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The Effect of Species Soybean Vein Necrosis Orthotospovirus (SVNV) on Life Table Parameters of Its Vector, Soybean Thrips (Neohydatothrips variabilis Thysanoptera: Thripidae)

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Soybean vein necrosis, caused by soybean vein necrosis virus (SVNV) is an important viral disease of soybeans that can be seed borne or insect vectored. This plant viral disease affects seed qualitative parameters, including seed oil content. Increased damage is observed in late planted soybeans. The disease is widespread, and almost all soybean-growing states in USA are affected. Globally, SVNV is reported in Canada, the United States, Egypt and Pakistan. In order to manage the disease, it is important to understand the vector’s biology and the effect of SVNV on life table parameters (survival, longevity, mortality, doubling time, generation, rate of intrinsic increase) of vector soybean thrips, which can help to establish pest management predictive models. We used an age-stage two-sex life table estimation model to define the effect of SVNV on the life parameters of male and female soybean thrips. Overall, we found that SVNV infection increased viruliferous thrips survival, longevity, gross reproduction rate, life expectancy and decreased population doubling time. Overall viruliferous thrips benefit from SVNV infection and transmission due to better survival, longevity and increased fitness.

Abstract

Soybean vein necrosis orthotospovirus (SVNV: Tospoviridae: Orthotospovirus), the causal agent of soybean vein necrosis disease, is vectored by soybean thrips Neohydatothrips variabilis (Beach, 1896), and to a lesser extent by five other thrips species. There is increasing incidence of soybean vein necrosis (SVN) disease in all soybean growing states in the United States, Canada, Egypt and Pakistan, necessitating a study of the system’s ecology and management. We addressed the effect of SVNV on the life table parameters of the vector. We used an ‘age-stage two-sex’ life table approach, which provided detailed life stage durations of each larval instar and adults (both sexes). Our results showed that the intrinsic rate of increase (r), finite rate of increase (λ) and mortality index (qx) were higher in the infected population, while the net reproduction rate (Ro), cumulative probability of survival (lx) and gross reproduction rate (GRR) were lower in the uninfected population. Overall, in both infected and uninfected populations, the number of eggs producing haploid males via arrhenotoky ranged from 9–12 per female. Male to female ratio was female biased in the infected population. Overall, our study provided evidence that virus infection, by decreasing the population doubling time, could enhance the virus and vector populations in soybeans.

SUBMITTER: Hameed A

PROVIDER: S-EPMC9324745 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Simple Summary Soybean thrips are an important vector of Soybean vein necrosis virus disease, found in all soybean-growing regions of the United States and Canada. The disease reduces the seed oil content and fatty acid profiles in infected plants. It is important to know the morphology of the female reproductive system of soybean thrips to understand the egg-laying mechanism and develop strategies for virus vector management. For this purpose, we used fuchsin staining, paraffin-based histology, dissections, serial block-face scanning electron microscopy and confocal laser scanning microscopy techniques to understand the structure and motorization of the internal and external genitalia of soybean thrips. We also investigated the egg-laying behavior of soybean thrips. The female reproductive system is composed of two ovaries, an oviduct, an accessory gland, an appendage gland, a common oviduct and a vagina. Female soybean thrips lay eggs in the parenchymatous tissues near the veins of the leaves. The appendage gland likely secretes lubrication to facilitate the movement of eggs through the external genitalia. Seven muscles support the movement of eggs from the ovaries to the leaf surface. The anatomy and probable role of each muscle is also described. Abstract Soybean thrips (Neohydatothrips variabilis) are an important phytophagous vector of the widely recognized Soybean vein necrosis orthotospovirus (SVNV). Understanding the egg-laying behavior of these thrips could aid in developing strategies for the management of the vector and virus. In this study, we described the egg-laying behavior of N. variabilis and reconstructed the three-dimensional morphology of the female terminalia by using serial block-face scanning electron microscopy (SBFSEM) and confocal laser scanning microscopy (CLSM). The female reproductive system consists of two panoistic ovaries consisting of eight ovarioles. The appendage gland is connected to the ovaries by two muscles, and to the body wall by a single muscle. The spermatheca is connected to the eighth tergum through four branched muscles, to the basivalvulae of the ovipositor by one muscle and to the vagina by a single muscle. The external genitalia are operated by seven muscles. The movement of the eggs inside the ovipositor is achieved by the back and forth “rocking” movement of the first valvulae and valvifer. Eggs are deposited into the parenchymatous tissue alongside leaf veins. To the best of our knowledge, this is the first study describing the internal and external genitalia of N. variabilis.

Project description:Soybean vein necrosis virus (SVNV) is a newly discovered species of tospovirus infecting soybean plants that is transmitted by the primary vector, soybean thrips (Neohydatothrips variabilis), and two additional secondary vectors, tobacco thrips (Frankliniella fusca) and eastern flower thrips (F. tritici). This study was undertaken to elucidate the association between virus acquisition [6, 12, 24, and 48 h acquisition access period (AAP)] and transmission efficiency [12, 24, and 48 h inoculation access period (IAP)] in the primary vector, N. variabilis, and to examine the mechanisms of vector competence by analyzing the effect of AAP (6, 12, and 24 h) on virus infection in various tissues. In addition, we examined virus infection in tissues of the two secondary vectors. We found a significant effect of virus acquisition on transmission efficiency, transmission rate post 6 and 48 h AAP was significantly lower than 12 and 24 h AAP. Our analysis did not reveal a correlation between virus transmission rate and virus RNA in corresponding N. variabilis adults. On the contrary, N. variabilis adults harboring higher accumulation of the virus (>104) resulted in lower transmission rates. Analysis of SVNV infection in the tissues revealed the presence of the virus in the foregut, midgut (region 1, 2, and 3), tubular salivary glands and principal salivary glands (PSG) of adults of all three vector species, however, the frequency of infected tissues was highest in N. variabilis followed by F. fusca and F. tritici. The frequency of SVNV infection in individual tissues specifically the salivary glands was lowest after 6 h AAP compared to 12 and 24 h AAP. This finding is in agreement with the transmission assays, where significantly lower virus transmission rate was observed post 6 h AAP. In addition, N. variabilis adults with high PSG infection (12 and 24 h AAP) were likely to have high percentage of foregut and midgut region 2 infection. Overall, results from the transmission assays and immunolabeling experiments suggest that shorter AAP results in reduced virus infection in the various tissues especially PSG, which are important determinants of vector competence in SVNV-thrips interaction.

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The Effect of Species Soybean Vein Necrosis Orthotospovirus (SVNV) on Life Table Parameters of Its Vector, Soybean Thrips (Neohydatothrips variabilis Thysanoptera: Thripidae)

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