Lack of transcriptional coordination between mitochondrial and nuclear oxidative phosphorylation genes in the presence of two divergent mitochondrial genomes

Xu, Ran; Iannello, Mariangela; Havird, Justin C.; Milani, Liliana; Ghiselli, Fabrizio

doi:10.24272/j.issn.2095-8137.2021.348

Cited by 4 publications

(1 citation statement)

References 121 publications

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“…Numerous works have sought to elucidate the molecular mechanisms beyond DUI and speculated on the evolutionary process behind the maintenance of divergent mtDNA lineages within species, especially considering that heteroplasmy is generally considered an unfavorable condition, generally converging on the hypothesis that DUI might be linked to sexual differentiation ( Breton et al 2018 ; Capt et al 2018 ). Having two different mitochondrial genomes with sex-specific and tissue-specific distribution opens up questions about the existence of tissue and sex-specific coordination of gene regulation, namely regarding nuclear genes involved in mitochondrial biology ( Ghiselli et al 2021b ; Maeda et al 2021 ; Xu et al 2022 ).…”

Section: Introductionmentioning

confidence: 99%

Multi-tissue RNA-Seq Analysis and Long-read-based Genome Assembly Reveal Complex Sex-specific Gene Regulation and Molecular Evolution in the Manila Clam

Martelossi

Smits

et al. 2022

Genome Biology and Evolution

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The molecular factors and gene regulation involved in sex determination and gonad differentiation in bivalve molluscs are unknown. It has been suggested that doubly uniparental inheritance (DUI) of mitochondria may be involved in these processes in species such as the ubiquitous and commercially relevant Manila clam, Ruditapes philippinarum. We present the first long-read-based de novo genome assembly of a Manila clam, and a RNA-Seq multi-tissue analysis of 15 females and 15 males. The highly contiguous genome assembly was used as reference to investigate gene expression, alternative splicing, sequence evolution, tissue-specific co-expression networks, and sexual contrasting SNPs. Differential expression and differential splicing analyses revealed sex-specific transcriptional regulation in gonads, but not in somatic tissues. Co-expression networks revealed complex gene regulation in gonads, and genes in gonad-associated modules showed high tissue specificity. However, male gonad-associated modules showed contrasting patterns of sequence evolution and tissue specificity. One gene set was related to the structural organization of male gametes and presented slow sequence evolution but high pleiotropy, while another gene set was enriched in reproduction-related processes and characterized by fast sequence evolution and tissue specificity. Sexual contrasting SNPs were found in genes overrepresented in mitochondrial related functions, providing new candidates for investigating the relationship between mitochondria and sex in DUI species. Together, these results increase our understanding of the role of differential expression, differential splicing, and sequence evolution of sex-specific genes in an understudied taxon. We also provide resourceful genomic data for studies regarding sex diagnosis and breeding in bivalves.

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Section: Introductionmentioning

confidence: 99%

Multi-tissue RNA-Seq Analysis and Long-read-based Genome Assembly Reveal Complex Sex-specific Gene Regulation and Molecular Evolution in the Manila Clam

Martelossi

Smits

et al. 2022

Genome Biology and Evolution

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Mitonuclear compatibility is maintained despite relaxed selection on male mitochondrial DNA in bivalves with doubly uniparental inheritance

Smith,

Mejia-Trujillo,

Havird

2024

Evolution

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Mitonuclear coevolution is common in eukaryotes, but bivalve lineages that have doubly uniparental inheritance (DUI) of mitochondria may be an interesting example. In this system, females transmit mtDNA (F mtDNA) to all offspring, while males transmit a different mtDNA (M mtDNA) solely to their sons. Molecular evolution and functional data suggest oxidative phosphorylation (OXPHOS) genes encoded in M mtDNA evolve under relaxed selection due to their function being limited to sperm only (vs. all other tissues for F mtDNA). This has led to the hypothesis that mitonuclear coevolution is less important for M mtDNA. Here, we use comparative phylogenetics, transcriptomics, and proteomics to understand mitonuclear interactions in DUI bivalves. We found nuclear OXPHOS proteins coevolve and maintain compatibility similarly with both F and M mtDNA OXPHOS proteins. Mitochondrial recombination did not influence mitonuclear compatibility and nuclear-encoded OXPHOS genes were not upregulated in tissues with M mtDNA to offset dysfunction. Our results support that selection maintains mitonuclear compatibility with F and M mtDNA despite relaxed selection on M mtDNA. Strict sperm transmission, lower effective population size, and higher mutation rates may explain the evolution of M mtDNA. Our study highlights that mitonuclear coevolution and compatibility may be broad features of eukaryotes.

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Bivalves as Emerging Model Systems to Study the Mechanisms and Evolution of Sex Determination: A Genomic Point of View

Nicolini,

Ghiselli,

Luchetti

et al. 2023

Genome Biology and Evolution

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Bivalves are a diverse group of molluscs that have recently attained a central role in plenty of biological research fields, thanks to their peculiar life history traits. Here we propose that bivalves should be considered as emerging model systems also in sex-determination studies, since they would allow to investigate: (i) the transition between environmental and genetic sex determination, with respect to different reproductive backgrounds and sexual systems (from species with strict gonochorism to species with various forms of hermaphroditism); (ii) the genomic evolution of sex chromosomes, considering that no heteromorphic sex chromosomes are currently known and that homomorphic sex chromosomes have been identified just in few species of scallops; (iii) the putative role of mitochondria at some level of the sex determination signaling pathway, in a mechanism that may resemble the cytoplasmatic male sterility of plants; (iv) the evolutionary history of sex-determination related gene families with respect to other animal groups. In particular, we think that this last topic may lay the foundations for expanding our understanding of bivalve sex determination, as our current knowledge is quite fragmented and limited to few species. As a matter of fact, tracing the phylogenetic history and diversity of sex-determination related gene families (such as the Dmrt, Sox and Fox genes) would allow to perform more targeted functional experiments and genomic analyses, but also fostering the possibility of establishing a solid comparative framework.

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Lack of transcriptional coordination between mitochondrial and nuclear oxidative phosphorylation genes in the presence of two divergent mitochondrial genomes

Cited by 4 publications

References 121 publications

Multi-tissue RNA-Seq Analysis and Long-read-based Genome Assembly Reveal Complex Sex-specific Gene Regulation and Molecular Evolution in the Manila Clam

Multi-tissue RNA-Seq Analysis and Long-read-based Genome Assembly Reveal Complex Sex-specific Gene Regulation and Molecular Evolution in the Manila Clam

Mitonuclear compatibility is maintained despite relaxed selection on male mitochondrial DNA in bivalves with doubly uniparental inheritance

Bivalves as Emerging Model Systems to Study the Mechanisms and Evolution of Sex Determination: A Genomic Point of View

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