Impact Factor 4.076

The 3rd most cited journal in Microbiology

This article is part of the Research Topic

Genome Invading RNA Networks

Editorial ARTICLE Provisionally accepted The full-text will be published soon. Notify me

Front. Microbiol. | doi: 10.3389/fmicb.2018.00581

Editorial: Genome Invading RNA-Networks

  • 1Molecular Biology and Biochemistry, University of California, Irvine, United States
  • 2telos - Philosophische Praxis, Austria

It has been long accepted that newly acquired biological information is mostly derived from random‚ error-based’ events (Eigen 1971). However, the serial nature of acquiring such random events makes it very difficult to account for the origin or modification of regulatory networks. There is now abundant empirical evidence establishing the crucial role of non-coding DNA (acting through the expression of RNA with its complex biology) to create regulatory control (Mattick 2003, Atkins et al. 2011). Along with the parallel comeback of regulatory RNA in virology, RNA is now at center stage in how we think about complex organisms (Koonin et al. 2006, Atkins et al. 2011).

Regulatory RNAs derive from infectious events and can co-operate, build communities, generate nucleotide sequences de novo and insert/delete themselves into host genetic content (Villarreal 2005, Koonin 2009). In this sense genome invading RNA-networks determine host genetic identities (self recognition) throughout all kingdoms including the virosphere (Britten 2004, Marraffini and Sontheimer 2010, Villarreal 2011a). But inclusion of a transmissive viral RNA biology differs fundamentally from conventional thinking in that it represents a vertical domain of life providing vast amounts of linked information not derrived from direct ancestors (Villarreal 2014). Interestingly single RNA stem loops react as physico-chemical entities exclusively, whereas with the network-cooperation of various RNA stem-loops in a module-like manner biological selection emerges (Manrubia and Briones 2007, Vaidya 2012, Higgs and Lehman 2015). Additionally co-operating RNAs outcompete selfish genetic parasites (Hayden and Lehman 2006, Vaidya et al. 2012).

Thus we can argue, that for DNA based organisms, the introduction of infective collectives of RNA groups are a central driving force of evolution. Such RNA groups are co-adapted from persistent infectious agents and now serve as regulatory tools in nearly all cellular processes (Witzany 2016) as documented in several retrovirus derived mobile genetic elements (Brosius 1999, Villarreal 2011b, Chuong et al. 2016). Additionally, the resulting productive RNA-networks constantly produce new sequence space (i.e. complex regulation) which not only further serve as adaptation tools for their cell-based host organisms but also provides crucial roles in evolutionary novelty (Villarreal 2011b). This RNA productivity results out of the empirical fact that a single RNA sequence can fold into different and unrelated secondary structures with different functions in a (environmentally determined) context-depending way (Schultes and Bartel 2000).

Infection derived RNAs serve as the agents of regulatory networks in the cellular transcriptome (Feschotte 2008, Briones et al. 2009, Koonin 2009, Villarreal and Witzany 2010). Without transcription from the genetic storage medium of DNA into the living world of such RNA agents, no relevant genetic process in the cellular transcriptome can be initiated (Volff 2006). RNAs, with their inherent repeat syntax, format the expression of coding sequences and organize the coherent line-up of timely coordinated steps of replication (Shapiro and Sternberg 2005). The transport of genetic information to the progeny cells is also coordinated by these agents (Spadafora 2017). Furthermore, they are crucial for the cooperation between networks of RNA-stem loops to constitute important nucleoprotein complexes such as ribosome, spliceosome, and editosome (Witzany 2011). Therefore, such RNA groups are essential for complex order of genome constructions (Witzany 2014).

Additionally of interest is that infectious non-coding RNAs insert preferentially in non-coding DNA areas, whereas coding DNA usually is not the target (Bushman 2003, Mitchell et al 2004, Bartel 2009). In this perspective the non-coding DNA is the preferred habitat to settle down by infectious RNAs, e.g. y-chromosome in human genomes (Shapiro 2002, Villarreal 2009, Lambowitz and Zimmerly 2011). This may indicate that the preferred change in evolutionary processes occurs in regulatory sections and not in the information storage coding for proteins, the main source for “mutations” in previous theoretical concepts of evolution (Villarreal and Witzany 2013).

Frontiers Research Topic Genome Invading RNA-Networks highlightes various RNA networks being active in host genomes.
Gaurav Sablok et al. (2017) discussed classification, identification and roles of tRNA derived smallRNAs across plants and their potential involvement in abiotic and biotic stresses. Lu Wang et al. (2017) investigated how retrotransposon insertion polymorphisms can impact human health and disease. Karin Moelling et al. (2017) demonstrated that RNase H-like activities of retroviruses, TEs, and phages, have built up innate and adaptive immune systems throughout all domains of life. Sheng-Rui Liu at al. (2017) summarize recent advances in understanding the roles of miRNAs involved in the plant defense against viruses and viral counter-defense. Marek Malicki et al. (2017) review three retrotransposon classes that might represent a domestication of the selfish elements. Laleh Habibi and collegue (2017) exemplified direct action of RNA networks in shaping the genome. Anja Pecman et al. (2017) compared two different approaches for detection and discovery of plant viruses and viroids. Shohei Nagata et al. (2017) found that sequence changes in the RNase H domain and the reverse transcriptase connection domain are responsible for subtype classification. Hany Zinad et al. (2017) suggest that natural antisense transcripts interfere with their corresponding sense transcript to elicit concordant and discordant regulation. Eric Ottesen et al. (2017) describe how the abundance of Alu-like sequences may contribute toward Survival Motor Neuron gene pathogenesis. Ascensión Ariza-Mateos and collegue (2017) show how RNA viruses mimic key factors of the host cell. Corrado Spadafora (2017) found that spermatozoa act as collectors of somatic information and as delivering vectors to the next generation. Daniel Frías-Lasserre and collegue (2017) demonstrate how current epigenetic advances on non-coding RNAs has changed the perspective on evolutionary relevant variations. Luis Scolaro et al. (2017) demonstrate that evolutive processes for viruses are now interpreted as coordinated phenomenon that leads to global non-random remodeling of the population. Herve Seligman and collegue (2017) found that ribosomal RNA stem-loop hairpins resemble those formed by viruses and short parasitic repeats infesting bacterial genomes. Cheng Fu et al. (2017) provide deep insights into the molecular mechanisms of influenza virus infection.

More and more empirical evidence establishes the crucial role of natural genetic content editors such as viruses and RNA-networks to create genetic novelty, complex regulatory control, epigenetics, genetic identity, immunity, inheritance vectors, new sequence space, evolution of complex organisms and evolutionary transitions (Villarreal and Witzany 2015, Chuong et al. 2016, Spadafora this issue).

Genetic identities of RNA-networks such as e.g., group I introns, group II introns, viroids, RNA viruses, retrotransposons, LTRs, non-LTRs, SINEs, LINEs, Alus invade and even persist in host genomes (Villarreal 2009). Also mixed networks of RNA- and DNA viruses derived parts that integrate into host genomes have been found (Stedman 2015), not forgetting persistent retroviral infections and the essential roles of reverse transcriptases and related RNase H endonucleases (Moelling and Broecker 2015).

Highly dynamic RNA-Protein networks such as ribosome, editosome and spliceosome together with several context-dependent sequence modificating interactions, such as pseudo-knotting, frame-shifting, loop-kissing, by-passing translation generate a large variety of RNA regulatory functions out of a given DNA content (Cao et al. 2014, Denzler et al. 2014, Peselis and Serganov 2014, Samatova et al. 2014, Keam and Hutvagner 2015, Atkins et al. 2016).

There are reasonable expectations that this new empirically based perspective on the evolution of genetic novelty and biological information will have more explanatory power in the future than the „error-replication“ narrative of the last century.

Keywords: RNA Networks, genetic identities, regulatory RNAs, infectious agents, Natural Genetic Content Operators

Received: 11 Feb 2018; Accepted: 14 Mar 2018.

Edited by:

David Gilmer, Université de Strasbourg, France

Reviewed by:

Cristina Romero-López, Institute of Parasitology and Biomedicine "López-Neyra" (CSIC), Spain
Roland Marquet, UPR9002 Architecture et Réactivité de l'ARN, France  

Copyright: © 2018 Villarreal and Witzany. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Guenther Witzany, telos - Philosophische Praxis, Buermoos, Austria,