Virus Factories of Cauliflower Mosaic Virus Are Virion Reservoirs That Engage Actively in Vector Transmission

Abstract

cCauliflower mosaic virus (CaMV) forms two types of inclusion bodies within infected plant cells: numerous virus factories, which are the sites for viral replication and virion assembly, and a single transmission body (TB), which is specialized for virus transmission by aphid vectors. The TB reacts within seconds to aphid feeding on the host plant by total disruption and redistribution of its principal component, the viral transmission helper protein P2, onto microtubules throughout the cell. At the same time, virions also associate with microtubules. This redistribution of P2 and virions facilitates transmission and is reversible; the TB reforms within minutes after vector departure. Although some virions are present in the TB before disruption, their subsequent massive accumulation on the microtubule network suggests that they also are released from virus factories. Using drug treatments, mutant viruses, and exogenous supply of viral components to infected protoplasts, we show that virions can rapidly exit virus factories and, once in the cytoplasm, accumulate together with the helper protein P2 on the microtubule network. Moreover, we show that during reversion of this phenomenon, virions from the microtubule network can either be incorporated into the reverted TB or return to the virus factories. Our results suggest that CaMV factories are dynamic structures that participate in vector transmission by controlled release and uptake of virions during TB reaction.

Selective autophagy limits cauliflower mosaic virus infection by NBR1-mediated targeting of viral capsid protein and particles

“…However, nbr1 and atg5 mutants did not show alterations in symptom appearance or aphid transmission rates when used as feeding source, arguing against any significant ability of NBR1 to suppress the spread of infection within and from plants. Both systemic movement and virus particle acquisition by aphids occurs from infected cells and is tightly linked to viral inclusion body functions (VFs and TBs) (27,34,35). Indeed, we propose, based on several observations, that viral particles stored in inclusions are protected from autophagy.…”

Mutations within A 35 amino acid region of P6 influence self-association, inclusion body formation, and Caulimovirus infectivity

“…Interestingly, viruses may induce formation of more than one type of IB in infected cells, each with different functions. For example, the CaMV genome encodes two proteins that can form different types of IBs: P6 and P2 (Bak et al, 2013; Espinoza et al, 1991). P2, encoded by CaMV gene II, forms electron-lucent IBs that are dynamic, either aggregating or dissociating in response to various stimuli (Armour et al, 1983; Blanc et al, 1993; Espinoza et al, 1991; Khelifa et al, 2007; Martiniere et al, 2013; Woolston et al, 1983).…”

“…P6 edIBs are sites where CaMV protein synthesis, genome replication, and virion assembly are thought to occur (Haas et al, 2002; Hull, 2002; Mazzolini et al, 1989). P6 IBs are also dynamic, releasing virus particles in response to certain stimuli (Bak et al, 2013). P6 may contain several self-association domains (Li and Leisner, 2002) to permit simultaneous interaction with other P6s, permitting aggregation into edIBs.…”

Microtubule Regulation and Function during Virus Infection

“…Remarkably, transmission bodies react within seconds to the presence of aphids on the plant by rapid disruption and redistribution of the core transmission body helper protein, P2, onto MTs, driving the release of virions from the transmission body and factories onto MTs. Within minutes of the aphid leaving, virions return to factories and the transmission body, which rapidly reforms in a form of vector "perceptive behavior" through the plant host (140)(141)(142). Horizontal transmission of viruses between insects may also involve MT-regulated structures called occlusion bodies.…”