RNA-Mediated Epigenetic Programming of Genome Rearrangements

Nowacki, Mariusz; Shetty, Keerthi S.; Landweber, Laura F.

doi:10.1146/annurev-genom-082410-101420

Cited by 70 publications

(82 citation statements)

References 135 publications

(178 reference statements)

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“…We think the answer is yes. The ciliates can be considered as a maxiploidy system that uses the many gene copies of its macronucleus in a form of auto-recombination to combat accumulation of mutations and generate diversity (83,84). However, one might wonder whether the amicronucleate population will in the end be as long lived as the one that still uses sexuality on encountering environmental stress.…”

Section: On the Advantages Of Meiotic Sexmentioning

confidence: 99%

Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life

Speijer

Lukeš

Eliáš

2015

Proc. Natl. Acad. Sci. U.S.A.

257

267

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Sexual reproduction and clonality in eukaryotes are mostly seen as exclusive, the latter being rather exceptional. This view might be biased by focusing almost exclusively on metazoans. We analyze and discuss reproduction in the context of extant eukaryotic diversity, paying special attention to protists. We present results of phylogenetically extended searches for homologs of two proteins functioning in cell and nuclear fusion, respectively (HAP2 and GEX1), providing indirect evidence for these processes in several eukaryotic lineages where sex has not been observed yet. We argue that (i) the debate on the relative significance of sex and clonality in eukaryotes is confounded by not appropriately distinguishing multicellular and unicellular organisms; (ii) eukaryotic sex is extremely widespread and already present in the last eukaryotic common ancestor; and (iii) the general mode of existence of eukaryotes is best described by clonally propagating cell lines with episodic sex triggered by external or internal clues. However, important questions concern the relative longevity of true clonal species (i.e., species not able to return to sexual procreation anymore). Long-lived clonal species seem strikingly rare. We analyze their properties in the light of meiotic sex development from existing prokaryotic repair mechanisms. Based on these considerations, we speculate that eukaryotic sex likely developed as a cellular survival strategy, possibly in the context of internal reactive oxygen species stress generated by a (proto) mitochondrion. Thus, in the context of the symbiogenic model of eukaryotic origin, sex might directly result from the very evolutionary mode by which eukaryotic cells arose.reactive oxygen species | evolution | protists | eukaryotes | sex

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Section: On the Advantages Of Meiotic Sexmentioning

confidence: 99%

Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life

Speijer

Lukeš

Eliáš

2015

Proc. Natl. Acad. Sci. U.S.A.

257

267

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“…Afterwards, the old macronuclei degenerate, and a new macronucleus develops from a descendant of the post-mating zygote nucleus. Forming a new macronucleus is guided by RNA molecules from the old macronucleus [97]. The process is complex and involves elimination of much germ-line-specific DNA (up to 90%, depending on the species), as well as reassembly of scrambled germ-line sequences into accurate coding sequences [95,98].…”

Section: Over Multiple Cell Cycles In Vegetative Populations By Strucmentioning

confidence: 99%

How life changes itself: The Read–Write (RW) genome

Shapiro

2013

Physics of Life Reviews

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The genome has traditionally been treated as a Read-Only Memory (ROM) subject to change by copying errors and accidents. In this review, I propose that we need to change that perspective and understand the genome as an intricately formatted Read-Write (RW) data storage system constantly subject to cellular modifications and inscriptions. Cells operate under changing conditions and are continually modifying themselves by genome inscriptions. These inscriptions occur over three distinct time-scales (cell reproduction, multicellular development and evolutionary change) and involve a variety of different processes at each time scale (forming nucleoprotein complexes, epigenetic formatting and changes in DNA sequence structure). Research dating back to the 1930s has shown that genetic change is the result of cell-mediated processes, not simply accidents or damage to the DNA. This cell-active view of genome change applies to all scales of DNA sequence variation, from point mutations to large-scale genome rearrangements and whole genome duplications (WGDs). This conceptual change to active cell inscriptions controlling RW genome functions has profound implications for all areas of the life sciences.

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“…The idea that an organism produces an RNA-encoded, heritable list of all helpful genetic information ("RNA Cache") was validated both in unicellular Oxytricha trifallax, and in animals [64].…”

Section: Guest List: Rna Licensingmentioning

confidence: 99%

“…Oxytricha ciliates have two genomes packed inside two nuclei, a somatic one that encodes for all the vegetative growth functions, and a germline one that is responsible for sexual reproduction [64]. During the development of the somatic nucleus, Oxytricha gets rid of all parasitic DNA elements, which compose the majority of the germline DNA (>95%).…”

Section: Guest List: Rna Licensingmentioning

confidence: 99%

Guest list or black list: heritable small RNAs as immunogenic memories

Rechavi

2014

Trends in Cell Biology

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Small RNA-mediated gene silencing plays a pivotal role in genome immunity by recognizing and eliminating viruses and transposons which otherwise may colonize the genome. However, this can be challenging since individual genomic parasites are highly diverse, and employ multiple immune evasion techniques. In this review, I discuss a new theory proposing that the integrity of the germline is maintained by transgenerationally-transmitted RNA "memories" that record ancestral gene expression patterns, and delineate "Self" from "Foreign" sequences. To maintain such recollection two tactics are employed in parallel: "black listing" of invading nucleic acids, and "guest listing" of endogenous genes. Studies in a number of organisms have shown that this memorization is used by the next generation small RNAs to act as "Inherited Vaccines" that ambush invading elements, or as "Inherited Licenses" that grant the transcription of autogenous sequences. KeywordsSmall RNA; Transgenerational Inheritance; Inherited Immunity; Self Vs. Non-Self; "Inherited Vaccines" Overview of transgenerational inheritanceEvolution progresses through an interplay between two major forces, selection and variation. Since the formulation of the Modern Synthesis the theory holds that the environment is limited in its contribution to the evolutionary course of action -it affects selection, but not the degree of variation [1,2]. However, recent discoveries in epigenetics suggest that the environment may influence variability as well [1]. If the parental environment is predictive of the conditions that the progeny will face (often for sessile or short-lived organisms), epigenetic responses can change the output of the encoded genetic information in an adaptive manner [3]. For example, the water flea Daphnia changes its normal developmental course and develops a "helmet" that protects it from predators, if it is born to a mother that survived a similar attack [4].Correspondence to: odedrechavi@gmail.com. Over the years, controversy surrounded the study of environmentally affected transgenerational inheritance. Today, an improved understanding of epigenetic mechanisms at the molecular level has provided a logical background to explain how, heretically, an adaptive acquired trait could become heritable [5]. Several epigenetic mechanisms could regulate the expression of relevant genes during transgenerational inheritance including DNA methylation, histone modification, and transmission of regulatory RNAs. Moreover, in many organisms, these pathways appear to be interconnected [5][6][7][8]. Europe PMC Funders GroupThis review will concentrate on recent discoveries that establish a role for small RNAs in transgenerational transmission of acquired defense. Furthermore, exciting examples of RNA-mediated non-Mendelian genetic effects will be discussed, along with their possible implications for the study of evolution and immunology. RNA-mediated gene silencing and inheritanceSince the original discovery that small RNAs derived from exogenously-provided dou...

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RNA-Mediated Epigenetic Programming of Genome Rearrangements

Cited by 70 publications

References 135 publications

Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life

Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life

How life changes itself: The Read–Write (RW) genome

Guest list or black list: heritable small RNAs as immunogenic memories

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