Genomic fossils reveal adaptation of non-autonomous pararetroviruses driven by concerted evolution of noncoding regulatory sequences

Chen, Sunlu; Zheng, Huizhen; Kishima, Yuji

doi:10.1371/journal.ppat.1006413

Cited by 9 publications

(6 citation statements)

References 79 publications

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“…While the replication of Caulimoviridae does not require integration into host genomes, endogenous plant pararetroviruses (EPRVs) were identified in many angiosperms in the pregenomic era (17), for example, banana (18) and tobacco (19). Genome-scale data provide important resources to explore the distribution and diversity of EPRVs within plant genomes, which would improve our understanding of the macroevolution of Caulimoviridae and the relationship between viruses and their hosts (20). By mining a variety of plant genomes, Geering et al (21) identified a novel lineage of EPRVs in flowering plants (angiosperms), sometimes with a high copy number, which was designated "Florendovirus" and was thought to constitute a new genus within the Caulimoviridae.…”

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confidence: 99%

Euphyllophyte Paleoviruses Illuminate Hidden Diversity and Macroevolutionary Mode of Caulimoviridae

Gong

Han

2018

J Virol

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Endogenous viral elements (paleoviruses) provide "molecular fossils" for studying the deep history and macroevolution of viruses. Endogenous plant pararetroviruses (EPRVs) are widespread in angiosperms, but little is known about EPRVs in earlier-branching plants. Here we use a large-scale phylogenomic approach to investigate the diversity and macroevolution of plant pararetroviruses (formally known as ). We uncover an unprecedented and unappreciated diversity of EPRVs within the genomes of gymnosperms and ferns. The known angiosperm viruses constitute only a minor part of the diversity. By characterizing the distribution of EPRVs, we show that no major euphyllophyte lineages escape the activity of , raising the possibility that many exogenous remain to be discovered in euphyllophytes. We find that the copy numbers of EPRVs are generally high, suggesting that EPRVs might define a unique group of repetitive elements and represent important components of euphyllophyte genomes. Evolutionary analyses suggest an ancient origin of and at least three independent origins of in angiosperms. Our findings reveal the remarkable diversity of and have important implications for understanding the origin and macroevolution of plant pararetroviruses. Few viruses have been documented in plants outside angiosperms. Viruses can occasionally integrate into host genomes, forming endogenous viral elements (EVEs). Endogenous plant pararetroviruses (EPRVs) are widespread in angiosperms. In this study, we performed comprehensive comparative and phylogenetic analyses of EPRVs and found that EPRVs are present in the genomes of gymnosperms and ferns. We identified numerous EPRVs in gymnosperm and fern genomes, revealing an unprecedented depth in the diversity of plant pararetroviruses. Plant pararetroviruses mainly underwent cross-species transmission, and angiosperm pararetroviruses arose at least three times. Our study provides novel insights into the diversity and macroevolution of plant pararetroviruses.

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confidence: 99%

Euphyllophyte Paleoviruses Illuminate Hidden Diversity and Macroevolutionary Mode of Caulimoviridae

Gong

Han

2018

J Virol

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“…EPRVs in hosts record past viral infections [11] and have coevolved with their hosts, providing an opportunity to study the evolutionary correlation between viruses and hosts [14]. In the current study, the coevolution of bananas and BSVs in China was investigated (Figure 7) by analyzing the BEVs gene characteristics, BEVs distribution in different banana chromosomes, and the various cultivated bananas, together with the findings of previous research [9,20], to reveal the coevolutionary relationship between BSVs and bananas.…”

Section: Coevolution Of Bevs With Bsvs and Bananasmentioning

confidence: 93%

“…EPRVs, as viral fossils, play a critical role in gene transfer from virus to host [11]. They have become an essential component of the genomes of host plants with time [31].…”

Section: Bevs In Different Genotypes Of Bananasmentioning

confidence: 99%

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Distribution and Location of BEVs in Different Genotypes of Bananas Reveal the Coevolution of BSVs and Bananas

Rao,

Chen,

et al. 2023

IJMS

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Members of the family Caulimoviridae contain abundant endogenous pararetroviral sequences (EPRVs) integrated into the host genome. Banana streak virus (BSV), a member of the genus Badnavirus in this family, has two distinct badnaviral integrated sequences, endogenous BSV (eBSV) and banana endogenous badnavirus sequences (BEVs). BEVs are distributed widely across the genomes of different genotypes of bananas. To clarify the distribution and location of BEVs in different genotypes of bananas and their coevolutionary relationship with bananas and BSVs, BEVs and BSVs were identified in 102 collected banana samples, and a total of 327 BEVs were obtained and categorized into 26 BEVs species with different detection rates. However, the majority of BEVs were found in Clade II, and a few were clustered in Clade I. Additionally, BEVs and BSVs shared five common conserved motifs. However, BEVs had two unique amino acids, methionine and lysine, which differed from BSVs. BEVs were distributed unequally on most of chromosomes and formed hotspots. Interestingly, a colinear relationship of BEVs was found between AA and BB, as well as AA and SS genotypes of bananas. Notably, the chromosome integration time of different BEVs varied. Based on our findings, we propose that the coevolution of bananas and BSVs is driven by BSV Driving Force (BDF), a complex interaction between BSVs, eBSVs, and BEVs. This study provides the first clarification of the relationship between BEVs and the coevolution of BSVs and bananas in China.

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“…The mining and analysis of EVEs has had an important impact on the emerging field of paleovirology, with implications for the characterization of viral origins and evolution as well as host–virus and virus–virus coevolution ( Patel et al. 2011 ; Feschotte and Gilbert 2012 ; Aiewsakun and Katzourakis 2015a ; Chen et al. 2017 ).…”

Section: Introductionmentioning

confidence: 99%

Ancient Endogenous Pararetroviruses in Oryza Genomes Provide Insights into the Heterogeneity of Viral Gene Macroevolution

Chen

Saito

Encabo

et al. 2018

Genome Biology and Evolution

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Endogenous viral sequences in eukaryotic genomes, such as those derived from plant pararetroviruses (PRVs), can serve as genomic fossils to study viral macroevolution. Many aspects of viral evolutionary rates are heterogeneous, including substitution rate differences between genes. However, the evolutionary dynamics of this viral gene rate heterogeneity (GRH) have been rarely examined. Characterizing such GRH may help to elucidate viral adaptive evolution. In this study, based on robust phylogenetic analysis, we determined an ancient endogenous PRV group in Oryza genomes in the range of being 2.41–15.00 Myr old. We subsequently used this ancient endogenous PRV group and three younger groups to estimate the GRH of PRVs. Long-term substitution rates for the most conserved gene and a divergent gene were 2.69 × 10−8 to 8.07 × 10−8 and 4.72 × 10−8 to 1.42 × 10−7 substitutions/site/year, respectively. On the basis of a direct comparison, a long-term GRH of 1.83-fold was identified between these two genes, which is unexpectedly low and lower than the short-term GRH (>3.40-fold) of PRVs calculated using published data. The lower long-term GRH of PRVs was due to the slightly faster rate decay of divergent genes than of conserved genes during evolution. To the best of our knowledge, we quantified for the first time the long-term GRH of viral genes using paleovirological analyses, and proposed that the GRH of PRVs might be heterogeneous on time scales (time-dependent GRH). Our findings provide special insights into viral gene macroevolution and should encourage a more detailed examination of the viral GRH.

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Genomic fossils reveal adaptation of non-autonomous pararetroviruses driven by concerted evolution of noncoding regulatory sequences

Cited by 9 publications

References 79 publications

Euphyllophyte Paleoviruses Illuminate Hidden Diversity and Macroevolutionary Mode of Caulimoviridae

Euphyllophyte Paleoviruses Illuminate Hidden Diversity and Macroevolutionary Mode of Caulimoviridae

Distribution and Location of BEVs in Different Genotypes of Bananas Reveal the Coevolution of BSVs and Bananas

Ancient Endogenous Pararetroviruses in Oryza Genomes Provide Insights into the Heterogeneity of Viral Gene Macroevolution

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