Cytonuclear coevolution in a holoparasitic plant with highly disparate organellar genomes

Ceriotti, Luis F; Gatica-Soria, Leonardo M; Sanchez‐Puerta, M. Virginia

doi:10.1007/s11103-022-01266-9

Cited by 8 publications

(7 citation statements)

References 95 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Other studies of this complex further indicated that the rates of clpP1 evolution strongly correlate with the amino acid sequence divergence in interacting nuclear‐encoded CLP counterparts in various angiosperms (Rockenbach et al., 2016; Williams et al., 2019). This may reflect the coevolution of genes involved in cytonuclear interactions to keep them functional (Abdel‐Ghany et al., 2022; Ceriotti et al., 2022; Forsythe et al., 2021; Sloan et al., 2014; Williams et al., 2019). Among the genes involved in the cytonuclear complexes, we were able to identify PSBW , involved in the PSII supercomplex, with a biased expression in advanced generations, and differences in the amino acid sequence between Lolium and Festuca .…”

Section: Discussionmentioning

confidence: 99%

“…These challenges encompass chromosomal rearrangements, mitotic and meiotic abnormalities, and genome‐wide gene expression alterations affected by epigenetic responses to the novel genomic constitution (Glombik et al., 2021; Kopecky et al., 2009; Majka et al., 2023; Svačina et al., 2020). One of the challenges for newly arising polyploids is the disruption of stoichiometry between nuclear‐ and organelle‐encoded genes (Ceriotti et al., 2022; Fernandes Gyorfy et al., 2021; Ferreira de Carvalho et al., 2019; Gong et al., 2012, 2014; Li et al., 2020, 2022; Sehrish et al., 2015; Sharbrough et al., 2017; Wang et al., 2017; Zhai et al., 2019). Core functions in eukaryotes depend on the integration and coevolution of nuclear and organelle genomes, particularly within multi‐subunit enzyme complexes (Rand et al., 2004; Roux et al., 2016; Woodson & Chory, 2008).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Cytonuclear interplay in auto‐ and allopolyploids: a multifaceted perspective from the Festuca‐Lolium complex

Shahbazi,

Majka,

Kubíková

et al. 2024

The Plant Journal

View full text Add to dashboard Cite

SUMMARYRestoring cytonuclear stoichiometry is necessary after whole‐genome duplication (WGD) and interspecific/intergeneric hybridization in plants. We investigated this phenomenon in auto‐ and allopolyploids of the Festuca‐Lolium complex providing insights into the mechanisms governing cytonuclear interactions in early polyploid and hybrid generations. Our study examined the main processes potentially involved in restoring the cytonuclear balance after WGD comparing diploids and new and well‐established autopolyploids. We uncovered that both the number of chloroplasts and the number of chloroplast genome copies were significantly higher in the newly established autopolyploids and grew further in more established autopolyploids. The increase in the copy number of the chloroplast genome exceeded the rise in the number of chloroplasts and fully compensated for the doubling of the nuclear genome. In addition, changes in nuclear and organelle gene expression were insignificant. Allopolyploid Festuca × Lolium hybrids displayed potential structural conflicts in parental protein variants within the cytonuclear complexes. While biased maternal allele expression has been observed in numerous hybrids, our results suggest that its role in cytonuclear stabilization in the Festuca × Lolium hybrids is limited. This study provides insights into the restoration of the cytonuclear stoichiometry, yet it emphasizes the need for future research to explore post‐transcriptional regulation and its impact on cytonuclear gene expression stoichiometry. Our findings may enhance the understanding of polyploid plant evolution, with broader implications for the study of cytonuclear interactions in diverse biological contexts.

show abstract

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Cytonuclear interplay in auto‐ and allopolyploids: a multifaceted perspective from the Festuca‐Lolium complex

Shahbazi,

Majka,

Kubíková

et al. 2024

The Plant Journal

View full text Add to dashboard Cite

show abstract

“…The Balanophoraceae and Epipogium species exhibited intermediate degrees of aaRS and plastome gene loss, although the Balanophoraceae have lost all plastid tRNAs (Schelkunov et al , 2015, 2019; Chen et al , 2019; Serna-Sánchez et al , 2021; Yu et al , 2022). An increased plastome mutation rate caused by loss of DNA repair machinery (57, 58) in the Balanophoraceae may explain accelerated plastome (tRNA) gene losses relative to nuclear (aaRS) gene loss. Generally, loss of organellar aaRS correlates well with reduction of the plastome across heterotrophs.…”

Section: Discussionmentioning

confidence: 99%

“…S4). The (57,58) in the Balanophoraceae may explain accelerated plastome (tRNA) gene losses relative to nuclear (aaRS) gene loss. Generally, loss of organellar aaRS correlates well with reduction of the plastome across heterotrophs.…”

Section: Loss Of Photosynthesis Relaxes Constraints On Both Plastid A...mentioning

confidence: 99%

Photosynthesis drives retention of bacterial-like tRNA metabolism in plant organelles

DeTar,

Chustecki,

Martinez-Hottovy

et al. 2023

Preprint

Self Cite

View full text Add to dashboard Cite

Eukaryotic nuclear genomes often encode distinct sets of protein translation machinery for function in the cytosol vs. organelles (mitochondria and plastids). This phenomenon raises questions about why multiple translation systems are maintained even though they are capable of comparable functions, and whether they evolve differently depending on the compartment where they operate. These questions are particularly interesting in land plants because translation machinery, including aminoacyl-tRNA synthetases (aaRS), is often dual-targeted to both the plastids and mitochondria. These two organelles have quite different metabolisms, with much higher rates of translation in plastids to supply the abundant, rapid-turnover proteins required for photosynthesis. Previous studies have indicated that plant organellar aaRS evolve more slowly compared to mitochondrial aaRS in other eukaryotes that lack plastids. Thus, we investigated the evolution of nuclear-encoded organellar and cytosolic translation machinery across a broad sampling of angiosperms, including non-photosynthetic (heterotrophic) plant species with reduced rates of plastid gene expression to test the hypothesis that translational demands associated with photosynthesis constrain the evolution of bacterial-like enzymes involved in organellar tRNA metabolism. Remarkably, heterotrophic plants exhibited wholesale loss of many organelle-targeted aaRS and other enzymes, even though translation still occurs in their mitochondria and plastids. These losses were often accompanied by apparent retargeting of cytosolic enzymes and tRNAs to the organelles, sometimes preserving aaRS-tRNA charging relationships but other times creating surprising mismatches between cytosolic aaRS and mitochondrial tRNA substrates. Our findings indicate that the presence of a photosynthetic plastid drives the retention of specialized systems for organellar tRNA metabolism.

show abstract

“…The general principles of CmNR -environmental co-adaptation of organellar and nuclear genomes, replacement and/or co-editing of genes in both genomes for facilitated adaptation, and the importance of these co-adapted gene sets in reproductive isolation -apply to plants as well as animals. Mitonuclear coevolution is important in plants (Hanson & Bentolila, 2004;Havird et al, 2017) and, like mitochondria, the chloroplast has a reduced set of genes that complex intimately and co-evolve with nuclear genes (Ceriotti et al, 2022;Forsythe et al, 2021), influence adaptation to heat, drought, and other stressors (Song et al, 2021;Yoo et al, 2019), and contribute to reproductive isolation (Postel & Touzet, 2020;Sambatti et al, 2008).…”

Section: Elephas Maximus) Current Initiatives Aim To Selectively Edit...mentioning

confidence: 99%

Conservation Mitonuclear Replacement: Facilitated mitochondrial adaptation for a changing world

Iverson

2024

Evolutionary Applications

View full text Add to dashboard Cite

Most species will not be able to migrate fast enough to cope with climate change, nor evolve quickly enough with current levels of genetic variation. Exacerbating the problem are anthropogenic influences on adaptive potential, including the prevention of gene flow through habitat fragmentation and the erosion of genetic diversity in small, bottlenecked populations. Facilitated adaptation, or assisted evolution, offers a way to augment adaptive genetic variation via artificial selection, induced hybridization, or genetic engineering. One key source of genetic variation, particularly for climatic adaptation, are the core metabolic genes encoded by the mitochondrial genome. These genes influence environmental tolerance to heat, drought, and hypoxia, but must interact intimately and co‐evolve with a suite of important nuclear genes. These coadapted mitonuclear genes form some of the important reproductive barriers between species. Mitochondrial genomes can and do introgress between species in an adaptive manner, and they may co‐introgress with nuclear genes important for maintaining mitonuclear compatibility. Managers should consider the relevance of mitonuclear genetic variability in conservation decision‐making, including as a tool for facilitating adaptation. I propose a novel technique dubbed Conservation Mitonuclear Replacement (CmNR), which entails replacing the core metabolic machinery of a threatened species—the mitochondrial genome and key nuclear loci—with those from a closely related species or a divergent population, which may be better‐adapted to climatic changes or carry a lower genetic load. The most feasible route to CmNR is to combine CRISPR‐based nuclear genetic editing with mitochondrial replacement and assisted reproductive technologies. This method preserves much of an organism's phenotype and could allow populations to persist in the wild when no other suitable conservation options exist. The technique could be particularly important on mountaintops, where rising temperatures threaten an alarming number of species with almost certain extinction in the next century.

show abstract

Cytonuclear coevolution in a holoparasitic plant with highly disparate organellar genomes

Cited by 8 publications

References 95 publications

Cytonuclear interplay in auto‐ and allopolyploids: a multifaceted perspective from the Festuca‐Lolium complex

Cytonuclear interplay in auto‐ and allopolyploids: a multifaceted perspective from the Festuca‐Lolium complex

Photosynthesis drives retention of bacterial-like tRNA metabolism in plant organelles

Conservation Mitonuclear Replacement: Facilitated mitochondrial adaptation for a changing world

Contact Info

Product

Resources

About