Maize chlorotic mottle virus exhibits low divergence between differentiated regional sub-populations

Braidwood, Luke; Quito-Avila, Diego F.; Cabanas, Darlene; Bressan, Alberto; Wangai, Anne; Baulcombe, David C.

doi:10.1038/s41598-018-19607-4

Cited by 32 publications

(28 citation statements)

References 59 publications

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“…Comparison of the amino acid sequences of the viral proteins also exhibited high similarities, especially in the P7a, P111 and the CP regions as indicated in Table 5 . The 5′ and 3′UTRs were highly conserved in all the isolates under investigation confirming reports from previous studies ( Mahuku et al, 2015a ; Braidwood et al, 2018 ; Wamaitha et al, 2018 ).…”

Section: Discussionsupporting

confidence: 88%

“…MCMV genome sequence comparison with accessions from China, Africa and the USA reveals that MCMV is a highly conserved virus with identities ranging from 96 % to 99 %. This is typical of members of Tombusviridae where the diversity of nucleotides documented are between 0−0.02 with MCMV in the genus Machlomovirus recording lowest nucleotide diversities of 0.01 ( Varanda et al, 2014 and Braidwood et al, 2018 ). Comparison of the amino acid sequences of the viral proteins also exhibited high similarities, especially in the P7a, P111 and the CP regions as indicated in Table 5 .…”

Section: Discussionmentioning

confidence: 85%

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Occurrence, genetic diversity, and recombination of maize lethal necrosis disease-causing viruses in Kenya

et al. 2020

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Highlights Sugarcane mosaic virus (SCMV) and Maize chlorotic mottle virus (MCMV) were the only MLN causing viruses detected. MCMV and SCMV are widely distributed in all maize growing regions in Kenya. SCMV was more diverse and MCMV was largely conserved with little genetic diversity. MCMV alone can lead to severe MLN development. Genetic viral recombination signals detected only in SCMV viral genome samples.

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Section: Discussionsupporting

confidence: 88%

Section: Discussionmentioning

confidence: 85%

Occurrence, genetic diversity, and recombination of maize lethal necrosis disease-causing viruses in Kenya

et al. 2020

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“…MCMV, SCMV, MaYMV, and MATVs were distributed across Rwanda and detected in all areas sampled. As previously found, MCMV sequences in Rwanda were highly conserved(Braidwood et al, 2018), while SCMV sequences were highly diverse. MSV was detected at low rates, and was not detected in samples from the Eastern Province, Kigali, or three of four districts surveyed in the Western Province.…”

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confidence: 78%

Maize lethal necrosis viruses and other maize viruses in Rwanda

et al. 2020

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Maize lethal necrosis (MLN) is emergent in East Africa, first reported in 2011 in Kenya, and is devastating to maize production in the region. MLN is caused by coinfection of maize with the emergent maize chlorotic mottle virus (MCMV) and any of several maize‐infecting potyviruses endemic in East Africa and worldwide. Here, we examined the distribution of MCMV and sugarcane mosaic virus (SCMV), the major viruses contributing to MLN in Rwanda. These and other viruses in maize across Rwanda were further characterized by deep sequencing. When identified, MCMV had high titres and minimal sequence variability, whereas SCMV showed moderate titres and high sequence variability. Deep sequencing also identified maize streak virus and other maize‐associated viruses, including a previously described polerovirus, maize yellow mosaic virus, and barley yellow dwarf virus, diverse maize‐associated totiviruses, maize‐associated pteridovirus, Zea mays chrysovirus 1, and a maize‐associated betaflexivirus. Detection of each virus was confirmed in maize samples by reverse transcription polymerase chain reaction.

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“…Given the severe losses it has caused since 2011 in mixed infection with the potyvirus SCMV in East Africa [7, 63, 64], China [10, 65, 66] and Ecuador [13], and given the cost of screening seed worldwide to ensure absence of this seed-transmitted virus [63, 67, 68], MCMV is almost certainly the most economically important virus in the >76-member Tombusviridae family. Thus, it is imperative to understand the life cycle of MCMV, including translation, to identify molecular targets for genetic approaches to control this virus.…”

Section: Discussionmentioning

confidence: 99%

The RNA of maize chlorotic mottle virus - the essential virus in maize lethal necrosis disease - is translated via a panicum mosaic virus-like cap-independent translation element

Carino

Scheets

Miller

2020

Preprint

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Maize chlorotic mottle virus (MCMV) combines with a potyvirus in maize lethal necrosis disease (MLND), an emerging disease worldwide that often causes catastrophic yield loss. To inform resistance strategies, we characterized the translation initiation mechanism of MCMV. We report that, like other tombusvirids, MCMV RNA contains a cap-independent translation element (CITE) in its 3’ untranslated region (UTR). The MCMV 3’ CITE (MTE) was mapped to nucleotides 4164-4333 in the genomic RNA. SHAPE probing revealed that the MTE is a variant of the panicum mosaic virus-like 3’ CITE (PTE). Like the PTE, electrophoretic mobility shift assays (EMSAs) indicated that eukaryotic translation initiation factor 4E (eIF4E) binds the MTE despite the absence of a m7GpppN cap structure, which is normally required for eIF4E to bind RNA. The MTE interaction with eIF4E suggests eIF4E may be a soft target for engineered resistance to MCMV. Using a luciferase reporter system, mutagenesis to disrupt and restore base pairing revealed that the MTE interacts with the 5’ UTRs of both genomic RNA and the 3’-coterminal subgenomic RNA1 via long-distance kissing stem-loop base pairing to facilitate translation in wheat germ extract and in protoplasts. However, the MTE is a relatively weak stimulator of translation and has a weak, if any, pseudoknot, which is present in the most active PTEs. Most mutations designed to form a pseudoknot decreased translation activity. Mutations in the viral genome that reduced or restored translation prevented and restored virus replication, respectively, in maize protoplasts and in plants. We propose that MCMV, and some other positive strand RNA viruses, favors a weak translation element to allow highly efficient viral RNA synthesis.Author SummaryIn recent years, maize lethal necrosis disease has caused massive crop losses in East Africa and Ecuador. It has also emerged in East Asia. Maize chlorotic mottle virus (MCMV) infection is required for this disease. While some tolerant maize lines have been identified, there are no known resistance genes that confer full immunity to MCMV. In order to design better resistance strategies against MCMV, we focused on how the MCMV genome is translated, the first step of gene expression required for infection by all positive strand RNA viruses. We identified a structure (cap-independent translation element) in the 3’ untranslated region of the viral RNA genome that allows the virus to usurp a host translation initiation factor in a way that differs from host mRNA interactions with the translational machinery. This difference may guide engineering of – or breeding for – resistance to MCMV. Moreover, this work adds to the diversity of known eukaryotic translation initiation mechanisms, as it provides more information on mRNA structural features that permit noncanonical interaction with a translation factor. Finally, owing to the conflict between ribosomes translating and viral replicase copying viral RNA, we propose that MCMV has evolved a relatively weak translation element in order to permit highly efficient RNA synthesis, and that this replication-translation trade-off may apply to other positive strand RNA viruses.

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Maize chlorotic mottle virus exhibits low divergence between differentiated regional sub-populations

Cited by 32 publications

References 59 publications

Occurrence, genetic diversity, and recombination of maize lethal necrosis disease-causing viruses in Kenya

Occurrence, genetic diversity, and recombination of maize lethal necrosis disease-causing viruses in Kenya

Maize lethal necrosis viruses and other maize viruses in Rwanda

The RNA of maize chlorotic mottle virus - the essential virus in maize lethal necrosis disease - is translated via a panicum mosaic virus-like cap-independent translation element

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