Fibrillar structures induced by a plant reovirus target mitochondria to activate typical apoptotic response and promote viral infection in insect vectors

Abstract

Numerous plant viruses that cause significant agricultural problems are persistently transmitted by insect vectors. We wanted to see if apoptosis was involved in viral infection process in the vector. We found that a plant reovirus (rice gall dwarf virus, RGDV) induced typical apoptotic response during viral replication in the leafhopper vector and cultured vector cells, as demonstrated by mitochondrial degeneration and membrane potential decrease. Fibrillar structures formed by nonstructural protein Pns11 of RGDV targeted the outer membrane of mitochondria, likely by interaction with an apoptosis-related mitochondrial protein in virus-infected leafhopper cells or nonvector insect cells. Such association of virus-induced fibrillar structures with mitochondria clearly led to mitochondrial degeneration and membrane potential decrease, suggesting that RGDV Pns11 was the inducer of apoptotic response in insect vectors. A caspase inhibitor treatment and knockdown of caspase gene expression using RNA interference each reduced apoptosis and viral accumulation, while the knockdown of gene expression for the inhibitor of apoptosis protein improved apoptosis and viral accumulation. Thus, RGDV exploited caspase-dependent apoptotic response to promote viral infection in insect vectors. For the first time, we directly confirmed that a nonstructural protein encoded by a persistent plant virus can induce the typical apoptotic response to benefit viral transmission by insect vectors.

Apoptotic neurodegeneration in whitefly promotes the spread of TYLCV

“…These results revealed that the silencing of apoptosis-related caspases was behaviorally unfavorable to TYLCV transmission ( Figure 4O ). Likewise, for leafhoppers, Rice gall dwarf virus activates the caspase-dependent apoptosis by targeting the mitochondria, and inducing mitochondrial degeneration to promote viral infections within the insect vector ( Chen et al, 2019 ). These findings suggested that vector apoptosis could be utilized by PTVs to promote the virus spread.…”

“…By contrast, plant viruses theoretically cause limited or no physical damage to insect vectors, but some cases of severe lesions leading to slower behavior and recognition dysfunction have been reported previously, suggesting that nerve damage and immune activation may be involved in the interaction between plant virus and its insect vector ( Ingwell et al, 2012 ; Mauck et al, 2012 ; Moreno-Delafuente et al, 2013 ). Intriguingly, it has been shown that some intracellular immune responses of insect vectors, such as apoptosis and autophagy, benefit virus propagation and transmission, which is contrary to the established antiviral function in the virus-host interaction ( Chen et al, 2019 ; Chen et al, 2017 ; Huang et al, 2015 ; Wang et al, 2012 ).…”

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

“…In 2015, Huang et al (38) reported that apoptosis induced by a plant RNA virus (rice ragged stunt virus) promotes virus transmission by its insect vector, a planthopper. More recently, Chen et al (39) conducted more detailed investigations on the apoptosis activated by another plant RNA virus (rice gall dwarf virus) and provided substantial evidence for the roles of apoptosis in promoting viral infection in its insect vector, a leafhopper. However, as a whole, not much is yet known about the relationship between plant viruses and apoptosis of their insect vectors, partially due to the scarcity of efficient genetic and molecular methods that are applicable to research on a range of plant viruses.…”

A Neuron-Specific Antiviral Mechanism Modulates the Persistent Infection of Rice Rhabdoviruses in Leafhopper Vectors

“…By contrast, plant viruses may also manipulate vector immune systems for their efficient infection in the midgut. For example, autophagy and apoptosis can be activated by rice gall dwarf virus, a plant reovirus, to promote viral replication in the midgut of leafhopper vectors (Chen et al, 2017;Chen Q. et al, 2019). The nucleoprotein of rice stripe virus, a tenuivirus, promotes its replication by activating the c-Jun N-terminal kinase pathway in the midgut of its planthopper vector (Wang et al, 2017).…”