductive organs. By electron microscopy large aggregates of virus-like particles in para-crystalline lattices were found in cells of the gastric caecae. The particles, reminiscent to picorna-like viruses, occurred mainly in the cytoplasm, whereas some virus particles were sparsely scattered in vacuoles. Occasionally, particles were observed in membrane-bound vesicles or in long tubular membrane structures in the cytoplasm. The accumulation of the picorna-like virus particles in the cytoplasm and the presence of the virus in membrane structures give a strong indication that the virus replicates in the mite.