DNA abandonment and the mechanisms of uniparental inheritance of mitochondria and chloroplasts

Abstract

For most eukaryotic organisms, the nuclear genomes of both parents are transmitted to the progeny following biparental inheritance. For mitochondria and chloroplasts, however, uniparental inheritance (UPI) is frequently observed. The maternal mode of inheritance for mitochondria in animals can be nearly absolute, suggesting an adaptive advantage for UPI. In other organisms, however, the mode of inheritance for mitochondria and chloroplasts can vary greatly even among strains of a species. Here, I review the data on the transmission of organellar DNA (orgDNA) from parent to progeny and the structure, copy number, and stability of orgDNA molecules. I propose that UPI is an incidental by-product of DNA abandonment, a process that lowers the metabolic cost of orgDNA repair.

Atypical mitochondrial inheritance patterns in eukaryotes

“…The bottleneck mechanisms have been most thoroughly studied in mammals and include the following: (i) a physical bottleneck during oogenesis that greatly reduces mitochondrial genome copy number and exposes deleterious mutations to purifying selection before the re-initialization of mtDNA replication during oocyte maturation; (ii) a genetic bottleneck during oogenesis that occurs as a result of selective replication of a subset of mtDNA molecules; and (iii) another genetic bottleneck during early embryogenesis that occurs as a result of reduction in mtDNA copies per cell owing to dilution as cells rapidly divide, followed by amplification of a subpopulation of mtDNA molecules (see Jokinen and Battersby (2013) and Mishra and Chan (2014) for reviews). The current state of knowledge of the molecular mechanisms underlying the elimination of paternal mtDNA or mitochondrial structures for ensuring the maternal transmission of mtDNA has also been addressed in recent reviews (Bendich 2013;Sato and Sato 2013;Song et al 2014;Greiner et al 2015). For example, studies in mammals suggest that elimination of paternal mtDNA is dependent on a mechanism involving the ubiquitin-proteasome system (Sutovsky et al 1999).…”

“…Furthermore, in most cases where there is no maternal inheritance, mitochondria are nonetheless inherited uniparentally, suggesting that a general explanation might exist for the repeated evolution of diverse mechanisms to achieve uniparental inheritance (UPI) of mitochondria. It has been proposed that UPI has been selected as a mechanism to avoid the spread of selfish cytoplasmic elements and limit mitonuclear conflicts (Ballard and Whitlock 2004;Hoekstra 2011;Lane 2011;Bendich 2013;Sato and Sato 2013;Song et al 2014;Greiner et al 2015). Another recent and perhaps not mutually exclusive explanation for the evolution of UPI and other mechanisms ensuring mitochondrial homoplasmy is simply selection against heteroplasmy (Christie et al 2015).…”

“…Key components of this model are as follows: (i) UPI of mitochondria arises to avoid the spread of selfish organellar genomes (maladaptive and (or) incompatible with the host nucleus); (ii) UPI is unstable because mitochondria are susceptible to Muller's ratchet (UPI and low recombination rates cause the accumulation of deleterious mutations in the mtDNA -but see Bendich (2013)); (iii) Muller's ratchet drives a relaxation of UPI via occasional paternal (or maternal) leakage or regular biparental transmission; and (iv) the evolution of selfish mtDNAs is again possible during biparental inheritance episodes and therefore, UPI is restored (and repeatedly lost) over evolutionary timeframes (Greiner et al 2015). According to these authors, if UPI is evolutionarily unstable, three major patterns in mitochondrial inheritance should be observable -the repeated and independent evolution of biparental transmission, frequent paternal leakage (in the predominant SMI situation), and a switch to UPI by various mechanisms even between closely related species -and this is indeed what is reported in the literature (Greiner et al 2015).…”

“…However, despite the growing number of studies describing the diverse molecular mechanisms underlying the maternal inheritance of mitochondria, the potential causes of the near-universal stability of the SMI system are still far from being fully understood (Bendich 2013;Sato and Sato 2013;Song et al 2014;Greiner et al 2015). Furthermore, exceptions to SMI have been reported in diverse eukaryotic taxa, leading to the prediction that several distinct molecular mechanisms controlling mtDNA transmission are present among the eukaryotes.…”

The “fast” and the “slow” modes of mitochondrial DNA degradation

“…Moreover, mitochondria possess a unique mechanism for the degradation of damaged mtDNA molecules, which co-exists with DNA repair and may be activated by excessive mtDNA damage (Furda et al, 2012; Shokolenko et al, 2009, 2013b). This pathway, together with the high-redundancy of organellar genomes may enable effective management of even relatively high levels of mtDNA damage in both mitochondria and chloroplasts (Bendich, 2013). …”