Specific Cells in the Primary Salivary Glands of the Whitefly Bemisia tabaci Control Retention and Transmission of Begomoviruses

Abstract

The 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.

Persistent, circulative transmission of begomoviruses by whitefly vectors

“…The study obtained 13,615 unigenes, among which several highly expressed genes with functions that might be involved in virus transmission or passage such as genes encoding for secretory proteins [73]. Recently, Wei et al [72 ] suggested that specific cells in the PSGs, the cells around the secretory regions are an important site that controls the specificity of TYLCV and TYLCCNV transmission. Localization of TYLCV in the midgut of Bemisia tabaci following acquisition of the virus from infected plants for several days.…”

“…Those molecular changes were accompanied with suppressing immune responses in the whitefly by down regulating the expression of genes involved in Toll signaling and mitogen activated protein kinase (MAPK) pathways [71]. B. tabaci PSGs are a major organ in the transmission pathway of begomoviruses [72 ] ( Figure 1), and the transcriptome of the PSGs of MED B. tabaci was sequenced [73] for the possible identification of receptors or proteins involved in begomoviruses transmission. The study obtained 13,615 unigenes, among which several highly expressed genes with functions that might be involved in virus transmission or passage such as genes encoding for secretory proteins [73].…”

Further insight into reproductive incompatibility between putative cryptic species of the Bemisia tabaci whitefly complex

“…Experimental studies have shown that putative species of this complex differ in many aspects of their biology, such as host range (Zang et al ., ; Xu et al ., ; Sun et al ., ), resistance to insecticide (Wang et al ., ; Rao et al ., ; Horowitz & Ishaaya, ), behavior (Liu et al ., ; Crowder et al ., ; Luan & Liu, ; Wang et al . ; Luan et al ., ) and specificity of begomovirus transmission (Li et al ., ; Polston et al ., ; Wei et al ., , ). Thus recognition of the cryptic species in this whitefly complex is critical to meaningful biological research and effective management (Boykin et al ., ; De Barro, ; Boykin & De Barro, ).…”

The autophagy pathway participates in resistance to tomato yellow leaf curl virus infection in whiteflies

“…Virions are subsequently transported through the hemocoel into the salivary glands and from there they are finally excreted with the saliva during feeding. 13,14 During the circulative transmission of begomoviruses, viral particles interact with various whitefly proteins. 15,16 As demonstrated for tomato yellow leaf curl virus (TYLCV) which is a destructive pathogen of tomato crops, the whitefly GroEL protein seems to bind and protect TYLCV from degradation in the haemolymph.…”