Cytonuclear integration and co-evolution

Abstract

The partitioning of genetic material between the nucleus and cytoplasmic (mitochondrial and plastid) genomes within eukaryotic cells necessitates coordinated integration between these genomic compartments, with important evolutionary and biomedical implications. Classic questions persist about the pervasive reduction of cytoplasmic genomes via a combination of gene loss, transfer and functional replacement — and yet why they are almost always retained in some minimal form. One striking consequence of cytonuclear integration is the existence of ‘chimeric’ enzyme complexes composed of subunits encoded in two different genomes. Advances in structural biology and comparative genomics are yielding important insights into the evolution of such complexes, including correlated sequence changes and recruitment of novel subunits. Thus, chimeric cytonuclear complexes provide a powerful window into the mechanisms of molecular co-evolution.

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Fig. 1: Variation in mitochondrial gene content across eukaryotic lineages.
Fig. 2: Opposite trends in the cytonuclear movement of genes versus gene products.
Fig. 3: Acquisition of supernumerary subunits in chimeric cytonuclear enzyme complexes.

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Acknowledgements

The authors thank the reviewers for their insightful comments on an earlier version of this manuscript. This work was supported by a National Institutes of Health (NIH) postdoctoral Fellowship (F32 GM116361 to J.C.H.), a National Science Foundation (NSF) Graduate Research Fellowship (DGE-1321845 to A.M.W.), an NSF-funded GAUSSI Graduate Fellowship (DGE-1450032 to J.M.W.) and grants from NSF (MCB-1412260 and MCB-1733227 to D.B.S.), NIH (NIGMS R01 GM118046 to D.B.S.) and the U.S. Department of Agriculture (2015-67017-23143 to A.J.C.).

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Nature Reviews Genetics thanks D. M. Rand, T. A. Richards, D. R. Smith and the other, anonymous reviewer(s) for their contribution to the peer review of this work.

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All authors contributed to researching data for the article, discussion of content and reviewing and editing the manuscript for submission. D.B.S. was primarily responsible for writing the manuscript.

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Glossary

Plastids

Organelles that were endosymbiotically derived from cyanobacteria and can differentiate into multiple functional types, the most well known of which is the chloroplast.

Endosymbiotic gene transfer

(EGT). The process by which genes are functionally transferred from cytoplasmic genomes to the nucleus (also known as intracellular gene transfer).

Last eukaryotic common ancestor

(LECA). The most recent common ancestor of all extant eukaryotes — an organism that is thought to have already acquired mitochondria and undergone substantial cytonuclear integration.

TIM/TOM

The translocase of the inner mitochondrial membrane (TIM) and the translocase of the outer mitochondrial membrane (TOM) mediate import of nuclear-encoded proteins into the mitochondria.

TIC/TOC

The translocase of the inner chloroplast membrane (TIC) and the translocase of the outer chloroplast membrane (TOC) mediate import of nuclear-encoded proteins into the plastids.

Nuclear mitochondrial DNAs

(NUMTs). Insertions of mitochondrial DNA into the nucleus (usually non-functional).

Nuclear plastid DNAs

(NUPTs). Insertions of plastid DNA into the nucleus (usually non-functional).

Double-stranded breaks

Breaks in DNA molecules that, when subsequently repaired by processes such as non-homologous end-joining, can result in incorporation of other DNA sequences.

Retroprocessing

The process by which a mature RNA transcript is reverse transcribed and recombined back into the genome.

Oxidative phosphorylation

(OXPHOS). A biochemical process that occurs in the mitochondria and is mediated by a set of cytonuclear enzyme complexes, in which energy generated by electron transfer results in the synthesis of ATP.

Supernumerary subunits

Protein subunits within cytonuclear enzyme complexes that were not present in the bacterial progenitors of mitochondria or plastids and have been recruited to these complexes during eukaryotic evolution.

Paralogues

Genes that are related to each other as the result of an earlier gene duplication event within a genome.

Mother’s curse

The concept articulated by Frank and Hurst and later named by Gemmell et al. that cytoplasmic alleles that are harmful to male reproduction may persist in populations because strict maternal inheritance shields these effects from selection.

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Sloan, D.B., Warren, J.M., Williams, A.M. et al. Cytonuclear integration and co-evolution. Nat Rev Genet 19, 635–648 (2018). https://doi.org/10.1038/s41576-018-0035-9

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