Origins of Life and Evolution of Biospheres

, Volume 41, Issue 6, pp 587–607 | Cite as

“Hypothesis for the Modern RNA World”: A pervasive Non-coding RNA-Based Genetic Regulation is a Prerequisite for the Emergence of Multicellular Complexity

  • Irma Lozada-Chávez
  • Peter F. Stadler
  • Sonja J. Prohaska
Article
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Abstract

The transitions to multicellularity mark the most pivotal and distinctive events in life’s history on Earth. Although several transitions to “simple” multicellularity (SM) have been recorded in both bacterial and eukaryotic clades, transitions to complex multicellularity (CM) have only happened a few times in eukaryotes. A large number of cell types (associated with large body size), increased energy consumption per gene expressed, and an increment of non-protein-coding DNA positively correlate with CM. These three factors can indeed be understood as the causes and consequences of the regulation of gene expression. Here, we discuss how a vast expansion of non-protein-coding RNA (ncRNAs) regulators rather than large numbers of novel protein regulators can easily contribute to the emergence of CM. We also propose that the evolutionary advantage of RNA-based gene regulation derives from the robustness of the RNA structure that makes it easy to combine genetic drift with functional exploration. We describe a model which aims to explain how the evolutionary dynamic of ncRNAs becomes dominated by the accessibility of advantageous mutations to innovate regulation in complex multicellular organisms. The information and models discussed here outline the hypothesis that pervasive ncRNA-based regulatory systems, only capable of being expanded and explored in higher eukaryotes, are prerequisite to complex multicellularity. Thereby, regulatory RNA molecules in Eukarya have allowed intensification of morphological complexity by stabilizing critical phenotypes and controlling developmental precision. Although the origin of RNA on early Earth is still controversial, it is becoming clear that once RNA emerged into a protocellular system, its relevance within the evolution of biological systems has been greater than we previously thought.

Keywords

Modern RNA world Multicellular complexity Eukaryote evolution Genome complexity Non-coding RNA Gene regulation 
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Notes

Acknowledgements

IL-C is funded by the fellowship 185993 from the National Council of Science and Technology of Mexico. We thank Christian Arnold and an anonymous referee for valuable comments and suggestions. We dedicate this article to the memory of Lynn Margulis, whose work has allowed us to go forward on the understanding of the origin and evolution of complex life on Earth.

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Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Irma Lozada-Chávez
    • 1
    • 2
    • 3
  • Peter F. Stadler
    • 2
    • 3
    • 4
    • 5
    • 6
    • 7
    • 8
  • Sonja J. Prohaska
    • 1
    • 3
  1. 1.Computational EvoDevo GroupUniversity of LeipzigLeipzigGermany
  2. 2.Bioinformatics Group, Department of Computer ScienceUniversity of LeipzigLeipzigGermany
  3. 3.Interdisciplinary Center for BioinformaticsUniversity of LeipzigLeipzigGermany
  4. 4.Max Planck Institute for Mathematics in the SciencesLeipzigGermany
  5. 5.Fraunhofer Institut für Zelltherapie und Immunologie (IZI)LeipzigGermany
  6. 6.Department of Theoretical ChemistryUniversity of ViennaWienAustria
  7. 7.Center For Non-Coding RNA in Technology and HealthUniversity of CopenhagenFrederiksberg CDenmark
  8. 8.Santa Fe InstituteSanta FeUSA

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