Why are most organelle genomes transmitted maternally?

Abstract

Why the DNA-containing organelles, chloroplasts, and mitochondria, are inherited maternally is a long standing and unsolved question. However, recent years have seen a paradigm shift, in that the absoluteness of uniparental inheritance is increasingly questioned. Here, we review the field and propose a unifying model for organelle inheritance. We argue that the predominance of the maternal mode is a result of higher mutational load in the paternal gamete. Uniparental inheritance evolved from relaxed organelle inheritance patterns because it avoids the spread of selfish cytoplasmic elements. However, on evolutionary timescales, uniparentally inherited organelles are susceptible to mutational meltdown (Muller's ratchet). To prevent this, fall-back to relaxed inheritance patterns occurs, allowing low levels of sexual organelle recombination. Since sexual organelle recombination is insufficient to mitigate the effects of selfish cytoplasmic elements, various mechanisms for uniparental inheritance then evolve again independently. Organelle inheritance must therefore be seen as an evolutionary unstable trait, with a strong general bias to the uniparental, maternal, mode.

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).…”

“…Building on the aforementioned ideas, a unifying model for organellar inheritance has recently been proposed by Greiner 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).…”

“…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).…”

“…The predominance of maternal (vs. paternal) inheritance of mitochondria in sexually reproducing eukaryotes could be explained by a higher mutational load in the paternal gamete due to higher oxidative damage, thus favouring the evolution of paternal gamete-controlled organelle exclusion mechanisms (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).…”