Ballard, JWO

Camus, MF

DeSalle, R

Garvin, MR

Gospodaryov, DV

Richter, U

English

UCL Discovery

Editorial: Energy-producingorganelles and the nucleus: aphenomenal genomic friendshipDmytro V. Gospodaryov1*, J. William O. Ballard2,3*,M. Florencia Camus4*, Rob DeSalle5,6*, Michael R. Garvin7* andUwe Richter8,9*1Department of Biochemistry and Biotechnology, Vasyl Stefanyk Precarpathian National University, Ivano-Frankivsk, Ukraine, 2School of Biosciences, University of Melbourne, Parkville, VIC, Australia, 3Departmentof Environment and Genetics, School of Agriculture, Biomedicine and Environment, La Trobe University,Melbourne, VIC, Australia, 4Department of Genetics, Evolution and Environment, University CollegeLondon, London, United Kingdom, 5Institute for Comparative Genomics, American Museum of NaturalHistory, New York, NY, United States, 6Division of Invertebrate Zoology, American Museum of NaturalHistory, New York, NY, United States, 7Computational Predictive Biology, Oak Ridge National Laboratory,Oak Ridge, TN, United States, 8Wellcome Centre for Mitochondrial Research, Faculty of Medical Sciences,Newcastle University, Newcastle Upon Tyne, United Kingdom, 9Organismal and Evolutionary BiologyResearch Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki,FinlandKEYWORDSmitochondria, chloroplast, endosymbioses, mitonuclear coevolution, mitonuclearcoadaptation, Drosophila melanogaster, Caenorhabditis elegans, mitochondrial genomeEditorial on the Research TopicEnergy-producing organelles and the nucleus: a phenomenal genomicfriendshipMitochondria and chloroplasts are energy-producing organelles that are considered to bedescendants of bacteria that were either phagocytosed by or had invaded proto-eukaryotic cells.Mitochondria are essential for obligatory aerobic respiration in animal and plant cells, whereasplants are incapable of synthesizing organic compounds without chloroplasts. Notably,mitochondria and chloroplasts retained some of the gene expression machinery of theirbacterial ancestors and this machinery included a part of the original genome, bacterial-likeribosomes, as well as parts of the replication, transcription, and translation factors, similar tothose that operate in contemporary bacteria. However, mitochondrial transcription andreplication machineries are largely of bacteriophage origin and were acquired from anancestor of a T3/T7-like bacteriophage that was likely present in the ancestral α-proteobacterium at the time of the mitochondrial endosymbiosis (Filée and Forterre, 2005;Shutt and Gray, 2006). Plant mitochondrial genomes are more complex, having more genes,than either fungal and streamlined animal mitochondrial DNA genomes. The endosymbiosesbetween a eukaryotic ancestor and ancestors of mitochondria and chloroplasts are mutuallybeneficial. Nevertheless, each participant lost independence in order to acquire other benefitsthat allowed them to propagate and occupy new niches. The eukaryotic ancestor contributedsubstantial and beneficial metabolic pathways to the symbiont. However, it became vulnerableto damages done to the symbiont. In turn, the symbionts allowed the host cell to encodeessential parts of their proteome. Essentially, the symbionts forced the host to include them intothe host’s evolutionary trajectories. For example, complexes I, III, IV, and V of themitochondrial oxidative phosphorylation (OXPHOS) system are composed of subunitsOPEN ACCESSEDITED AND REVIEWED BYSamuel A. Cushman,Forest Service, United States Departmentof Agriculture (USDA), United States*CORRESPONDENCEDmytro V. Gospodaryov,dmytro.gospodaryov@pnu.edu.uaJ. William O. Ballard,Bill.Ballard@unimelb.edu.auM. Florencia Camus,f.camus@ucl.ac.ukRob DeSalle,desalle@amnh.orgMichael R. Garvin,garvinmr@ornl.govUwe Richter,uwe.richter@ncl.ac.ukRECEIVED 27 May 2023ACCEPTED 15 June 2023PUBLISHED 23 June 2023CITATIONGospodaryov DV, Ballard JWO,Camus MF, DeSalle R, Garvin MR andRichter U (2023), Editorial: Energy-producing organelles and the nucleus: aphenomenal genomic friendship.Front. Genet. 14:1230032.doi: 10.3389/fgene.2023.1230032COPYRIGHT© 2023 Gospodaryov, Ballard, Camus,DeSalle, Garvin and Richter. This is anopen-access article distributed under theterms of the Creative CommonsAttribution License (CC BY). The use,distribution or reproduction in otherforums is permitted, provided the originalauthor(s) and the copyright owner(s) arecredited and that the original publicationin this journal is cited, in accordance withaccepted academic practice. No use,distribution or reproduction is permittedwhich does not comply with these terms.Frontiers in Genetics frontiersin.org01TYPE EditorialPUBLISHED 23 June 2023DOI 10.3389/fgene.2023.1230032encoded by both nuclear and mitochondrial genomes. The assemblyof the complexes occurs with the assistance of nuclear-encodedfactors. Mutations that affect coordination between the nuclear-encoded and mitochondria-encoded subunits of the complexescould profoundly change OXPHOS effectiveness (Couvillion et al.,2016). Nuclear-encoded proteins are essential for the transcription ofmitochondrial DNA and translation of mitochondrial messengerRNA. Therefore, a discordance in operation of the genomesdecreases fitness of the whole organism.Mitochondria generate a number of signaling molecules such asreactive oxygen species (ROS), acetyl coenzyme A, dicarboxylic acids(α-ketoglutarate, succinate, and fumarate), and regulate turnover ofothers such as calcium, adenylates, and guanylates. This means thatmitochondria are involved in a complex organismal response to thechanges in its environment. The changes are sensed by cellularsignaling machinery and the signal is transduced to the nuclear-encoded transcription factors that, in turn, shape the mitochondrialproteome. This algorithm is confirmed by Rodríguez et al., whoshowed that larvae of the fruit fly, Drosophila melanogaster, strainswith specific mitochondrial haplotypes respond differently to dietwith N-acetyl cysteine.Numerous theories postulate a key role for energy-producingorganelles, particularly mitochondria, in the origin of multicellularityand sexual recombination (Garg and Martin, 2016; Radzvilaviciuset al., 2016). Indeed, mitochondria provided ATP for a multitudeof functions that are not present in prokaryotes, such as complexintercellular communication, neural impulses, exchange ofmetabolites or division of labor. In the majority of organisms,the egg has an abundance of mitochondria whereas a sperm hasvery few. Interestingly, intracellular mitochondria-like insectparasites such as Wolbachia maximize their survival, affectingmales’ fertility and changing the ratio between females andmales in the host’s population (Werren et al., 2008). It allowsparasites to survive in the germline of females. The oppositesituation was shown in the case of mismatch between nuclearand mitochondrial genomes that are believed to coevolve. Naturalpopulations of the nematode Caenorhabditis elegans contain a verysmall proportion of males. However, mutations in mitochondrialgenes that encode subunits of the respiratory chain strongly affectsex determination in C. elegans (Bever et al.).It is remarkable that nuclear genes are inherited from both parentsand undergo recombination further, whereas mitochondrial genes havepredominantly maternal inheritance (Torres-Gonzalez and Makova).Surprisingly, such peculiarities in inheritance of nuclear andmitochondrial genomes enable a situation where an individualobtains a mitochondrially-encoded proteome that is not wellcoordinated with its nuclear-encoded proteome (Torres-Gonzalezand Makova). Basically, it may result in the above-describedsituations when mitochondrial genes influence a response toenvironmental changes or affect the natural ratio between sexes.A frequent cause of the above-mentioned mitonuclearmismatches is that a subset of the subunits of the mitochondrialOXPHOS system complexes are encoded by nuclear DNA whereasothers are encoded by mitochondrial DNA. We expect formation ofthe perfect match and coordination between nuclear- andmitochondrial-encoded subunits due to long-term coevolution.Nuclear-encoded replication machinery genes, namely, DNApolymerase γ, helicase, single strand binding proteins (SSB), andother factors should also coevolve with mitochondrial-encodedproteins. Ciesielski et al. show that DNA polymerase γ can directlyinteract with mitochondrial SSB that, in turn, decreases binding ofDNA polymerase γ to single-stranded DNA without primers attached.The same research teamdiscovered that the iron-sulfur (Fe-S) cluster inthe N-terminal domain of the fruit fly’s mitochondrial DNA helicase isbound to the membrane. They have also found that this Fe-S cluster isdelivered by the iron-sulfur cluster assembly factor IND1 (iron-sulfurcluster assembly protein known to be required specifically for NADHdehydrogenase), which was previously shown to take part in theassembly of the complex I (So et al.). This adds complexity to ourunderstanding of integration of the host (a proto-eukaryotic cell) andits symbiont (mitochondria) proteomes.The articles in the Research Topic “Energy-Producing Organellesand the Nucleus: A Phenomenal Genomic Friendship” represent anumber of excellent examples that show consequences ofmitonuclear discordance. The article of Triant and Pearsonexplores the methods to study mitonuclear interactions. Finally,the article of Christian et al. reviews mechanisms of proteintransport into non-green plastids, a good model to study how thehost proteins are delivered to the organelle of endosymbiotic origin.It is tempting to see the continuation of the studies conducted by thecontributors and further development of stories started on the pagesof Frontiers in Genetics. Indeed, we further learn that the BAR andCOX lines with mitonuclear mismatch respond to the N-acetylcysteine treatment by suppression of complex I-linked respiration(Camus et al., 2023). We also see a deeper study of protein-proteininteractions in mitochondrial DNA replication machinery in insectcells (Plaza et al., 2023).The general theme of the interaction of organellar and nucleargenomes is one of cooperation. This cooperation necessitatescompensatory evolution between two genomes with differentmutational processes and vastly different modes of inheritancemaking for very strange bedfellows indeed.In general, Frontiers in Genetics issues up to hundred ResearchTopics that explore different aspects of the endosymbiotic genomearchitecture and intergenomic communication. Among them, and inaddition to our Topic we would recommend readers to find even morein the parallel collections of articles such as “Impact of CytonuclearIncompatibilities on the Evolution of Species,” “MitochondrialGenomes and Mitochondrion Related Gene Insights to FungalEvolution,” “Evolution of Plant Mitochondrial Genomes,”“Evolution of Mitochondrial Genomes,” “Mitochondrial Geneticsand Epigenetics,” “Interorganelle communication in aging,” and others.Author contributionsDG: Writing—original draft. JWOB, MFC, RD, MG, and UR:Writing—review and editing. All authors contributed to the articleand approved the submitted version.Conflict of interestThe authors declare that the research was conducted in theabsence of any commercial or financial relationships that could beconstrued as a potential conflict of interest.Frontiers in Genetics frontiersin.org02Gospodaryov et al. 10.3389/fgene.2023.1230032Publisher’s noteAll claims expressed in this article are solely those of the authorsand do not necessarily represent those of their affiliatedorganizations, or those of the publisher, the editors and thereviewers. Any product that may be evaluated in this article, orclaim that may be made by its manufacturer, is not guaranteed orendorsed by the publisher.ReferencesCamus, M. F., Rodriguez, E., Kotiadis, V., Carter, H., and Lane, N. (2023). Redoxstress shortens lifespan through suppression of respiratory complex I in flies withmitonuclear incompatibilities. Exp. Gerontol. 175, 112158. doi:10.1016/j.exger.2023.112158Couvillion, M. T., Soto, I. C., Shipkovenska, G., and Churchman, L. S. (2016).Synchronized mitochondrial and cytosolic translation programs. Nature 533,499–503. doi:10.1038/nature18015Filée, J., and Forterre, P. (2005). Viral proteins functioning in organelles: A crypticorigin? Trends Microbiol. 13, 510–513. doi:10.1016/j.tim.2005.08.012Garg, S. G., and Martin, W. F. (2016). Mitochondria, the cell cycle, and the origin ofsex via a syncytial eukaryote common ancestor.Genome Biol. Evol. 8, 1950–1970. doi:10.1093/gbe/evw136Plaza, -G. A, I., Lemishko, K. M., Crespo, R., Truong, T. Q., Kaguni, L. S., Cao-García,F. J., et al. (2023). Mechanism of strand displacement DNA synthesis by the coordinatedactivities of human mitochondrial DNA polymerase and SSB. Nucleic Acids Res. 51,1750–1765. doi:10.1093/nar/gkad037Radzvilavicius, A. L., Hadjivasiliou, Z., Pomiankowski, A., and Lane, N. (2016).Selection for mitochondrial quality drives evolution of the germline. PLoS Biol. 14,e2000410. doi:10.1371/journal.pbio.2000410Shutt, T. E., and Gray, M. W. (2006). Bacteriophage origins of mitochondrialreplication and transcription proteins. Trends Genet. 22, 90–95. doi:10.1016/j.tig.2005.11.007Werren, J. H., Baldo, L., and Clark, M. E. (2008).Wolbachia: Master manipulators ofinvertebrate biology. Nat. Rev. Microbiol. 6, 741–751. doi:10.1038/nrmicro1969Frontiers in Genetics frontiersin.org03Gospodaryov et al. 10.3389/fgene.2023.1230032

Editorial: Energy-producing organelles and the nucleus: a phenomenal genomic friendship

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Editorial: Energy-producing organelles and the nucleus: a phenomenal genomic friendship

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