Inheritance through the cytoplasm

Abstract

Most heritable information in eukaryotic cells is encoded in the nuclear genome, with inheritance patterns following classic Mendelian segregation. Genomes residing in the cytoplasm, however, prove to be a peculiar exception to this rule. Cytoplasmic genetic elements are generally maternally inherited, although there are several exceptions where these are paternally, biparentally or doubly-uniparentally inherited. In this review, we examine the diversity and peculiarities of cytoplasmically inherited genomes, and the broad evolutionary consequences that non-Mendelian inheritance brings. We first explore the origins of vertical transmission and uniparental inheritance, before detailing the vast diversity of cytoplasmic inheritance systems across Eukaryota. We then describe the evolution of genomic organisation across lineages, how this process has been shaped by interactions with the nuclear genome and population genetics dynamics. Finally, we discuss how both nuclear and cytoplasmic genomes have evolved to co-inhabit the same host cell via one of the longest symbiotic processes, and all the opportunities for intergenomic conflict that arise due to divergence in inheritance patterns. In sum, we cannot understand the evolution of eukaryotes without understanding hereditary symbiosis.

Fig. 1. Cytoplasmically inherited elements produce variation at multiple scales of biological organisation.

New mutations that arise immediately produce intra-organellar variation depicted here by differently coloured nucleoids (Mitochondria & Chloroplast panel). If mutations (differently coloured nucleoids) spread between organelles, variation between organelles is observed (Plant Cell panel). Note that mitochondria often form reticulated syncytia, rather than discrete compartments, in contrast to chloroplasts, which may facilitate recombination and therefore spread of mutations throughout the cell. Intracellular variation can give rise to intra-tissue variation, depicted here in the form of a variegated leaf (Psychotria leaf panel). Psychotria also features bacterial leaf nodules (dark green circles) that contain Burkholderia bacteria which are vertically inherited through the seed. Variation within tissues can then give rise to variation across tissues (Psychotria Plant panel). If germlines are segregated late, this can result in distinct alleles being propagated to the next generation from different parts of the plant. As a consequence, the variation that originated at the individual organelle level can finally be observed between individuals within populations (Psychotria population panel).

Fig. 2. Conflicts between cytoplasmically inherited elements and their hosts.

Differences in inheritance patterns between nuclear and cytoplasmic elements provides an arena for intergenomic conflict. A Mothers curse hypothesis: maternal inheritance of mitochondria can result in the accumulation of mutations with sexually antagonistic effects in the mtDNA genome. B Cytoplasmic sex ratio distortion in species with separate sexes. Commonly, investment into male and female offspring is equal. Maternal inheritance ties symbiont fitness to the production and survival of female hosts. This is manifested in parthenogenesis induction (left), where all progeny are daughters. Male-killing (middle), where the symbiont kills male progeny it enters, and sibling females have greater access to resources, and higher survival, as a result. Feminisation (right), where the symbiont impacts development in progeny that have a male karyotype such that they differentiate as female hosts. C Cytoplasmic incompatibility is the result of severe miscommunication between cytoplasmic and nuclear genomes, and a classic example of how cytoplasmic elements can spread through a population. When hosts carrying the symbiont (red) mate with uninfected hosts (grey), CI can result in inviable offspring in a unidrectional (left) or bidirectional (right) fashion.