Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-23T17:13:29.487Z Has data issue: false hasContentIssue false

Re-criticizing RNA-mediated cell evolution: a radical perspective

Published online by Cambridge University Press:  06 July 2015

Christos Kotakis*
Affiliation:
Institute of Plant Biology, Biological Research Center, Hungarian Academy of Sciences, Szeged, H-6726, Hungary

Abstract

Genetic inter-communication of the nucleic-organellar dual in eukaryotes is dominated by DNA-directed phenomena. RNA regulatory circuits have also been observed in artificial laboratory prototypes where gene transfer events are reconstructed, but they are excluded from the primary norm due to their rarity. Recent technical advances in organellar biotechnology, genome engineering and single-molecule tracking give novel experimental insights on RNA metabolism not only at cellular level, but also on organismal survival. Here, I put forward a hypothesis for RNA's involvement in gene piece transfer, taken together the current knowledge on the primitive RNA character as a biochemical modulator with model organisms from peculiar natural habitats. It is proposed that RNA molecules of special structural signature and functional identity can drive evolution, integrating the ecological pressure of environmental oscillations into genome imprinting by buffering-out epigenetic aberrancies.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Accomplishment of the unfulfilled; a parenthetical trait of simplicity

References

Alleman, M., Sidorenko, L., McGinnis, K., Seshadri, V., Dorweiler, J.E., White, J., Sikkink, K. & Chandler, V.L. (2006). An RNA-dependent RNA polymerase is required for paramutation in maize. Nature 442(7100), 295298.Google Scholar
Antonicka, H. & Shoubridge, E.A. (2015). Mitochondrial RNA granules are centers for posttranscriptional RNA processing and ribosome biogenesis. Cell Rep. pii: S2211-1247(15)00055-8. doi: 10.1016/j.celrep.2015.01.030 Google Scholar
Archibald, J.M. (2015). Genomic perspectives on the birth and spread of plastids. Proc. Natl. Acad. Sci. USA. pii: 201421374.Google Scholar
Bassett, A.R., Tibbit, C., Ponting, C.P. & Liu, J.L. (2013). Highly efficient targeted mutagenesis of Drosophila with the CRISPR/Cas9 system. Cell Rep. 4(1), 220228.Google Scholar
Bhaya, D., Davison, M. & Barrangou, R. (2011). CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation. Annu. Rev. Genet. 45, 273297.Google Scholar
Bock, R. & Timmis, J.N. (2008). Reconstructing evolution: gene transfer from plastids to the nucleus. Bioessays 30(6), 556566.CrossRefGoogle ScholarPubMed
Buxbaum, A.R., Haimovich, G. & Singer, R.H. (2015). In the right place at the right time: visualizing and understanding mRNA localization. Nat. Rev. Mol. Cell. Biol. 16(2), 95109.Google Scholar
Cho, S.K., Chaabane, S.B., Shah, P., Poulsen, C.P. & Yang, S.W. (2014). COP1 E3 ligase protects HYL1 to retain microRNA biogenesis. Nat. Commun. 5, 5867.Google Scholar
Cockell, C.S. (2014). Habitable worlds with no signs of life. Philos. Trans. A Math. Phys. Eng. Sci. 372(2014), 20130082.Google Scholar
Eberle, A.B. & Visa, N. (2014). Quality control of mRNP biogenesis: networking at the transcription site. Semin. Cell Dev. Biol. 32, 3746.CrossRefGoogle ScholarPubMed
Germain, A., Hotto, A.M., Barkan, A. & Stern, D.B. (2013). RNA processing and decay in plastids. Wiley Interdiscip. Rev. RNA 4(3), 295316.Google Scholar
Gómez, G. & Pallás, V. (2010). Noncoding RNA mediated traffic of foreign mRNA into chloroplasts reveals a novel signaling mechanism in plants. PLoS ONE 5(8), e12269.CrossRefGoogle ScholarPubMed
Huang, C.Y., Ayliffe, M.A. & Timmis, J.N. (2003). Direct measurement of the transfer rate of chloroplast DNA into the nucleus. Nature 422(6927), 7276.CrossRefGoogle ScholarPubMed
Jheeta, S. (2013). Horizontal gene transfer and its part in the reorganisation of genetics during the LUCA epoch. Life (Basel) 3(4), 518523.Google ScholarPubMed
Jheeta, S. & Joshi, P.C. (2014). Prebiotic RNA synthesis by montmorillonite catalysis. Life (Basel) 4(3), 318330.Google Scholar
Karginov, F.V. & Hannon, G.J. (2010). The CRISPR system: small RNA-guided defense in bacteria and archaea. Mol. Cell 37(1), 719.Google Scholar
Kotakis, C. (2015). Non-coding RNAs’ partitioning in the evolution of photosynthetic organisms via energy transduction and redox signaling. RNA Biol. 12(1), 101104.CrossRefGoogle ScholarPubMed
Kotakis, C., Vrettos, N., Daskalaki, M.G., Kotzabasis, K. & Kalantidis, K. (2011). DCL3 and DCL4 are likely involved in the light intensity-RNA silencing cross talk in Nicotiana benthamiana . Plant Signal. Behav. 6(8), 11801182.Google Scholar
Lane, N., Martin, W.F., Raven, J.A. & Allen, J.F. (2013). Energy, genes and evolution: introduction to an evolutionary synthesis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368(1622), 20120253.Google Scholar
Lefebvre-Legendre, L., Merendino, L., Rivier, C. & Goldschmidt-Clermont, M. (2014). On the complexity of chloroplast RNA metabolism: psaA trans-splicing can be bypassed in Chlamydomonas . Mol. Biol. Evol. 31(10), 26972707.CrossRefGoogle ScholarPubMed
Lister, D.L., Bateman, J.M., Purton, S. & Howe, C.J. (2003). DNA transfer from chloroplast to nucleus is much rarer in Chlamydomonas than in tobacco. Gene 316, 3338.Google Scholar
Lloyd, A.H. & Timmis, J.N. (2011). The origin and characterization of new nuclear genes originating from a cytoplasmic organellar genome. Mol. Biol. Evol. 28(7), 20192028.Google Scholar
Mattick, J.S. & Clark, M.B. (2011). RNA lights up. Nat. Biotechnol. 29(10), 883884.Google Scholar
Moore, C.E., Curtis, B., Mills, T., Tanifuji, G. & Archibald, J.M. (2012). Nucleomorph genome sequence of the cryptophyte alga Chroomonas mesostigmatica CCMP1168 reveals lineage-specific gene loss and genome complexity. Genome Biol. Evol. 4(11), 11621175.Google Scholar
Morris, K.V. (2015). The theory of RNA-mediated gene evolution. Epigenetics 10(1), 15.CrossRefGoogle ScholarPubMed
Pal, C. (1998). Plasticity, memory and the adaptive landscape of the genotype. Proc. Roy. Soc. London. B. 265(1403), 13191323.Google Scholar
Petrillo, E., Godoy, , Herz, M.A., Fuchs, A., Reifer, D., Fuller, J., Yanovsky, M.J., Simpson, C., Brown, J.W., Barta, A., Kalyna, M. & Kornblihtt, A.R. (2014). A chloroplast retrograde signal regulates nuclear alternative splicing. Science 344(6182), 427430.Google Scholar
Schmitz-Linneweber, C., Lampe, M.K., Sultan, L.D. & Ostersetzer-Biran, O. (2015). Organellar maturases: a window into the evolution of the spliceosome. Biochim. Biophys. Acta. pii: S0005-2728(15)00020-1. doi: 10.1016/j.bbabio.2015.01.009 CrossRefGoogle ScholarPubMed
Scholz, I., Lange, S.J., Hein, S., Hess, W.R. & Backofen, R. (2013). CRISPR-Cas systems in the cyanobacterium Synechocystis sp. PCC6803 exhibit distinct processing pathways involving at least two Cas6 and a Cmr2 protein. PLoS ONE 8(2), e56470.CrossRefGoogle Scholar
Sheppard, A.E., Madesis, P., Lloyd, A.H., Day, A., Ayliffe, M.A. & Timmis, J.N. (2011). Introducing an RNA editing requirement into a plastid-localised transgene reduces but does not eliminate functional gene transfer to the nucleus. Plant Mol. Biol. 76(3–5), 299309.CrossRefGoogle Scholar
Shiina, N. & Nakayama, K. (2014). RNA granule assembly and disassembly modulated by nuclear factor associated with double-stranded RNA 2 and nuclear factor 45. J. Biol. Chem. 289(30), 2116321180.Google Scholar
Timmis, J.N. (2012). Endosymbiotic evolution: RNA intermediates in endosymbiotic gene transfer. Curr. Biol. 22(9), R296R298.Google Scholar
Wang, D., Lloyd, A.H. & Timmis, J.N. (2012). Environmental stress increases the entry of cytoplasmic organellar DNA into the nucleus in plants. Proc. Natl. Acad. Sci. USA 109(7), 24442448.Google Scholar
Wischmann, C. & Schuster, W. (1995). Transfer of rps10 from the mitochondrion to the nucleus in Arabidopsis thaliana: evidence for RNA-mediated transfer and exon shuffling at the integration site. FEBS Lett. 374(2), 152156.Google Scholar
Zhang, J., Khan, S.A., Hasse, C., Ruf, S., Heckel, D.G. & Bock, R. (2015). Pest control. Full crop protection from an insect pest by expression of long double-stranded RNAs in plastids. Science 347(6225), 991994.Google Scholar