16 Sep 2023

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.
Advertisement
Heredity (2023)
Metrics details
Several functional classes of short noncoding RNAs are involved in manifold regulatory processes in eukaryotes, including, among the best characterized, miRNAs. One of the most intriguing regulatory networks in the eukaryotic cell is the mito-nuclear crosstalk: recently, miRNA-like elements of mitochondrial origin, called smithRNAs, were detected in a bivalve species, Ruditapes philippinarum. These RNA molecules originate in the organelle but were shown in vivo to regulate nuclear genes. Since miRNA genes evolve easily de novo with respect to protein-coding genes, in the present work we estimate the probability with which a newly arisen smithRNA finds a suitable target in the nuclear transcriptome. Simulations with transcriptomes of 12 bivalve species suggest that this probability is high and not species specific: one in a hundred million (1 × 10−8) if five mismatches between the smithRNA and the 3’ mRNA are allowed, yet many more are allowed in animals. We propose that novel smithRNAs may easily evolve as exaptation of the pre-existing mitochondrial RNAs. In turn, the ability of evolving novel smithRNAs may have played a pivotal role in mito-nuclear interactions during animal evolution, including the intriguing possibility of acting as speciation trigger.
This is a preview of subscription content, access via your institution

Subscribe to this journal
Receive 12 print issues and online access
251,40 € per year
only 20,95 € per issue

Rent or buy this article
Prices vary by article type
from$1.95
to$39.95

Prices may be subject to local taxes which are calculated during checkout
All data used for the present study are publicly available in GenBank.
Andersson DI, Jerlstrom-Hultqvist J, Nasvall J (2015) Evolution of new functions de novo and from preexisting genes. Cold Spring Harb Perspect Biol 7:a017996
Article  PubMed  PubMed Central  Google Scholar 
Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/
Auyeung VC, Ulitsky I, McGeary SE, Bartel DP (2013) Beyond secondary structure: primary-sequence determinants license pri-miRNA hairpins for processing. Cell 152:844–858
Article  CAS  PubMed  PubMed Central  Google Scholar 
Babiarz JE, Ruby JG, Wang Y, Bartel DP, Blelloch R (2008) Mouse ES cells express endogenous shRNAs, siRNAs, and other microprocessor-independent, dicer-dependent small RNAs. Genes Dev 22:2773–2785
Article  CAS  PubMed  PubMed Central  Google Scholar 
Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136:215–233
Article  CAS  PubMed  PubMed Central  Google Scholar 
Bartel DP (2018) Metazoan microRNAs. Cell 173:20–51
Article  CAS  PubMed  PubMed Central  Google Scholar 
Berezikov E, Liu N, Flynt AS, Hodges E, Rooks M, Hannon GJ et al. (2010) Evolutionary flux of canonical microRNAs and mirtrons in Drosophila. Nat Genet 42:6–9
Article  CAS  PubMed  PubMed Central  Google Scholar 
Bernstein E, Caudy AA, Hammond SM, Hannon GJ (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409:363–366
Article  CAS  PubMed  Google Scholar 
Bettinazzi S, Plazzi F, Passamonti M (2016) The complete female- and male-transmitted mitochondrial genome of Meretrix lamarckii. PLoS ONE 11:e0153631
Article  PubMed  PubMed Central  Google Scholar 
Bofill-De Ros X, Yang A, Gu S (2020) IsomiRs: expanding the miRNA repression toolbox beyond the seed. Biochim Biophys Acta Gene Regul Mech 1863:194373
Article  CAS  PubMed  Google Scholar 
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120
Article  CAS  PubMed  PubMed Central  Google Scholar 
Boore JL (1999) Animal mitochondrial genomes. Nucleic Acids Res 27:1767–1780
Article  CAS  PubMed  PubMed Central  Google Scholar 
Bottje WG, Khatri B, Shouse SA, Seo D, Mallmann B, Orlowski SK et al. (2017) Identification and differential abundance of mitochondrial genome encoding small RNAs (mitosRNA) in breast muscles of modern broilers and unselected chicken breed. Front Physiol 8:816
Article  PubMed  PubMed Central  Google Scholar 
Bråte J, Neumann RS, Fromm B, Haraldsen AAB, Tarver JE, Suga H et al. (2018) Unicellular origin of the animal microRNA machinery. Curr Biol 28:3288–3295.e5
Article  PubMed  PubMed Central  Google Scholar 
Breton S, Milani L, Ghiselli F, Guerra D, Stewart DT, Passamonti M (2014) A resourceful genome: updating the functional repertoire and evolutionary role of animal mitochondrial DNAs. Trends Genet 30:555–564
Article  CAS  PubMed  Google Scholar 
Burton RS, Barreto FS (2012) A disproportionate role for mtDNA in Dobzhansky-Muller incompatibilities? Mol Ecol 21:4942–4957
Article  CAS  PubMed  Google Scholar 
Cavalier-Smith T (2010) Origin of the cell nucleus, mitosis and sex: roles of intracellular coevolution. Biol Direct 5:7
Article  PubMed  PubMed Central  Google Scholar 
Cerutti H, Casas-Mollano JA (2006) On the origin and functions of RNA-mediated silencing: from protists to man. Curr Genet 50:81–99
Article  CAS  PubMed  PubMed Central  Google Scholar 
Chen CZ, Schaffert S, Fragoso R, Loh C (2013) Regulation of immune responses and tolerance: the microRNA perspective. Immunol Rev 253:112–128
Article  PubMed  PubMed Central  Google Scholar 
Chen L, Dahlstrom JE, Lee S-H, Rangasamy D (2012) Naturally occurring endo-siRNA silences LINE-1 retrotransposons in human cells through DNA methylation. Epigenetics 7:758–771
Article  CAS  PubMed  Google Scholar 
Clayton DA (2000) Transcription and replication of mitochondrial DNA. Hum Reprod 15:11–17
Article  PubMed  Google Scholar 
Cohen P (2014) New role for the mitochondrial peptide humanin: protective agent against chemotherapy-induced side effects. J Natl Cancer Inst 106:dju006
Article  PubMed  PubMed Central  Google Scholar 
Connelly SV, Manzella-Lapeira J, Levine ZC, Brzostowski J, Krymskaya L, Rahman RS et al. (2021) Restructured mitochondrial-nuclear interaction in Plasmodium falciparum dormancy and persister survival after artemisinin exposure. mBio 12:e00753–21
Article  CAS  PubMed  PubMed Central  Google Scholar 
Czech B, Malone CD, Zhou R, Stark A, Schlingeheyde C, Dus M et al. (2008) An endogenous small interfering RNA pathway in Drosophila. Nature 453:798–802
Article  CAS  PubMed  PubMed Central  Google Scholar 
D’Souza AR, Minczuck M (2018) Mitochondrial transcription and translation: overview. Ess Biochem 62:309–320
Article  Google Scholar 
Desvignes T, Sydes J, Montfort J, Bobe J, Postlethwait JH (2021) Evolution after whole-genome duplication: teleost microRNAs. Mol Biol Evol 38:3308–3331
Article  CAS  PubMed  PubMed Central  Google Scholar 
Dexheimer PJ, Cochella L (2020) MicroRNAs: from mechanism to organism. Front Cell Dev Biol 8:409
Article  PubMed  PubMed Central  Google Scholar 
Dobzhansky T (1937) Genetics and the origin of species. Columbia University Press, New York
Google Scholar 
Dowling DK, Friberg U, Lindell J (2008) Evolutionary implication of non-neutral mitochondrial genetic variation. Trends Ecol Evol 23:546–554
Article  PubMed  Google Scholar 
Fang W, Bartel DP (2015) The menu of features that define primary microRNAs and enable de novo design of microRNA genes. Mol Cell 60:131–145
Article  CAS  PubMed  PubMed Central  Google Scholar 
Formaggioni A, Luchetti A, Plazzi F (2021) Mitochondrial genomic landscape: a portrait of the mitochondrial genome 40 years after the first complete sequence. Life 11:663
Article  PubMed  PubMed Central  Google Scholar 
Furuse Y, Finethy R, Saka HA, Xet-Mull AM, Sisk DM, Smith KL et al. (2014) Search for microRNAs expressed by intracellular bacterial pathogens in infected mammalian cells. PLoS ONE 9:e106434
Article  PubMed  PubMed Central  Google Scholar 
García-López J, Brieño-Enríquez MA, del Mazo J (2013) MicroRNA biogenesis and variability. BioMol Concepts 4:367–380
Article  PubMed  Google Scholar 
Gershoni M, Templeton AR, Mishmar D (2009) Mitochondrial bioenergetics as a major motive force of speciation. Bioessays 31:642–650
Article  CAS  PubMed  Google Scholar 
Ghildiyal M, Seitz H, Horwich MD, Li C, Du T, Lee S et al. (2008) Endogenous siRNAs derived from transposons and mRNAs in Drosophila somatic cells. Science 320:1077–1081
Article  CAS  PubMed  PubMed Central  Google Scholar 
Ghildiyal M, Zamore PD (2009) Small silencing RNAs: an expanding universe. Nat Rev Genet 10:94–108
Article  CAS  PubMed  PubMed Central  Google Scholar 
Ghiselli F, Gomes-dos-Santos A, Adema CM, Lopes-Lima M, Sharbrough J, Boore JL (2021) Molluscan mitochondrial genomes break the rules. Philos Trans R Soc B 376:20200159
Article  Google Scholar 
Ghiselli F, Milani L, Guerra D, Chang PL, Breton S, Nuzhdin SV et al. (2013) Structure, transcription, and variability of metazoan mitochondrial genome: perspectives from an unusual mitochondrial inheritance system. Genome Biol Evol 5:1535–1554
Article  CAS  PubMed  PubMed Central  Google Scholar 
Gouzy J, Carrere S, Schiex T (2009) FrameDP: sensitive peptide detection on noisy matured sequences. Bioinformatics 25:670–671
Article  CAS  PubMed  PubMed Central  Google Scholar 
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I et al. (2011) Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat Biotechnol 29:644–652
Article  CAS  PubMed  PubMed Central  Google Scholar 
Ha M, Kim VN (2014) Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol 15:509–524
Article  CAS  PubMed  Google Scholar 
Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J et al. (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 8:1494–1512
Article  CAS  PubMed  Google Scholar 
Hemmi K, Kakehashi R, Kambayashi C, Du Preez L, Minter L, Furuno N et al. (2020) Exceptional enlargement of the mitochondrial genome results from distinct causes in different rain frogs (Anura: Brevicipitidae: Breviceps). Int J Genomics 2020:6540343
Article  PubMed  PubMed Central  Google Scholar 
Hertel J, Stadler PF (2015) The expansion of animal microRNA families revisited. Life (Basel) 5:905–920
CAS  PubMed  Google Scholar 
Hill GE (2019) Mitonuclear ecology. Oxford series in ecology and evolution. Oxford University Press, Oxford
Book  Google Scholar 
Hillen HS, Temiakov D, Cramer P (2018) Structural basis of mitochondrial transcription. Nat Struct Mol Biol 25:754–765
Article  CAS  PubMed  PubMed Central  Google Scholar 
Huang Z, Teeling EC (2017) ExUTR: a novel pipeline for large-scale prediction of 3’-UTR sequences from NGS data. BMC Genomics 18:847
Article  PubMed  PubMed Central  Google Scholar 
Jiao Y, Zheng Z, Du X, Wang Q, Huang R, Deng Y et al. (2014) Identification and characterization of microRNAs in pearl oyster Pinctada martensii by solexa deep sequencing. Mar Biotechnol 16:54–62
Article  CAS  Google Scholar 
Kawamura Y, Saito K, Kin T, Ono Y, Asai K, Sunohara T et al. (2008) Drosophila endogenous small RNAs bind to Argonaute 2 in somatic cells. Nature 453:793–797
Article  CAS  PubMed  Google Scholar 
Kim SS, Lee S-JV (2019) Non-coding RNAs in Caenorhabditis elegans aging. Mol Cells 42:379–385
CAS  PubMed  PubMed Central  Google Scholar 
Komatsu S, Kitai H, Suzuki HI (2023) Network regulation of microRNA biogenesis and target interaction. Cells 12:306
Article  CAS  PubMed  PubMed Central  Google Scholar 
Kutyumov VA, Predeus AV, Starunov VV, Maltseva AL, Ostrovsky AN (2021) Mitochondrial gene order of the freshwater bryozoan Cristatella mucedo retains ancestral lophotrochozoan features. Mitochondrion 59:96–104
Article  CAS  PubMed  Google Scholar 
Landerer E, Villegas J, Burzio VA, Oliveira L, Villota C, Lopez C et al. (2011) Nuclear localization of the mitochondrial ncRNAs in normal and cancer cells. Cell Oncol (Dordr) 34:297–305
Article  CAS  PubMed  Google Scholar 
Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25
Article  PubMed  PubMed Central  Google Scholar 
Larriba E, del Mazo J (2016) Role of non-coding RNAs in the transgenerational epigenetic transmission of the effects of reprotoxicants. Int J Mol Sci 17:452
Article  PubMed  PubMed Central  Google Scholar 
Lavrov D, Pett W (2016) Animal mitochondrial DNA as we do not know it: mt-genome organization and evolution in nonbilaterian lineages. Genome Biol Evol 8:2896–2913
Article  CAS  PubMed  PubMed Central  Google Scholar 
Lavrov DV, Pett W, Voigt O, Wörheide G, Forget L, Lang BF et al. (2013) Mitochondrial DNA of Clathrina clathrus (Calcarea, Calcinea): six linear chromosomes, fragmented rRNAs, tRNA editing, and a novel genetic code. Mol Biol Evol 30:865–880
Article  CAS  PubMed  Google Scholar 
Lee C, Yen K, Cohen P (2013) Humanin: a harbinger of mitochondrial-derived peptides? Trends Endocrinol Metab 24:222–228
Article  CAS  PubMed  PubMed Central  Google Scholar 
Li HW, Ding SW (2005) Antiviral silencing in animals. FEBS Lett 579:5965–5973
Article  CAS  PubMed  PubMed Central  Google Scholar 
Li Y, Kocot KM, Tassia MG, Cannon JT, Bernt M, Halanych KM (2018) Mitogenomics reveals a novel genetic code in hemichordata. Genome Biol Evol 11:29–40
Article  PubMed Central  Google Scholar 
Lu J, Fu Y, Kumar S, Shen Y, Zeng K, Xu A et al. (2008a) Adaptive evolution of newly emerged micro-RNA genes in Drosophila. Mol Biol Evol 25:929–938
Article  CAS  PubMed  PubMed Central  Google Scholar 
Lu J, Shen Y, Wu Q, Kumar S, He B, Shi S et al. (2008b) The birth and death of microRNA genes in Drosophila. Nat Genet 40:351–355
Article  CAS  PubMed  Google Scholar 
Lynch M (2007) The evolution of genetic networks by non-adaptive processes. Nat Rev Genet 8:803–813
Article  CAS  PubMed  Google Scholar 
Lyu Y, Shen Y, Li H, Chen Y, Guo L, Zhao Y et al. (2014) New microRNAs in Drosophila—birth, death and cycles of adaptive evolution. PLoS Genet 10:e1004096
Article  PubMed  PubMed Central  Google Scholar 
Ma X, He K, Shi Z, Li M, Li F, Chen X-X (2021) Large-scale annotation and evolution analysis of miRNA in insects. Genome Biol Evol 13:evab083
Article  PubMed  PubMed Central  Google Scholar 
Maniataki E, Mourelatos Z (2005) Human mitochondrial tRNAMet is exported to the cytoplasm and associates with the Argonaute 2 protein. RNA 11:849–852
Article  CAS  PubMed  PubMed Central  Google Scholar 
Marker C, Zemann A, Terhörst T, Kiefmann M, Kastenmayer JP, Green P et al. (2002) Experimental RNomics: identification of 140 candidates for small non-messenger RNAs in the plant Arabidopsis thaliana. Curr Biol 12:2002–2013
Article  CAS  PubMed  Google Scholar 
Matzke MA, Birchler JA (2005) RNAi-mediated pathways in the nucleus. Nat Rev Genet 6:24–35
Article  CAS  PubMed  Google Scholar 
McGeary SE, Lin KS, Shi CY, Pham TM, Bisaria N, Kelley GM et al. (2019) The biochemical basis of microRNA targeting efficacy. Science 366:eaav1741
Article  CAS  PubMed  PubMed Central  Google Scholar 
Mercer TR, Neph S, Dinger ME, Crawford J, Smith MA, Shearwood A-MJ et al. (2011) The human mitochondrial transcriptome. Cell 146:645–658
Article  CAS  PubMed  PubMed Central  Google Scholar 
Michlewski G, Cáceres JF (2019) Post-transcriptional control of miRNA biogenesis. RNA 25:1–16
Article  CAS  PubMed  PubMed Central  Google Scholar 
Milani L, Ghiselli F, Maurizii MG, Passamonti M (2011) Doubly uniparental inheritance of mitochondria as a model system for studying germ line formation. PLoS ONE 6:e28194
Article  CAS  PubMed  PubMed Central  Google Scholar 
Mohammed J, Bortolamiol-Becet D, Flynt AS, Gronau I, Siepel A, Lai EC (2014) Adaptive evolution of testis-specific, recently evolved, clustered miRNAs in Drosophila. RNA 20:1195–1209
Article  CAS  PubMed  PubMed Central  Google Scholar 
Mohammed J, Flynt AS, Panzarino AM, Mondal MMH, DeCruz M, Siepel A et al. (2018) Deep experimental profiling of microRNA diversity, deployment, and evolution across the Drosophila genus. Genome Res 28:52–65
Article  CAS  PubMed  PubMed Central  Google Scholar 
Monnens M, Thijs S, Briscoe AG, Clark M, Frost EJ, Littlewood DTJ et al. (2020) The first mitochondrial genomes of endosymbiotic rhabdocoels illustrate evolutionary relaxation of atp8 and genome plasticity in flatworms. Int J Biol Macromol 162:454–469
Article  CAS  PubMed  Google Scholar 
Moran Y, Agron M, Praher D, Technau U (2017) The evolutionary origin of plant and animal microRNAs. Nat Ecol Evol 1:27
Article  PubMed  Google Scholar 
Muller HJ (1942) Isolating mechanisms, evolution, and temperature. Biol Symp 6:71–125
Google Scholar 
O’Brien J, Hayder H, Zayed Y, Peng C (2018) Overview of microRNA biogenesis, mechanisms of actions, and circulation. Front Endocrinol 9:402
Article  Google Scholar 
Okamura K, Chung W-J, Ruby JG, Guo H, Bartel DP, Lai EC (2008) The Drosophila hairpin RNA pathway generates endogenous short interfering RNAs. Nature 453:803–806
Article  CAS  PubMed  PubMed Central  Google Scholar 
Osigus H-J, Eitel M, Schierwater B (2017) Deep RNA sequencing reveals the smallest known mitochondrial micro exon in animals: the placozoan cox1 single base pair exon. PLoS ONE 12:e0177959
Article  PubMed  PubMed Central  Google Scholar 
Ovciarikova J, Shikha S, Sheiner L (2022) Nuclear interactions: a spotlight on nuclear mitochondrial membrane contact sites. Contact 5:1–7
Article  Google Scholar 
Passamonti M, Calderone M, Delpero M, Plazzi F (2020) Clues of in vivo nuclear gene regulation by mitochondrial short non-coding RNAs. Sci Rep 10:8219
Article  CAS  PubMed  PubMed Central  Google Scholar 
Passamonti M, Ghiselli F (2009) Doubly uniparental inheritance: two mitochondrial genomes, one precious model for organelle DNA inheritance and evolution. DNA Cell Biol 28:79–89
Article  CAS  PubMed  Google Scholar 
Passamonti M, Plazzi F (2020) Doubly uniparental inheritance and beyond: the contribution of the Manila clam Ruditapes philippinarum. J Zool Syst Evol Res 58:529–540
Article  Google Scholar 
Petrov DA, Hartl DL (1998) High rate of DNA loss in the Drosophila melanogaster and Drosophila virilis species groups. Mol Biol Evol 15:293–302
Article  CAS  PubMed  Google Scholar 
Petrov DA, Lozovskaya ER, Hartl DL (1996) High intrinsic rate of DNA loss in Drosophila. Nature 384:346–349
Article  CAS  PubMed  Google Scholar 
Phillips D, Reilley MJ, Aponte AM, Wang G, Boja E, Gucek M et al. (2010) Stoichiometry of STAT3 and mitochondrial proteins: implications for the regulation of oxidative phosphorylation by protein-protein interactions. J Biol Chem 285:23532–23536
Article  CAS  PubMed  PubMed Central  Google Scholar 
Plazzi F, Ribani A, Passamonti M (2013) The complete mitochondrial genome of Solemya velum (Mollusca: Bivalvia) and its relationships with Conchifera. BMC Genomics 14:409
Article  CAS  PubMed  PubMed Central  Google Scholar 
Poole CB, Gu W, Kumar S, Jin J, Davis PJ, Bauche D et al. (2014) Diversity and expression of microRNAs in the filarial parasite, Brugia malayi. PLoS ONE 9:e96498
Article  PubMed  PubMed Central  Google Scholar 
Pozzi A, Dowling DK (2022) New insights into mitochondrial–nuclear interactions revealed through analysis of small RNAs. Genome Biol Evol 14:evac023
Article  CAS  PubMed  PubMed Central  Google Scholar 
Pozzi A, Plazzi F, Milani L, Ghiselli F, Passamonti M (2017) SmithRNAs: could mitochondria “bend” nuclear regulation? Mol Biol Evol 34:1960–1973
Article  CAS  PubMed  PubMed Central  Google Scholar 
Pu L, Liu H, Wang G, Li B, Xia G, Shen M et al. (2019) Complete mitochondrial genome of the cockle Anadara antiquata (Linnaeus, 1758). Mitochondrial DNA Part B Resour 4:2293–2294
Article  Google Scholar 
Rackham O, Shearwood AM, Mercer TR, Davies SM, Mattick JS, Filipovska A (2011) Long noncoding RNAs are generated from the mitochondrial genome and regulated by nuclear-encoded proteins. RNA 17:2085–2093
Article  CAS  PubMed  PubMed Central  Google Scholar 
Rand DM, Hanley RA, Fry AJ (2004) Cytonuclear coevolution: the genomics of cooperation. Trends Ecol Evol 19:645–653
Article  PubMed  Google Scholar 
Riggs CL, Summers A, Warren DE, Nilsson GE, Lefevre S, Dowd WW et al. (2018) Small non-coding RNA expression and vertebrate anoxia tolerance. Front Genet 9:230
Article  PubMed  PubMed Central  Google Scholar 
Rissland OS (2020) Big insights into small RNAs. Biochemistry 59:1551–1552
Article  CAS  PubMed  Google Scholar 
Ro S, Ma H-Y, Park C, Ortogero N, Song R, Hennig GW et al. (2013) The mitochondrial genome encodes abundant small noncoding RNAs. Cell Res 23:759–774
Article  CAS  PubMed  PubMed Central  Google Scholar 
Ruby JG, Jan CH, Bartel DP (2007) Intronic microRNA precursors that bypass Drosha processing. Nature 448:83–86
Article  CAS  PubMed  PubMed Central  Google Scholar 
Schlotterer C (2015) Genes from scratch – the evolutionary fate of de novo genes. Trends Genet 31:215–219
Article  PubMed  PubMed Central  Google Scholar 
Schuster A, Lopez JV, Becking LE, Kelly M, Pomponi SA, Wörheide G et al. (2017) Evolution of group I introns in Porifera: new evidence for intron mobility and implications for DNA barcoding. BMC Evol Biol 17:82
Article  PubMed  PubMed Central  Google Scholar 
Shabalina SA, Koonin EV (2008) Origins and evolution of eukaryotic RNA interference. Trends Ecol Evol 23:P578–P587
Article  Google Scholar 
Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM (2015) BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31:3210–3212
Article  PubMed  Google Scholar 
Taanmann JW (1999) The mitochondrial genome: structure, transcription, translation and replication. Biochim Biophys Acta 1410:103–123
Article  Google Scholar 
Tam OH, Aravin AA, Stein P, Girard A, Murchison EP, Cheloufi S et al. (2008) Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 453:534–538
Article  CAS  PubMed  PubMed Central  Google Scholar 
Tan GC, Chan E, Molnar A, Sarkar R, Alexieva D, Isa IM et al. (2014) 5’ isomiR variation is of functional and evolutionary importance. Nucleic Acids Res 42:9424–9435
Article  CAS  PubMed  PubMed Central  Google Scholar 
Torri A, Jaeger J, Pradeu T, Saleh M-C (2022) The origin of RNA interference: adaptive or neutral evolution? PLoS Biol 20:e3001715
Article  CAS  PubMed  PubMed Central  Google Scholar 
Trindade Rosa M, Oliveira DS, Loreto ELS (2017) Characterization of the first mitochondrial genome of a catenulid flatworm: Stenostomum leucops (Platyhelminthes). J Zool Syst Evol Res 55:98–105
Article  Google Scholar 
van Wijnen AJ, van de Peppel J, van Leeuwen JP, Lian JB, Stein GS, Westendorf JJ et al. (2013) MicroRNA functions in osteogenesis and dysfunctions in osteoporosis. Curr Osteoporos Rep 11:72–82
Article  PubMed  PubMed Central  Google Scholar 
VanKuren NW, Long M (2018) Gene duplicates resolving sexual conflict rapidly evolved essential gametogenesis functions. Nat Ecol Evol 2:705–712
Article  PubMed  PubMed Central  Google Scholar 
Velandia-Huerto CA, Yazbeck AM, Schor J, Stadler PF (2022) Evolution and phylogeny of microRNAs – protocols, pitfalls, and problems. Methods Mol Biol 2257:211–233
Article  PubMed  Google Scholar 
Vendramin R, Marine JC, Leucci E (2017) Non-coding RNAs: the dark side of nuclear-mitochondrial communication. EMBO J 36:1123–1133
Article  CAS  PubMed  PubMed Central  Google Scholar 
Wagner EG, Simons RW (1994) Antisense RNA control in bacteria, phages, and plasmids. Annu Rev Microbiol 48:713–742
Article  CAS  PubMed  Google Scholar 
Wang M, Jiang S, Wu W, Yu F, Chang W, Li P et al. (2018) Non-coding RNAs function as immune regulators in teleost fish. Front Immunol 9:2801
Article  PubMed  PubMed Central  Google Scholar 
Watanabe T, Totoki Y, Toyoda A, Kaneda M, Kuramochi-Miyagawa S, Obata Y et al. (2008) Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 453:539–543
Article  CAS  PubMed  Google Scholar 
Weber-Lotfi F, Dietrich A (2018) Intercompartment RNA trafficking in mitochondrial function and communication. In: Cruz-Reyes J, Gray M (eds) RNA metabolism in mitochondria. nucleic acids and molecular biology 34. Springer, Cham, p 73–124
Chapter  Google Scholar 
Wood DE, Lu J, Langmead B (2019) Improved metagenomic analysis with Kraken 2. Genome Biol 20:257
Article  CAS  PubMed  PubMed Central  Google Scholar 
Yang N, Kazazian Jr HH (2006) L1 retrotransposition is suppressed by endogenously encoded small interfering RNAs in human cultured cells. Nat Struct Mol Biol 13:763–771
Article  CAS  PubMed  Google Scholar 
Yazbeck AM, Tout KR, Stadler PF, Hertel J (2017) Towards a consistent, quantitative evaluation of microRNA evolution. J Integr Bioinform 14:20160013
Article  PubMed  PubMed Central  Google Scholar 
Yekta S, Tabin CJ, Bartel DP (2008) MicroRNAs in the Hox network: an apparent link to posterior prevalence. Nat Rev Genet 9:789–796
Article  CAS  PubMed  PubMed Central  Google Scholar 
Zhao Y, Lu G-A, Yang H, Lin P, Liufu Z, Tang T et al. (2021) Run or die in the evolution of new microRNAs–testing the red queen hypothesis on de novo new genes. Mol Biol Evol 38:1544–1553
Article  CAS  PubMed  Google Scholar 
Zouros E, Rodakis GC (2019) Doubly uniparental inheritance of mtDNA: an unappreciated defiance of a general rule. Adv Anat Embryol Cell Biol 231:25–49
Article  PubMed  Google Scholar 
Download references
This study was supported by the Italian Ministry of University and Research PRIN 2020 (2020BE2BC3) funded to MP. YLC was supported by EUR G.E.N.E. (reference #ANR-17-EURE-0013) and is part of the Université Paris Cité (IdEx #ANR-18-IDEX-0001), funded by the French Government through its “Investments for the Future” program. We are grateful to the people at the ESEB 2022 symposium “Beyond transcription: the role of post-transcriptional gene regulation in adaptation and evolution” for sharing ideas and suggestions. We also want to thank three anonymous reviewers, whose comments and criticism greatly improved the original manuscript.
Youn Le Cras
Present address: Magistère Européen de Génétique, Université Paris Cité, 85 Boulevard Saint Germain, 75006, Paris, Italy
Department of Biological, Geological and Environmental Sciences, University of Bologna, via Selmi, 3 – 40126, Bologna, BO, Italy
Federico Plazzi, Youn Le Cras, Alessandro Formaggioni & Marco Passamonti
You can also search for this author in PubMed Google Scholar
You can also search for this author in PubMed Google Scholar
You can also search for this author in PubMed Google Scholar
You can also search for this author in PubMed Google Scholar
FP and MP conceived and supervised the study. YLC and AF analyzed the data. FP and MP drafted the original manuscript. All authors read and approved the final manuscript.
Correspondence to Federico Plazzi.
The authors declare no competing interests.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
Reprints and Permissions
Plazzi, F., Le Cras, Y., Formaggioni, A. et al. Mitochondrially mediated RNA interference, a retrograde signaling system affecting nuclear gene expression. Heredity (2023). https://doi.org/10.1038/s41437-023-00650-5
Download citation
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1038/s41437-023-00650-5
Anyone you share the following link with will be able to read this content:
Sorry, a shareable link is not currently available for this article.

Provided by the Springer Nature SharedIt content-sharing initiative

Advertisement
Heredity (Heredity) ISSN 1365-2540 (online) ISSN 0018-067X (print)
© 2023 Springer Nature Limited

source

Leave a Reply

Your email address will not be published. Required fields are marked *

This field is required.

This field is required.