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Native and Non-Native Bemisia tabaci NAFME Haplotypes Can Be Implicated in Dispersal of Endemic and Introduced Begomoviruses in Oman.

ABSTRACT: Irrigated agriculture and global trade expansion have facilitated diversification and spread of begomoviruses (Geminiviridae), transmitted by the Bemisia tabaci (Gennadius) cryptic species. Oman is situated on major crossroads between Africa and South Asia, where endemic/native and introduced/exotic begomoviruses occur in agroecosystems. The B. tabaci 'B mitotype' belongs to the North Africa-Middle East (NAFME) cryptic species, comprising at least eight endemic haplotypes, of which haplotypes 6 and/or 8 are recognized invasives. Prevalence and associations among native and exotic begomoviruses and NAFME haplotypes in Oman were investigated. Nine begomoviral species were identified from B. tabaci infesting crop or wild plant species, with 67% and 33% representing native and exotic species, respectively. Haplotypes 2, 3, and 5 represented 31%, 3%, and 66% of the B. tabaci population, respectively. Logistic regression and correspondence analyses predicted 'strong'- and 'close' virus-vector associations involving haplotypes 5 and 2 and the exotic chili leaf curl virus (ChiLCV) and endemic tomato yellow leaf curl virus-OM, respectively. Patterns favor a hypothesis of relaxed virus-vector specificity between an endemic haplotype and the introduced ChiLCV, whereas the endemic co-evolved TYLCV-OM and haplotype 2 virus-vector relationship was reinforced. Thus, in Oman, at least one native haplotype can facilitate the spread of endemic and introduced begomoviruses.

SUBMITTER: Shahid MS

PROVIDER: S-EPMC10056824 | biostudies-literature | 2023 Mar

REPOSITORIES: biostudies-literature

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Native and Non-Native Bemisia tabaci NAFME Haplotypes Can Be Implicated in Dispersal of Endemic and Introduced Begomoviruses in Oman.

Shahid Muhammad Shafiq MS Paredes-Montero Jorge R JR Ashfaq Muhammad M Al-Sadi Abdullah M AM Brown Judith K JK

Insects 20230308 3

Irrigated agriculture and global trade expansion have facilitated diversification and spread of begomoviruses (Geminiviridae), transmitted by the Bemisia tabaci (Gennadius) cryptic species. Oman is situated on major crossroads between Africa and South Asia, where endemic/native and introduced/exotic begomoviruses occur in agroecosystems. The B. tabaci 'B mitotype' belongs to the North Africa-Middle East (NAFME) cryptic species, comprising at least eight endemic haplotypes, o ...[more]

PMID: 36975953

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Project description:UnlabelledThe 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.

Project description:The widespread loss of native species and the introduction of non-native species has important consequences for island ecosystems. Non-native species may or may not functionally replace the role of native species in ecological processes such as seed dispersal. Although the majority of Hawaii's native plants require bird-mediated seed dispersal, only one native frugivore, Omao (Myadestes obscurus), persists in sufficient numbers to fill this functional role. Omao are restricted to less than half their original range, but two introduced frugivores are abundant throughout Hawaii. Given large-scale extinctions on islands, it is important to understand whether introduced birds serve as functional replacements or whether the absence of native frugivores alters plant communities. To assess seed dispersal by native and introduced birds, seed rain, vegetation characteristics, bird diet, density and habitat use were measured at three sites with Omao and three sites without Omao on Hawaii Island. The diet of native and introduced birds overlapped substantially, but Omao dispersed a variety of native species (n = 6) relatively evenly. In contrast, introduced birds dispersed an invasive species and fewer native species (n = 4), and >90 % of seeds dispersed by introduced birds were from two ubiquitous small-seeded species. Seed rain was significantly greater and more species rich at sites with Omao. These findings suggest that patterns of seed dispersal are altered following the local extinction of a native island frugivore. To more directly evaluate the relative roles of native and introduced frugivores in ecological processes, future studies could include reintroducing Omao to a suitable habitat within its historic range, or novel introductions to nearby islands where closely related species are now extinct. In an era of widespread extinction and invasion of island ecosystems, understanding the consequences of novel animal assemblages for processes like seed dispersal will be critical for maintaining diverse and self-regenerating plant communities.

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Dataset Information

Native and Non-Native Bemisia tabaci NAFME Haplotypes Can Be Implicated in Dispersal of Endemic and Introduced Begomoviruses in Oman.

Publications

Native and Non-Native <i>Bemisia tabaci</i> NAFME Haplotypes Can Be Implicated in Dispersal of Endemic and Introduced Begomoviruses in Oman.

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