Apoptosis in a Whitefly Vector Activated by a Begomovirus Enhances Viral Transmission

Abstract

Apoptosis is generally considered the first line of defense against viral infection. However, the role of apoptosis in the interactions between plant viruses and their insect vectors has rarely been investigated. By studying plant DNA viruses of the genus Begomovirus within the family Geminiviridae, which are transmitted by whiteflies of the Bemisia tabaci species complex in a persistent manner, we revealed that virus-induced apoptosis in insect vectors can facilitate viral accumulation and transmission. We found that infection with tomato yellow leaf curl virus activated the apoptosis pathway in B. tabaci. Suppressing apoptosis by inhibitors or silencing caspase-3 significantly reduced viral accumulation, while the activation of apoptosis increased viral accumulation in vivo. Moreover, the positive effect of whitefly apoptosis on virus accumulation and transmission was not due to its cross talk with the autophagy pathway that suppresses begomovirus infection in whiteflies. We further showed that viral replication, rather than the viral coat protein, is likely the critical factor in the activation of apoptosis by the virus. These novel findings indicate that similarly to many animal and a few plant RNA viruses, plant DNA viruses may activate apoptosis in their insect vectors leading to enhanced viral accumulation and transmission. IMPORTANCE Of the approximately 1,100 known plant viruses, about one-third are DNA viruses that are vectored by insects. Plant virus infections often induce cellular and molecular responses in their insect vectors, which can, in many cases, affect the spread of viruses. However, the mechanisms underlying vector responses that affect virus accumulation and transmission are poorly understood. Here, we examined the role of virus-induced apoptosis in the transmission of begomoviruses, a group of single-stranded plant DNA viruses that are transmitted by whiteflies and cause extensive damage to many crops worldwide. We demonstrated that virus infection can induce apoptosis in the insect vector conferring protection to the virions from degradation, leading to enhanced viral accumulation and transmission to host plants. Our findings provide valuable clues for designing new strategies to block the transmission of insect-vectored plant viruses, particularly plant DNA viruses.

Genomic Variation and Diversification in Begomovirus Genome in Implication to Host and Vector Adaptation

“…Begomoviral proteins have been characterized for understanding the mechanism of symptom recovery [ 61 , 62 ], virulence, and host resistance [ 63 , 64 ]. Coat protein (CP) is a multifunctional protein due to its interaction with plants and vectors [ 65 ].…”

PEBP regulates balance between apoptosis and autophagy, enabling coexistence of arbovirus and insect vector

“…It has been shown that apoptosis enhanced TYLCV loading while autophagy eliminated in MEAM1 whitefly (Wang et al, 2016; Wang et al, 2020c), but is still unclear whether simultaneous activation of apoptosis and autophagy was essential in MED whitefly for co-existence with TYLCV. We therefore introduced a serial of pharmacological experiments to artificially regulate the apoptosis and autophagy of whitefly, and to determine effects of these PCD on virus loading.…”

“…Although TYLCV could also induce PCD in MEAM1 species, the most striking difference is the initiation timepoint of PCD after acquiring TYLCV. Specifically, MED whitefly needs 6-12 hours to initiate PCD while MEAM1 needs a relative longer time from 24 to 48 hours (Wang et al, 2016; Wang et al, 2020c). Considering PCD could be essential for virus acquisition, PEBP4-dependent PCD in MED species has quicker initiation than PEBP4-independent PCD in MEAM1 species, possibly resulting in higher virus capacity for MED species (Kliot et al, 2020).…”

“…By contrast, PCD in insect vectors seems more compatible with arthropod-borne virus (arbovirus) with less or even no pathological symptoms during virus acquisition and transmission(Bartholomay and Michel, 2018; Brackney, 2017; Clem, 2016; Yang et al, 2020). Evidence suggests that arbovirus-induced PCD in insect vectors enhances the immune tolerance, while permitting coexistence of arbovirus with the vector (Chen et al, 2019; Chen et al, 2017; Wang et al, 2020c). The molecular and biochemical bases, however, remain largely elusive.…”

“…Previous results showed that both apoptosis and autophagy could be activated by TYLCV in MEAM1 whitefly (Wang et al, 2016; Wang et al, 2020b). While virus loading is facilitated by activation of apoptosis, it is apparently suppressed by initiation of autophagy (Wang et al, 2016; Wang et al, 2020a; Wang et al, 2020c). The underlying regulatory mechanism and ecological implication, however, remain largely unclear.…”