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Tomato yellow leaf curl virus (TYLCV) is a monopartite begomovirus and the causal agent of the destructive tomato leaf curl disease 7. Whether members of this family encode additional small proteins, below the arbitrary 10 kDa threshold established following identification of the first geminivirus species, remains elusive. Although geminivirus-encoded proteins are described as multifunctional, how the plethora of tasks required for a fruitful infection can be performed by only 4–8 proteins is an intriguing biological puzzle. In order to accomplish a successful infection, geminiviruses must tailor the cellular environment to favor their replication and spread for this purpose, they modify the transcriptional landscape of the infected cell, re-direct post-transcriptional modifications, and interfere with hormone signaling, among other processes (reviewed in 4, 5, 6), ultimately suppressing anti-viral defenses, creating conditions favorable to viral replication, and manipulating plant development. Eventually, the virus must move intracellularly, intercellularly, and systemically, invading new cells and making virions available for acquisition by the vector. Rolling-circle replication ensues, by which new ssDNA copies of the viral genome are produced. Following transmission by an insect vector, the geminiviral DNA genome must be released from the virion and reach the nucleus, where it will be converted into a double-stranded (ds) DNA replicative intermediate this dsDNA molecule will serve as template for the transcription of viral genes, including the replication-associated protein (Rep), which reprograms the cell cycle and recruits the host DNA replication machinery. The geminiviral infection cycle is complex, and multiple steps remain to be fully elucidated. Members of this family have small genomes, composed of one or two DNA molecules of less than 3 Kb each, in which the use of coding space is optimized by bidirectional and partially overlapping open reading frames (ORFs): in one <3 Kb molecule, geminiviruses contain up to 7 ORFs, with a known maximum of 8 viral proteins per virus. This family includes nine genera, based on host range, insect vector, and genome structure: Becurtovirus, Begomovirus, Curtovirus, Eragrovirus, Mastrevirus, Topocuvirus, Turncurtovirus, Capulavirus, and Grablovirus 3 most species described to date belong to the genus Begomovirus. Geminiviruses are a family of plant viruses with circular, single-stranded (ss) DNA genomes causing devastating diseases in crops around the globe.
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Nevertheless, higher numbers of virus-encoded proteins might enable more sophisticated infection mechanisms, and therefore maximization of the coding space would be expected to be an advantage to the pathogen. Most viruses have small genome sizes, with the concomitant limitation in coding capacity in order to overcome the restrictions imposed by their reduced proteome, viruses have evolved to encode multifunctional proteins that efficiently target hub proteins in their host cells (reviewed in 1, 2). Viruses are intracellular parasites that heavily rely on the host cell machinery to complete their infectious cycle. These results imply that the repertoire of geminiviral proteins can be expanded, and that getting a comprehensive overview of the molecular plant-geminivirus interactions will require the detailed study of small ORFs so far neglected.
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We prove that the largest of these additional ORFs, which we name V3, is required for full viral infection, and that the V3 protein localizes in the Golgi apparatus and functions as an RNA silencing suppressor. Using tomato yellow leaf curl virus, we demonstrate that some of these small ORFs are expressed during the infection, and that the encoded proteins display specific subcellular localizations. Here, we show that geminiviral genomes contain additional ORFs. Geminivirus-encoded proteins are traditionally identified by applying a 10-kDa arbitrary threshold however, it is increasingly clear that small proteins play relevant roles in biological systems, which calls for the reconsideration of this criterion. Geminiviruses are plant viruses with limited coding capacity.