Evolutionary inference across eukaryotes identifies universal features shaping organelle gene retention

Cellular and environmental dynamics influence species-specific extents of organelle gene retention

“…Plants (within Viridiplantae) are typically subject to diurnal light and temperature changes and, being sessile, cannot move away from other environmental changes, and they retain comparatively many oDNA genes. Sessile, intertidal eukaryotes (including multicellular red and brown algae) face both strong diurnal light fluctuations and semidiurnal tidal variation in oxygen, temperature, and salinity, and they retain the highest plastid DNA (ptDNA) counts (Giannakis et al, 2022). There will certainly be other factors influencing where a given gene is encoded, including the evolutionary history of a species and many other features.…”

“…The CoRR hypothesis proposes that genes are retained in oDNA to allow local, tight control of the energetic machinery (Allen, 2015), so that organelles can better adapt to imposed energetic demands. This idea is supported by the importance of retained oDNA genes in controlling redox processes (Martin et al, 2015; Allen, 2015; Giannakis et al, 2022).…”

“…These organelles were originally independent bacteria with their own genomes, and through processes of endosymbioses, they transferred most of their genes to the nuclear genome of the host cell or lost them completely (Martin et al, 2015; Sagan, 1967; Sloan et al, 2018; Adams and Palmer, 2003; Roger et al, 2017; Zaremba-Niedzwiedzka et al, 2017). However, they have retained a small subset of their genes in their own organelle DNA (oDNA), with oDNA in different species containing strikingly different gene counts (Adams and Palmer, 2003; Giannakis et al, 2022; Daley and Whelan, 2005; Johnston and Williams, 2016).…”

“…The first question, why a given gene is more or less likely to be retained in oDNA, has had several potential answers proposed over time (summarised in Giannakis et al (2022)). It has recently been shown that the combination of these can help explain gene-specific patterns of oDNA retention across organelles and eukaryotes (Giannakis et al, 2022). Of particular note here are the hydrophobicity hypothesis (von Heijne, 1986) and the co-localisation for redox regulation (CoRR) hypothesis (Allen and Raven, 1996; Allen, 2015).…”

“…The second question, why some species retain more organelle genes than others, remains more open. There exists substantial diversity in oDNA gene counts across eukaryotes (Roger et al, 2017; Giannakis et al, 2022). Some jakobid protists retain over 60 protein-coding mitochondrial DNA (mtDNA) genes, plants retain fewer and metazoa fewer still with a common 13-protein gene profile shared by a large majority of taxa (including humans).…”