Title: Beyond the Powerhouse: Integrating Mitonuclear Evolution, Physiology, and Theory in Comparative Biology
Abstract
Eukaryotes are the outcome of an ancient symbiosis and as such, eukaryotic cells fundamentally possess two genomes. As a consequence, gene products encoded by both nuclear and mitochondrial genomes must interact in an intimate and precise fashion to enable aerobic respiration in eukaryotes. This genomic architecture of eukaryotes is proposed to necessitate perpetual coevolution between the nuclear and mitochondrial genomes to maintain coadaptation, but the presence of two genomes also creates the opportunity for intracellular conflict. In the collection of papers that constitute this symposium volume, scientists working in diverse organismal systems spanning vast biological scales address emerging topics in integrative, comparative biology in light of mitonuclear interactions.
Onyshchenko, Anastasiia; Ruck, Elizabeth C.; Nakov, Teofil; Alverson, Andrew J.(
, American Journal of Botany)
Premise of the Study
Loss of photosynthesis is a common and often repeated trajectory in nearly all major groups of photosynthetic eukaryotes. One small subset of “apochloritic” diatoms in the genusNitzschiahave lost their ability to photosynthesize and require extracellular carbon for growth. Similar to other secondarily nonphotosynthetic taxa, apochloritic diatoms maintain colorless plastids with highly reduced plastid genomes. Although the narrow taxonomic breadth of apochloriticNitzschiasuggests a single loss of photosynthesis in their common ancestor, previous phylogenetic analyses suggested that photosynthesis was lost multiple times.
Methods
We analyzed genes from the nuclear, plastid, and mitochondrial genomes for a broad set of taxa to test whether photosynthesis was lost one or multiple times in Bacillariales. We also sequenced and characterized the plastid genome of a nonphotosyntheticNitzschiaspecies.
Key Results
Phylogenetic analyses showed that genes from all three genetic compartments either supported or failed to reject monophyly of apochloriticNitzschiaspecies, consistent with a single loss of photosynthesis in this group. The plastid genomes of two apochloriticNitzschiaare highly similar in all respects, indicating streamlining of the plastid genome before the split of these two species.
Conclusions
A better understanding of the phylogeny and ecology of apochloriticNitzschia, together with emerging genomic resources, will help identify the factors that have driven and maintained the loss of photosynthesis in this group of diatoms. Finally, some habitats host diverse communities of co‐occurring nonphotosynthetic diatoms, reflecting resource abundance or resource partitioning in ecologically favorable habitats.
Healy, Timothy M.; Burton, Ronald S.(
, Proceedings of the National Academy of Sciences)
Oxidative phosphorylation, the primary source of cellular energy in eukaryotes, requires gene products encoded in both the nuclear and mitochondrial genomes. As a result, functional integration between the genomes is essential for efficient adenosine triphosphate (ATP) generation. Although within populations this integration is presumably maintained by coevolution, the importance of mitonuclear coevolution in key biological processes such as speciation and mitochondrial disease has been questioned. In this study, we crossed populations of the intertidal copepodTigriopus californicusto disrupt putatively coevolved mitonuclear genotypes in reciprocal F2hybrids. We utilized interindividual variation in developmental rate among these hybrids as a proxy for fitness to assess the strength of selection imposed on the nuclear genome by alternate mitochondrial genotypes. Developmental rate varied among hybrid individuals, and in vitro ATP synthesis rates of mitochondria isolated from high-fitness hybrids were approximately two-fold greater than those of mitochondria isolated from low-fitness individuals. We then used Pool-seq to compare nuclear allele frequencies for high- or low-fitness hybrids. Significant biases for maternal alleles were detected on 5 (of 12) chromosomes in high-fitness individuals of both reciprocal crosses, whereas maternal biases were largely absent in low-fitness individuals. Therefore, the most fit hybrids were those with nuclear alleles that matched their mitochondrial genotype on these chromosomes, suggesting that mitonuclear effects underlie individual-level variation in developmental rate and that intergenomic compatibility is critical for high fitness. We conclude that mitonuclear interactions can have profound impacts on both physiological performance and the evolutionary trajectory of the nuclear genome.
The mitochondria contain their own genome derived from an alphaproteobacterial endosymbiont. From thousands of protein-coding genes originally encoded by their ancestor, only between 1 and about 70 are encoded on extant mitochondrial genomes (mitogenomes). Thanks to a dramatically increasing number of sequenced and annotated mitogenomes a coherent picture of why some genes were lost, or relocated to the nucleus, is emerging. In this review, we describe the characteristics of mitochondria-to-nucleus gene transfer and the resulting varied content of mitogenomes across eukaryotes. We introduce a ‘burst-upon-drift’ model to best explain nuclear-mitochondrial population genetics with flares of transfer due to genetic drift.
Warren, Jessica M; Salinas-Giegé, Thalia; Triant, Deborah A; Taylor, Douglas R; Drouard, Laurence; Sloan, Daniel B(
, Molecular Biology and Evolution)
Purugganan, Michael
(Ed.)
Abstract In most eukaryotes, transfer RNAs (tRNAs) are one of the very few classes of genes remaining in the mitochondrial genome, but some mitochondria have lost these vestiges of their prokaryotic ancestry. Sequencing of mitogenomes from the flowering plant genus Silene previously revealed a large range in tRNA gene content, suggesting rapid and ongoing gene loss/replacement. Here, we use this system to test longstanding hypotheses about how mitochondrial tRNA genes are replaced by importing nuclear-encoded tRNAs. We traced the evolutionary history of these gene loss events by sequencing mitochondrial genomes from key outgroups (Agrostemma githago and Silene [=Lychnis] chalcedonica). We then performed the first global sequencing of purified plant mitochondrial tRNA populations to characterize the expression of mitochondrial-encoded tRNAs and the identity of imported nuclear-encoded tRNAs. We also confirmed the utility of high-throughput sequencing methods for the detection of tRNA import by sequencing mitochondrial tRNA populations in a species (Solanum tuberosum) with known tRNA trafficking patterns. Mitochondrial tRNA sequencing in Silene revealed substantial shifts in the abundance of some nuclear-encoded tRNAs in conjunction with their recent history of mt-tRNA gene loss and surprising cases where tRNAs with anticodons still encoded in the mitochondrial genome also appeared to be imported. These data suggest that nuclear-encoded counterparts are likely replacing mitochondrial tRNAs even in systems with recent mitochondrial tRNA gene loss, and the redundant import of a nuclear-encoded tRNA may provide a mechanism for functional replacement between translation systems separated by billions of years of evolutionary divergence.
Hill, Geoffrey E.; Havird, Justin C.; Sloan, Daniel B.; Burton, Ronald S.; Greening, Chris; Dowling, Damian K.(
, Biological Reviews)
ABSTRACT
Metazoans exist only with a continuous and rich supply of chemical energy from oxidative phosphorylation in mitochondria. The oxidative phosphorylation machinery that mediates energy conservation is encoded by both mitochondrial and nuclear genes, and hence the products of these two genomes must interact closely to achieve coordinated function of core respiratory processes. It follows that selection for efficient respiration will lead to selection for compatible combinations of mitochondrial and nuclear genotypes, and this should facilitate coadaptation between mitochondrial and nuclear genomes (mitonuclear coadaptation). Herein, we outline the modes by which mitochondrial and nuclear genomes may coevolve within natural populations, and we discuss the implications of mitonuclear coadaptation for diverse fields of study in the biological sciences. We identify five themes in the study of mitonuclear interactions that provide a roadmap for both ecological and biomedical studies seeking to measure the contribution of intergenomic coadaptation to the evolution of natural populations. We also explore the wider implications of the fitness consequences of mitonuclear interactions, focusing on central debates within the fields of ecology and biomedicine.
Havird, Justin C., Weaver, Ryan J., Milani, Liliana, Ghiselli, Fabrizio, Greenway, Ryan, Ramsey, Adam J., Jimenez, Ana G., Dowling, Damian K., Hood, Wendy R., Montooth, Kristi L., Estes, Suzanne, Schulte, Patricia M., Sokolova, Inna M., and Hill, Geoffrey E. Beyond the Powerhouse: Integrating Mitonuclear Evolution, Physiology, and Theory in Comparative Biology. Integrative and Comparative Biology 59.4 Web. doi:10.1093/icb/icz132.
Havird, Justin C., Weaver, Ryan J., Milani, Liliana, Ghiselli, Fabrizio, Greenway, Ryan, Ramsey, Adam J., Jimenez, Ana G., Dowling, Damian K., Hood, Wendy R., Montooth, Kristi L., Estes, Suzanne, Schulte, Patricia M., Sokolova, Inna M., & Hill, Geoffrey E. Beyond the Powerhouse: Integrating Mitonuclear Evolution, Physiology, and Theory in Comparative Biology. Integrative and Comparative Biology, 59 (4). https://doi.org/10.1093/icb/icz132
Havird, Justin C., Weaver, Ryan J., Milani, Liliana, Ghiselli, Fabrizio, Greenway, Ryan, Ramsey, Adam J., Jimenez, Ana G., Dowling, Damian K., Hood, Wendy R., Montooth, Kristi L., Estes, Suzanne, Schulte, Patricia M., Sokolova, Inna M., and Hill, Geoffrey E.
"Beyond the Powerhouse: Integrating Mitonuclear Evolution, Physiology, and Theory in Comparative Biology". Integrative and Comparative Biology 59 (4). Country unknown/Code not available: Oxford University Press. https://doi.org/10.1093/icb/icz132.https://par.nsf.gov/biblio/10116648.
@article{osti_10116648,
place = {Country unknown/Code not available},
title = {Beyond the Powerhouse: Integrating Mitonuclear Evolution, Physiology, and Theory in Comparative Biology},
url = {https://par.nsf.gov/biblio/10116648},
DOI = {10.1093/icb/icz132},
abstractNote = {Abstract Eukaryotes are the outcome of an ancient symbiosis and as such, eukaryotic cells fundamentally possess two genomes. As a consequence, gene products encoded by both nuclear and mitochondrial genomes must interact in an intimate and precise fashion to enable aerobic respiration in eukaryotes. This genomic architecture of eukaryotes is proposed to necessitate perpetual coevolution between the nuclear and mitochondrial genomes to maintain coadaptation, but the presence of two genomes also creates the opportunity for intracellular conflict. In the collection of papers that constitute this symposium volume, scientists working in diverse organismal systems spanning vast biological scales address emerging topics in integrative, comparative biology in light of mitonuclear interactions.},
journal = {Integrative and Comparative Biology},
volume = {59},
number = {4},
publisher = {Oxford University Press},
author = {Havird, Justin C. and Weaver, Ryan J. and Milani, Liliana and Ghiselli, Fabrizio and Greenway, Ryan and Ramsey, Adam J. and Jimenez, Ana G. and Dowling, Damian K. and Hood, Wendy R. and Montooth, Kristi L. and Estes, Suzanne and Schulte, Patricia M. and Sokolova, Inna M. and Hill, Geoffrey E.},
}
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