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A Lysine Residue Essential for Geminivirus Replication Also Controls Nuclear Localization of the Tomato Yellow Leaf Curl Virus Rep Protein.

ABSTRACT: Geminiviruses are single-stranded DNA (ssDNA) viruses that infect a wide range of plants. To promote viral replication, geminiviruses manipulate the host cell cycle. The viral protein Rep is essential to reprogram the cell cycle and then initiate viral DNA replication by interacting with a plethora of nuclear host factors. Even though many protein domains of Rep have been characterized, little is known about its nuclear targeting. Here, we show that one conserved lysine in the N-terminal part of Rep is pivotal for nuclear localization of the Rep protein from Tomato yellow leaf curl virus (TYLCV), with two other lysines also contributing to its nuclear import. Previous work had identified that these residues are essential for Rep from Tomato golden mosaic virus (TGMV) to interact with the E2 SUMO-conjugating enzyme (SCE1). We here show that mutating these lysines leads to nuclear exclusion of TYLCV Rep without compromising its interaction with SCE1. Moreover, the ability of TYLCV Rep to promote viral DNA replication also depends on this highly conserved lysine independently of its role in nuclear import of Rep. Our data thus reveal that this lysine potentially has a broad role in geminivirus replication, but its role in nuclear import and SCE1 binding differs depending on the Rep protein examined.IMPORTANCE Nuclear activity of the replication initiator protein (Rep) of geminiviruses is essential for viral replication. We now define that one highly conserved lysine is important for nuclear import of Rep from three different begomoviruses. To our knowledge, this is the first time that nuclear localization has been mapped for any geminiviral Rep protein. Our data add another key function to this lysine residue, besides its roles in viral DNA replication and interaction with host factors, such as the SUMO E2-conjugating enzyme.

SUBMITTER: Maio F

PROVIDER: S-EPMC6498046 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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A Lysine Residue Essential for Geminivirus Replication Also Controls Nuclear Localization of the Tomato Yellow Leaf Curl Virus Rep Protein.

Maio Francesca F Arroyo-Mateos Manuel M Bobay Benjamin G BG Bejarano Eduardo R ER Prins Marcel M van den Burg Harrold A HA

Journal of virology 20190501 10

Geminiviruses are single-stranded DNA (ssDNA) viruses that infect a wide range of plants. To promote viral replication, geminiviruses manipulate the host cell cycle. The viral protein Rep is essential to reprogram the cell cycle and then initiate viral DNA replication by interacting with a plethora of nuclear host factors. Even though many protein domains of Rep have been characterized, little is known about its nuclear targeting. Here, we show that one conserved lysine in the N-terminal part of ...[more]

PMID: 30842320

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Project description:BackgroundViruses have evolved to create a cellular environment permissive for viral replication in susceptible hosts. Possibly both enabling and resulting from these virus-triggered changes, infected hosts undergo a dramatic transcriptional reprogramming, the analysis of which can shed light on the molecular processes underlying the outcome of virus-host interactions. The study of the transcriptional changes triggered by the plant DNA viruses geminiviruses is potentially hampered by the low representation of infected cells in the total population, a situation that becomes extreme in those cases, like that of Tomato yellow leaf curl virus (TYLCV), in which the virus is restricted to phloem companion cells.ResultsIn order to gain insight into how different the transcriptional landscapes of TYLCV-infected cells or whole tissues of TYLCV-infected plants might be, here we compare the transcriptional changes in leaf patches infected with TYLCV by agroinfiltration or in systemic leaves of TYLCV-infected plants in Nicotiana benthamiana. Our results show that, in agreement with previous works, infection by TYLCV induces a dramatic transcriptional reprogramming; the detected changes, however, are not equivalent in local and systemic infections, with a much larger number of genes differentially expressed locally, and some genes responding in an opposite manner. Interestingly, a transcriptional repression of the auxin signalling pathway and a transcriptional activation of the ethylene signalling pathway were detected in both local and systemically infected samples. A transcriptional activation of defence was also detectable in both cases. Comparison with the transcriptional changes induced by systemic infection by the geminivirus Tobacco curly shoot virus (TbSV) shows common subsets of up- and down-regulated genes similarly affected by both viral species, unveiling a common transcriptional repression of terpenoid biosynthesis, a process also suppressed by the geminivirus Tomato yellow leaf curl China virus.ConclusionsTaken together, the results presented here not only offer insight into the transcriptional changes derived from the infection by TYLCV in N. benthamiana, but also demonstrate that the resolution provided by local and systemic infection approaches largely differs, highlighting the urge to come up with a better system to gain an accurate view of the molecular and physiological changes caused by the viral invasion.

Dataset Information

A Lysine Residue Essential for Geminivirus Replication Also Controls Nuclear Localization of the Tomato Yellow Leaf Curl Virus Rep Protein.

Publications

A Lysine Residue Essential for Geminivirus Replication Also Controls Nuclear Localization of the Tomato Yellow Leaf Curl Virus Rep Protein.

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