Abstract
Rice tungro disease is caused by synergistic interaction of an RNA picorna-like virus Rice tungro spherical virus (RTSV) and a DNA pararetrovirus Rice tungro bacilliform virus (RTBV). It is spread by insects owing to an RTSV-encoded transmission factor. RTBV has evolved a ribosome shunt mechanism to initiate translation of its pregenomic RNA having a long and highly structured leader. We found that a long leader of RTSV genomic RNA remarkably resembles the RTBV leader: both contain several short ORFs (sORFs) and potentially fold into a large stem-loop structure with the first sORF terminating in front of the stem basal helix. Using translation assays in rice protoplasts and wheat germ extracts, we show that, like in RTBV, both initiation and proper termination of the first sORF translation in front of the stem are required for shunt-mediated translation of a reporter ORF placed downstream of the RTSV leader. The base pairing that forms the basal helix is required for shunting, but its sequence can be varied. Shunt efficiency in RTSV is lower than in RTBV. But in addition to shunting the RTSV leader sequence allows relatively efficient linear ribosome migration, which also contributes to translation initiation downstream of the leader. We conclude that RTSV and RTBV have developed a similar, sORF-dependent shunt mechanism possibly to adapt to the host translation system and/or coordinate their life cycles. Given that sORF-dependent shunting also operates in a pararetrovirus Cauliflower mosaic virus and likely in other pararetroviruses that possess a conserved shunt configuration in their leaders it is tempting to propose that RTSV may have acquired shunt cis-elements from RTBV during their co-existence.
Highlights
Rice tungro disease is a significant constraint for rice cultivation in South and Southeast Asia
It is caused by a synergistic interaction of two viruses, Rice tungro bacilliform virus (RTBV) and Rice tungro spherical virus (RTSV)
We demonstrate that a similar shunt mechanism has been developed by the RNA picorna-like virus RTSV and the DNA pararetrovirus RTBV that form a disease complex in rice
Summary
Rice tungro disease is a significant constraint for rice cultivation in South and Southeast Asia. RTBV on its own cannot be transmitted from plant to plant, but it can do so with the help of RTSV that encodes an insect transmission factor [1] This suggests that the two viruses have co-evolved into a unique disease complex, in which partners may have developed specialized and shared mechanisms enabling the complex to establish systemic infection and to accumulate in the same plant tissues in order to be cotransmitted. Instead, compelling evidence indicates that plant pararetroviruses have evolved a ribosome shunt mechanism, which combines features of 59 end-dependent scanning and internal initiation, to translate
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