Genome-defence small RNAs exapted for epigenetic mating-type inheritance

Abstract

In the ciliate Paramecium, transposable elements and their single-copy remnants are deleted during the development of somatic macronuclei from germline micronuclei, at each sexual generation. Deletions are targeted by scnRNAs, small RNAs produced from the germ line during meiosis that first scan the maternal macronuclear genome to identify missing sequences, and then allow the zygotic macronucleus to reproduce the same deletions. Here we show that this process accounts for the maternal inheritance of mating types in Paramecium tetraurelia, a long-standing problem in epigenetics. Mating type E depends on expression of the transmembrane protein mtA, and the default type O is determined during development by scnRNA-dependent excision of the mtA promoter. In the sibling species Paramecium septaurelia, mating type O is determined by coding-sequence deletions in a different gene, mtB, which is specifically required for mtA expression. These independently evolved mechanisms suggest frequent exaptation of the scnRNA pathway to regulate cellular genes and mediate transgenerational epigenetic inheritance of essential phenotypic polymorphisms.

Insights into Three Whole-Genome Duplications Gleaned from theParamecium caudatumGenome Sequence

“…Later work provided fundamental insights into major issues in biology, including mutagenesis (Igarashi 1966), molecular and developmental genetics (Sonneborn 1947), symbiosis (Beale et al 1969), mitochondrial genetics (Adoutte and Beisson 1972), aging (Siegel 1967), nuclear differentiation (Berger 1937), and gene regulation (Allen and Gibson 1972). More recently, Paramecium has been used to study maternal inheritance (Nowacki et al 2005), programmed genome rearrangements and transposon domestication (Arnaiz et al 2012), epigenetic inheritance (Singh et al 2014), and whole-genome duplication (Aury et al 2006;Lynn McGrath, Jean-Francois Gout, Parul Johri, Thomas Graeme Doak, and Michael Lynch, unpublished results). Although not as well-studied as the P. aurelia complex of species, P. caudatum also has a long history of research (Calkins 1902;Sonneborn 1933).…”

Environmental challenges may impact on somatic repair

“…Exaptation (the shift in the function of a trait during evolution, when a trait is co-opted for a different function than the original) may underlie some mechanisms which are involved in homoeostasis but it may also operate within the scenario presented in this book, which is the re-allocation of resources from germ line to soma. Those mechanisms originally developed in order to facilitate resource flow from soma to germ line (such as gene recombination and gamete selection), may (under certain circumstances, such as those discussed above) be exapted and operate in the opposite way: shift the balance of repair from germ line to soma [42]. This may not be a very long process, as it operates through epigenetic mechanisms some of which involve fast microRNA regulation [43].…”

Epigenetic factors in vital functions of the ciliate Dileptus anser

“…Specific molecular mechanisms of cell determination and differentiation for MT in ciliates were revealed later (see, e.g. : Cervantes et al, 2013;Singh et al, 2014;Vallesi et al, 2014). It was of undoubted importance for us to study the case of D. anser in this respect.…”