Different forms of African cassava mosaic virus capsid protein within plants and virions

Hipp, Katharina; Zikeli, Kerstin; Kepp, Gabi; Schmid, Lena; Shoeman, Robert L.; Jurkowski, Tomasz P.; Kleinow, Tatjana; Jeske, Holger

doi:10.1016/j.virol.2019.01.018

Cited by 6 publications

(5 citation statements)

References 74 publications

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“…Mass spectrometry of tryptic digests of the protein in the bands confirmed their identity as the expected geminivirus coat proteins (Figure S2). As in previous studies, [25,[47][48][49], additional faster migrating forms of the coat protein can be seen. The presence of coat protein in fractions from the middle of the gradient suggests that, unlike the encapsidation of alphasatellite DNA, all the coat proteins were able to form particles with full-length cssDNA.…”

Section: Transencapsidation Of Ayvv Genome-length Dnasupporting

confidence: 84%

Requirements for the Packaging of Geminivirus Circular Single-Stranded DNA: Effect of DNA Length and Coat Protein Sequence

Saunders

Richardson

Lawson

et al. 2020

Viruses

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Geminivirus particles, consisting of a pair of twinned isometric structures, have one of the most distinctive capsids in the virological world. Until recently, there was little information as to how these structures are generated. To address this, we developed a system to produce capsid structures following the delivery of geminivirus coat protein and replicating circular single-stranded DNA (cssDNA) by the infiltration of gene constructs into plant leaves. The transencapsidation of cssDNA of the Begomovirus genus by coat protein of different geminivirus genera was shown to occur with full-length but not half-length molecules. Double capsid structures, distinct from geminate capsid structures, were also generated in this expression system. By increasing the length of the encapsidated cssDNA, triple geminate capsid structures, consisting of straight, bent and condensed forms were generated. The straight geminate triple structures generated were similar in morphology to those recorded for a potato-infecting virus from Peru. These finding demonstrate that the length of encapsidated DNA controls both the size and stability of geminivirus particles.

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Section: Transencapsidation Of Ayvv Genome-length Dnasupporting

confidence: 84%

Requirements for the Packaging of Geminivirus Circular Single-Stranded DNA: Effect of DNA Length and Coat Protein Sequence

Saunders

Richardson

Lawson

et al. 2020

Viruses

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“…The resulting amino acid substitution (S56N) may disrupt phosphorylation of the viral coat protein (CP). The corresponding serine residue in the CP of African cassava mosaic virus (S62) is phosphorylated (Hipp et al 2019). Repeated observation of this substitution strongly suggests that it is selectively beneficial under our experimental conditions, particularly in the two Col-0 plants inoculated with WT virus, which reached mutation frequencies of 34% and 36% (Figure 3).…”

Section: Resultsmentioning

confidence: 99%

“…The S56N substitution detected in 7 of the 11 plants in this experiment likely prevents phosphorylation, providing a possible explanation for its selective benefit. Hipp et al (2019) detected by mass spectrometry partial phosphorylation of three N-terminal residues (one homologous to the CabLCV residue) in the CP of African cassava mosaic virus. Hipp et al suggested that this phosphorylation may promote ubiquitin-dependent proteasomal degradation of CP, similar to degradation of tomato yellow leaf curl virus CP (Gorovits et al 2014(Gorovits et al , 2016.…”

Section: Cp and Host-genotype-specific Differences In Selection Pressurementioning

confidence: 99%

“…The N terminus of CP also functions in nuclear localization and in ssDNA binding during virion assembly (Unseld et al 2001(Unseld et al , 2004, so other effects remain possible. This amino acid position is conserved across many geminiviruses, with the serine sometimes replaced with threonine (Hipp et al 2019), another residue that can be phosphorylated. Therefore, it is possible that the within-plant selective advantage we have observed is counterbalanced by long-term costs, particularly if the substitution interferes with packaging and/or whitefly transmission.…”

Section: Cp and Host-genotype-specific Differences In Selection Pressurementioning

confidence: 99%

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Rapid multilocus adaptation of clonal cabbage leaf curl virus populations toArabidopsis thaliana

Hoyer

Wilkins

Munshi

et al. 2021

Preprint

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Cabbage leaf curl virus (CabLCV) has a bipartite single-stranded DNA genome and infects the model plant Arabidopsis thaliana. CabLCV serves as a model for the genus Begomovirus, members of which cause tremendous crop losses worldwide. We have used CabLCV as a model for within-plant virus evolution by inoculating individual plants with infectious clones of both wild-type and mutagenized versions of the CabLCV genome. Consistent with previous reports, detrimental substitutions in the Replication-associated gene (Rep) were readily compensated for by direct reversion and/or alternative mutations. A surprising number of common mutations were detected elsewhere in both viral segments (DNA-A and DNA-B) indicating convergent evolution and suggesting that CabLCV may not be as well adapted to A. thaliana as commonly presumed. Consistent with this idea, a spontaneous coat protein variant consistently rose to higher allele frequency in a hypersusceptible A. thaliana accession (Sei-0) than in another susceptible accession (Col-0). Numerous high-frequency mutations were also detected in a candidate Rep binding site in DNA-B. Our results reinforce the fact that spontaneous mutation of this type of virus occurs rapidly and can change the majority consensus sequence of a within-plant virus population in weeks.

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“…On that former basis, we had hypothesized that an interference with phosphorylation-induced ubiquitination of proteins might result in amino acid position-specific effects in plants and change viral symptoms (for a more detailed discussion see Kleinow et al, 2009b). Recent data for the CP of the bipartite begomovirus African cassava mosaic virus support the idea of phosphorylation-mediated proteolysis as an important regulatory cornerstone: a differential CP phosphorylation in plants coinciding with a high turnover rate of the protein indicates its ubiquitin-dependent degradation by the proteasome (Hipp et al, 2019). An ubiquitination and subsequent degradation by the proteasome has also been observed for the CP of the monopartite begomovirus tomato yellow leaf curl virus (Gorovits et al, 2014;Gorovits et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

Phosphorylations of the Abutilon Mosaic Virus Movement Protein Affect Its Self-Interaction, Symptom Development, Viral DNA Accumulation, and Host Range

et al. 2020

Self Cite

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The genome of bipartite geminiviruses in the genus Begomovirus comprises two circular DNAs: DNA-A and DNA-B. The DNA-B component encodes a nuclear shuttle protein (NSP) and a movement protein (MP), which cooperate for systemic spread of infectious nucleic acids within host plants and affect pathogenicity. MP mediates multiple functions during intra-and intercellular trafficking, such as binding of viral nucleoprotein complexes, targeting to and modification of plasmodesmata, and release of the cargo after cell-to-cell transfer. For Abutilon mosaic virus (AbMV), phosphorylation of MP expressed in bacteria, yeast, and Nicotiana benthamiana plants, respectively, has been demonstrated in previous studies. Three phosphorylation sites (T221, S223, and S250) were identified in its C-terminal oligomerization domain by mass spectrometry, suggesting a regulation of MP by posttranslational modification. To examine the influence of the three sites on the self-interaction in more detail, MP mutants were tested for their interaction in yeast by twohybrid assays, or by Förster resonance energy transfer (FRET) techniques in planta. Expression constructs with point mutations leading to simultaneous (triple) exchange of T221, S223, and S250 to either uncharged alanine (MP AAA), or phosphorylation chargemimicking aspartate residues (MP DDD) were compared. MP DDD interfered with MP-MP binding in contrast to MP AAA. The roles of the phosphorylation sites for the viral life cycle were studied further, using plant-infectious AbMV DNA-B variants with the same triple mutants each. When co-inoculated with wild-type DNA-A, both mutants infected N. benthamiana plants systemically, but were unable to do so for some other plant species of the families Solanaceae or Malvaceae. Systemically infected plants developed symptoms and viral DNA levels different from those of wild-type AbMV for most virus-plant combinations. The results indicate a regulation of diverse MP functions by posttranslational modifications and underscore their biological relevance for a complex host plant-geminivirus interaction.

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Different forms of African cassava mosaic virus capsid protein within plants and virions

Cited by 6 publications

References 74 publications

Requirements for the Packaging of Geminivirus Circular Single-Stranded DNA: Effect of DNA Length and Coat Protein Sequence

Requirements for the Packaging of Geminivirus Circular Single-Stranded DNA: Effect of DNA Length and Coat Protein Sequence

Rapid multilocus adaptation of clonal cabbage leaf curl virus populations toArabidopsis thaliana

Phosphorylations of the Abutilon Mosaic Virus Movement Protein Affect Its Self-Interaction, Symptom Development, Viral DNA Accumulation, and Host Range

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