Brevipalpus mites (Acari: Tenuipalpidae): vectors of invasive, non-systemic cytoplasmic and nuclear viruses in plants
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Multi-directional interactions occur among plant hosts, Brevipalpus mites and the plant viruses they transmit. Such interactions should be considered when evaluating the severity of a disease such as citrus leprosis. The current understanding of Brevipalpus-transmitted viruses relies on the capability of the vector to transmit the disease, the persistence of the virus in the host plant and the ability of the disease to spread. Previously, we discussed the Citrus leprosis virus (CiLV) and its importance and spread over the past decade into new areas of South and Central America, most recently into southern Mexico and Belize. Here, we address key questions to better understand the biology of the mite vector, fitness costs, and the peculiarities of Brevipalpus mite reproduction, virus survival, transmissibility and spread, and the expansion of the host plant range of Brevipalpus species vectoring the disease.
KeywordsTenuipalpidae Vector–virus relationships Invasive species Brevipalpus phoenicis complex
Biological peculiarities of Brevipalpus mite vectors
Previous papers have reviewed the basic biology of several Brevipalpus species on citrus, tea and other plants (Oomen 1982; Haramoto 1969, Chiavegato 1986, Childers et al. 2003a, b). However, new information has come to light that species that have been previously identified as Brevipalpus phoenicis (Geijkes) are actually a complex of morphologically similar species (Beard et al. 2012) and biotypes which co-infest various plant species (Rodrigues et al. 2004, 2008, Kitajima et al. 2010). This requires a closer look at their biology to determine the relationship of the species within the complex that vector diseases with the invasive viruses, such as citrus leprosis and related plant viruses.
Expansion of Brevipalpus transmitted viruses (BTVs)
Brevipalpus transmitted viruses (BTVs) are New World plant pathogens with one known exception, the Orchid fleck virus that is reported worldwide (Kondo et al. 2003). Citrus leprosis-like symptoms were reported to occur in South Africa, Philippines, China, India, Japan, Java and Sri Lanka (Fawcett and Lee 1926, Fawcett 1936), but the causal agent and its vector were not confirmed.
The occurrence and spread of citrus leprosis through the Americas
Argentina (Misiones, Corrientes)
Brazil (Sao Paulo)
Bitancourt et al. (1933)
Brazil (Rio Grande do Sul)
Bitancourt and Grillo (1934)
Brazil (Minas Gerais)
Teixeira et al. (1993)
Domingues and Rodrigues (1999)
Mejia et al. (2002)
Dominguez et al. (2001)
Araya Gonzales (2000)
Leon et al. (2006)
Rodrigues et al. (2007)
It has been assumed that the cytoplasmic form of citrus leprosis is more virulent than the nuclear form. This is a speculative assertion and is not supported by direct experimental evidence, but rather based primarily on the frequency of occurrence of characteristic foliar and fruit lesions of the two types in the field. Citrus leprosis reached Mexico around 2004 and spread rapidly through all the major southern citrus-growing areas. Mexico is known to have a rich fauna of false spider mites including many species of Brevipalpus (Baker and Tuttle 1987, Mesa et al. 2009). Recently, both the cytoplasmic and nuclear types of citrus leprosis were identified in Mexico (G. Otero-Colina, pers. comm., 2012). Is it possible that the introduction of both forms of citrus leprosis into southern Mexico overlapped with the new biotypes of mites vectors? This could result in a different pattern of disease spread. To better understand the movement of the disease, it is important to know whether the viruses and the vector biotypes are spreading together, or whether the virus is spreading by vector biotypes or species already occurring in the new region.
Complex pathogen-vector-host interactions such as citrus leprosis represent a challenge for states, countries and regions to effectively establish quarantine measures and barriers. This is despite growing efforts and collaboration among various research institutions and governmental agencies. Biological field studies of Brevipalpus mite populations are needed that include both taxonomic and molecular identification of mite populations not only on citrus but also on adjacent agricultural crops and associated ornamental and ground cover plants including weeds that may serve as host plants.
New mite vectors, virus-infected plants, or virus-infected Brevipalpus mites could arrive into the USA through various pathways (Childers and Rodrigues 2005). Therefore, a proactive approach would be more effective than relying on conventional interception or quarantine measures (Heather and Hallman 2008). A coordinated effort among US citrus producing states is needed to: (1) identify the Brevipalpus species occurring within and around citrus orchards in each state, and (2) to determine the potential of those Brevipalpus species to transmit one or both forms of CiLV. Determining the identity and biology of the Brevipalpus vector(s) and virus types that are spreading in citrus and alternate host plants through Mexico, Belize and other Central American countries is needed. Also, determining the timing, magnitude and dispersal distances of Brevipalpus vector species would provide invaluable information for more effective management capabilities than currently exist (Childers and Rodrigues 2011). Research is needed to minimize the further spread of this serious citrus disease and to reduce potential economic losses.
Transmission of Citrus leprosis virus and vector fitness
Accumulated frequencies observed (Fo) and expected (Fe) of Brevipalpus phoenicis larvae hatching from colonies associated with citrus leprosis (CoAL, n = 90 eggs) and without citrus leprosis (CoNAL, n = 223 eggs)
Symbionts could influence vector behavior and directly or indirectly affect the ability to acquire or transmit the pathogen during the feeding process. Cardinium bacteria were reported to infect Brevipalpus populations (Weeks et al. 2001) but were shown not to affect the fitness of B. californicus mites associated with the transmission of orchid fleck virus in orchids (Chigira and Miura 2005).
Vector-transmitted parasites react to and induce changes in their environment both in the host and vector, as well as in response to other parasites (Matthews 2011). However, very little is known about the molecular and physiological changes in plant hosts and vectors during the process of infection by BTV’s. Considering the physiological changes in leprosis-infected tissues, Nogueira et al. (1996) reported higher levels of iron among other elements associated with citrus leprosis lesions. This was explained by the higher accumulation of ferritin-like arrays associated with pro-plastids on citrus infected cells (Rodrigues 1995). Freitas-Astua et al. (2007) reported the influence of viruses on the expression of plant genes related to plant energy and metabolism in the earlier stages of infection. This agrees with previous cytopathological observations (Rodrigues 1995). In addition, differential host susceptibility to citrus leprosis among citrus species, hybrids and varieties, as shown with ‘Sabará’ tangor and grapefruit could play important roles in virus persistence (Rodrigues 2006).
Social, environmental and economic impacts of Brevipalpus transmitted diseases
Mean yield (weight and number of fruits per tree) on 3-year-old sweet orange varieties (six plants/variety) and Palestine sweet lime infested with citrus leprosis-infected Brevipalpus mites, in 1999, Piracicaba, SP, Brazil
% fruits with symptoms
Other hosts plants with BTV’s including coffee, passion fruit and many ornamental plants have been reported by Kitajima et al. (2010) that included new areas of citrus introductions into both agricultural and natural environments (Rodrigues et al. 2008) and urban settings (Miranda et al. 2007). In many instances the initial spread of citrus leprosis goes unnoticed while both movement of people and goods occur.
Brevipalpus mites and viruses that they transmit are a growing phytosanitary threat to the citrus industries of the world. The mites themselves are intriguing organisms in terms of their genetic uniqueness (haploid females showing two non-homologous chromosomes), occurrence of symbionts affecting their sex ratios and the close relationship with numerous cytoplasmic and nuclear types of viruses. To date, these mite-vectored viruses include only non-systemic pathogens that persist under natural conditions and represent an increasing major economic, environmental and social threat to agricultural and ornamental industries.
We would like to thank Dr. Neusa L. Nogueira and Monica Lanzoni (Univ. São Paulo) and Diann S. Achor (Univ Florida) for their initial support and advice using electron microscopy analysis. Appreciation is extended to Dr. Elliot Kitajima (Univ. São Paulo) for fruitful discussions on CiLV-Brevipalpus interactions. The following funding agencies supported parts of the research presented in this paper: Fundecitrus, CNPq, CAPES (Brazil), USDA (CA Awards), and the California Citrus Research Board.
This article is distributed under the terms of the Creative Commons Attribution License which permits any use, distribution, and reproduction in any medium, provided the original author(s) and the source are credited.
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