4.5 Review

Inheritance through the cytoplasm

Journal

HEREDITY
Volume 129, Issue 1, Pages 31-43

Publisher

SPRINGERNATURE
DOI: 10.1038/s41437-022-00540-2

Keywords

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Funding

  1. UKRI Fellowship [NE/V014307/1]
  2. Leverhulme Trust [RPG-2019-109]
  3. National Science Foundation [DEB -1753695, DEB -1753851, IOS -1829176, IOS -2145811]
  4. UKRI grant [NE/S012346/1]
  5. New Mexico Institute of Mining and Technology
  6. NERC [NE/S012346/1, NE/V014307/1] Funding Source: UKRI

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In this article, the authors discuss the diversity and peculiarities of cytoplasmic inherited genomes, as well as the broad evolutionary consequences of non-Mendelian inheritance. The origins of vertical transmission and uniparental inheritance are explored, and the vast diversity of cytoplasmic inheritance systems in Eukaryota is described. The evolution of genomic organisation and its interactions with the nuclear genome and population genetics dynamics are also discussed. The authors highlight the importance of understanding hereditary symbiosis in order to understand the evolution of eukaryotes.
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.

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