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Network dynamics of eukaryotic LTR retroelements beyond phylogenetic trees.
Biol Direct. 2009 Nov 02; 4:41.BD

Abstract

BACKGROUND

Sequencing projects have allowed diverse retroviruses and LTR retrotransposons from different eukaryotic organisms to be characterized. It is known that retroviruses and other retro-transcribing viruses evolve from LTR retrotransposons and that this whole system clusters into five families: Ty3/Gypsy, Retroviridae, Ty1/Copia, Bel/Pao and Caulimoviridae. Phylogenetic analyses usually show that these split into multiple distinct lineages but what is yet to be understood is how deep evolution occurred in this system.

RESULTS

We combined phylogenetic and graph analyses to investigate the history of LTR retroelements both as a tree and as a network. We used 268 non-redundant LTR retroelements, many of them introduced for the first time in this work, to elucidate all possible LTR retroelement phylogenetic patterns. These were superimposed over the tree of eukaryotes to investigate the dynamics of the system, at distinct evolutionary times. Next, we investigated phenotypic features such as duplication and variability of amino acid motifs, and several differences in genomic ORF organization. Using this information we characterized eight reticulate evolution markers to construct phenotypic network models.

CONCLUSION

The evolutionary history of LTR retroelements can be traced as a time-evolving network that depends on phylogenetic patterns, epigenetic host-factors and phenotypic plasticity. The Ty1/Copia and the Ty3/Gypsy families represent the oldest patterns in this network that we found mimics eukaryotic macroevolution. The emergence of the Bel/Pao, Retroviridae and Caulimoviridae families in this network can be related with distinct inflations of the Ty3/Gypsy family, at distinct evolutionary times. This suggests that Ty3/Gypsy ancestors diversified much more than their Ty1/Copia counterparts, at distinct geological eras. Consistent with the principle of preferential attachment, the connectivities among phenotypic markers, taken as network-represented combinations, are power-law distributed. This evidences an inflationary mode of evolution where the system diversity; 1) expands continuously alternating vertical and gradual processes of phylogenetic divergence with episodes of modular, saltatory and reticulate evolution; 2) is governed by the intrinsic capability of distinct LTR retroelement host-communities to self-organize their phenotypes according to emergent laws characteristic of complex systems.

REVIEWERS

This article was reviewed by Eugene V. Koonin, Eric Bapteste, and Enmanuelle Lerat (nominated by King Jordan).

Authors+Show Affiliations

Institut Cavanilles de Biodiversitat i Biologia Evolutiva (ICBIBE), Universitat de València, Paterna, Valencia, Spain. carlos.llorens@uv.esNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info available

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

19883502

Citation

Llorens, Carlos, et al. "Network Dynamics of Eukaryotic LTR Retroelements Beyond Phylogenetic Trees." Biology Direct, vol. 4, 2009, p. 41.
Llorens C, Muñoz-Pomer A, Bernad L, et al. Network dynamics of eukaryotic LTR retroelements beyond phylogenetic trees. Biol Direct. 2009;4:41.
Llorens, C., Muñoz-Pomer, A., Bernad, L., Botella, H., & Moya, A. (2009). Network dynamics of eukaryotic LTR retroelements beyond phylogenetic trees. Biology Direct, 4, 41. https://doi.org/10.1186/1745-6150-4-41
Llorens C, et al. Network Dynamics of Eukaryotic LTR Retroelements Beyond Phylogenetic Trees. Biol Direct. 2009 Nov 2;4:41. PubMed PMID: 19883502.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Network dynamics of eukaryotic LTR retroelements beyond phylogenetic trees. AU - Llorens,Carlos, AU - Muñoz-Pomer,Alfonso, AU - Bernad,Lucia, AU - Botella,Hector, AU - Moya,Andrés, Y1 - 2009/11/02/ PY - 2009/10/26/received PY - 2009/11/02/accepted PY - 2009/11/4/entrez PY - 2009/11/4/pubmed PY - 2010/3/5/medline SP - 41 EP - 41 JF - Biology direct JO - Biol Direct VL - 4 N2 - BACKGROUND: Sequencing projects have allowed diverse retroviruses and LTR retrotransposons from different eukaryotic organisms to be characterized. It is known that retroviruses and other retro-transcribing viruses evolve from LTR retrotransposons and that this whole system clusters into five families: Ty3/Gypsy, Retroviridae, Ty1/Copia, Bel/Pao and Caulimoviridae. Phylogenetic analyses usually show that these split into multiple distinct lineages but what is yet to be understood is how deep evolution occurred in this system. RESULTS: We combined phylogenetic and graph analyses to investigate the history of LTR retroelements both as a tree and as a network. We used 268 non-redundant LTR retroelements, many of them introduced for the first time in this work, to elucidate all possible LTR retroelement phylogenetic patterns. These were superimposed over the tree of eukaryotes to investigate the dynamics of the system, at distinct evolutionary times. Next, we investigated phenotypic features such as duplication and variability of amino acid motifs, and several differences in genomic ORF organization. Using this information we characterized eight reticulate evolution markers to construct phenotypic network models. CONCLUSION: The evolutionary history of LTR retroelements can be traced as a time-evolving network that depends on phylogenetic patterns, epigenetic host-factors and phenotypic plasticity. The Ty1/Copia and the Ty3/Gypsy families represent the oldest patterns in this network that we found mimics eukaryotic macroevolution. The emergence of the Bel/Pao, Retroviridae and Caulimoviridae families in this network can be related with distinct inflations of the Ty3/Gypsy family, at distinct evolutionary times. This suggests that Ty3/Gypsy ancestors diversified much more than their Ty1/Copia counterparts, at distinct geological eras. Consistent with the principle of preferential attachment, the connectivities among phenotypic markers, taken as network-represented combinations, are power-law distributed. This evidences an inflationary mode of evolution where the system diversity; 1) expands continuously alternating vertical and gradual processes of phylogenetic divergence with episodes of modular, saltatory and reticulate evolution; 2) is governed by the intrinsic capability of distinct LTR retroelement host-communities to self-organize their phenotypes according to emergent laws characteristic of complex systems. REVIEWERS: This article was reviewed by Eugene V. Koonin, Eric Bapteste, and Enmanuelle Lerat (nominated by King Jordan). SN - 1745-6150 UR - https://www.unboundmedicine.com/medline/citation/19883502/Network_dynamics_of_eukaryotic_LTR_retroelements_beyond_phylogenetic_trees_ L2 - https://biologydirect.biomedcentral.com/articles/10.1186/1745-6150-4-41 DB - PRIME DP - Unbound Medicine ER -