Asymmetric genome merging leads to gene expression novelty through nucleo-cytoplasmic disruptions and transcriptomic shock inChlamydomonastriploids DOI Creative Commons
Lucas Prost‐Boxoen, Quinten Bafort, Antoine Van de Vloet

et al.

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: Aug. 8, 2024

Abstract Genome merging is a common phenomenon in many organisms, causing wide range of consequences on phenotype, adaptation, and gene expression, among other effects, yet its broader implications are not well understood. Two genome expression remain poorly understood: dosage effects evolution expression. In this study, we employed Chlamydomonas reinhardtii as model to investigate the asymmetric by crossing diploid with haploid strain create novel triploid line. Five independent clonal lineages derived from line were evolved for 425 asexual generations laboratory natural selection (LNS) experiment. Utilizing fitness assays, qPCR, RNA-Seq, assessed immediate subsequent over time. Our findings reveal substantial alterations protein homeostasis (proteostasis) cytonuclear stoichiometry. Notably, exhibited level dominance transgressivity ( i.e. , higher or lower than either parent). Ongoing pattern “functional dominance” parent was observed, alongside remarkable stability patterns across generations. Despite major nucleo-cytoplasmic disruptions, enhanced detected strain. By comparing generations, our results indicate that proteostasis restoration critical component rapid adaptation following possibly systems.

Language: Английский

Organellar transcripts dominate the cellular mRNA pool across plants of varying ploidy levels DOI Creative Commons
Evan S. Forsythe, Corrinne E. Grover, Emma R. Miller

et al.

Proceedings of the National Academy of Sciences, Journal Year: 2022, Volume and Issue: 119(30)

Published: July 19, 2022

Mitochondrial and plastid functions depend on coordinated expression of proteins encoded by genomic compartments that have radical differences in copy number organellar nuclear genomes. In polyploids, doubling the genome may add challenges to maintaining balanced involved cytonuclear interactions. Here, we use ribo-depleted RNA sequencing (RNA-seq) analyze transcript abundance for genomes leaf tissue from four different polyploid angiosperms their close diploid relatives. We find even though contain <1% genes genome, they generate majority (69.9 82.3%) messenger (mRNA) transcripts cell. are responsible a much smaller percentage (1.3 3.7%) mRNA pool but still produce higher abundances per gene compared genome. Nuclear encoding functionally interact with mitochondrial or products exhibit levels consistently more than 10-fold lower counterparts, indicating an extreme imbalance at level despite predominance equimolar interactions protein level. Nevertheless, interacting show strongly correlated across functional categories, suggesting observed stoichiometric does not preclude coordination expression. Finally, alter ratios relatives consistent systematic ways, successful plants able compensate perturbations associated doubling.

Language: Английский

Citations

31
Cytonuclear interplay in auto‐ and allopolyploids: a multifaceted perspective from the Festuca‐Lolium complex DOI Creative Commons
Mehrdad Shahbazi, Joanna Majka,

Denisa Kubíková

et al.

The Plant Journal, Journal Year: 2024, Volume and Issue: 118(4), P. 1102 - 1118

Published: Feb. 7, 2024

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

Language: Английский

Citations

6
Polyploid plants take cytonuclear perturbations in stride DOI Creative Commons
Daniel B. Sloan, Justin L. Conover, Corrinne E. Grover

et al.

The Plant Cell, Journal Year: 2024, Volume and Issue: 36(4), P. 829 - 839

Published: Jan. 24, 2024

Hybridization in plants is often accompanied by nuclear genome doubling (allopolyploidy), which has been hypothesized to perturb interactions between and organellar (mitochondrial plastid) genomes creating imbalances the relative copy number of these producing genetic incompatibilities maternally derived half allopolyploid from paternal progenitor. Several evolutionary responses have predicted ameliorate effects, including selection for changes protein sequences that restore cytonuclear interactions; biased gene retention/expression/conversion favoring maternal copies; fine-tuning numbers expression levels. Numerous recent studies, however, found are inconsistent rarely scale genome-wide generalities. The apparent robustness plant allopolyploidy may reflect features general allopolyploids such as lack F2 hybrid breakdown under disomic inheritance, others more plant-specific, slow sequence divergence preexisting regulatory cell size endopolyploidy during development. Thus, only act main barrier establishment lineages, perhaps helping explain why so pervasive evolution.

Language: Английский

Citations

5
Cell type–specific cytonuclear coevolution in three allopolyploid plant species DOI Creative Commons
Keren Zhang, Xueru Zhao, Yue Zhao

et al.

Proceedings of the National Academy of Sciences, Journal Year: 2023, Volume and Issue: 120(40)

Published: Sept. 25, 2023

Cytonuclear disruption may accompany allopolyploid evolution as a consequence of the merger different nuclear genomes in cellular environment having only one set progenitor organellar genomes. One path to reconcile potential cytonuclear mismatch is biased expression for maternal gene duplicates (homoeologs) encoding proteins that target plastids and/or mitochondria. Assessment this transcriptional form coevolution at level individual cells or cell types remains unexplored. Using single-cell (sc-) and single-nucleus (sn-) RNAseq data from eight tissues three species, we characterized type–specific variations coevolutionary homoeologous demonstrated temporal dynamics patterns across development stages during cotton fiber development. Our results provide unique insights into plant allopolyploids level.

Language: Английский

Citations

4
Asymmetric genome merging leads to gene expression novelty through nucleo‐cytoplasmic disruptions and transcriptomic shock in Chlamydomonas triploids DOI
Lucas Prost‐Boxoen, Quinten Bafort, Antoine Van de Vloet

et al.

New Phytologist, Journal Year: 2024, Volume and Issue: unknown

Published: Nov. 5, 2024

Summary Genome merging is a common phenomenon causing wide range of consequences on phenotype, adaptation, and gene expression, yet its broader implications are not well‐understood. Two genome expression remain particularly poorly understood: dosage effects evolution expression. We employed Chlamydomonas reinhardtii as model to investigate the asymmetric by crossing diploid with haploid strain create novel triploid line. Five independent clonal lineages derived from this line were evolved for 425 asexual generations in laboratory natural selection experiment. Utilizing fitness assays, flow cytometry, RNA‐Seq, we assessed immediate subsequent evolution. Our findings reveal substantial alterations size, protein homeostasis, cytonuclear stoichiometry. Gene exhibited expression‐level dominance transgressivity (i.e. level higher or lower than either parent). Ongoing pattern ‘functional dominance’ parent was observed. Despite major genomic nucleo‐cytoplasmic disruptions, enhanced detected strain. By comparing across generations, our results indicate that proteostasis restoration critical component rapid adaptation following possibly other systems.

Language: Английский

Citations

1
Nucleus-cytoplasm compatibility: A genetic system underlying allopolyploid speciation as exemplified in alloplasmic lines of wheat DOI Creative Commons
Chiharu Nakamura

CYTOLOGIA, Journal Year: 2023, Volume and Issue: 88(3), P. 189 - 195

Published: Sept. 24, 2023

In the tribe Triticeae, systematic studies using alloplasmic lines have greatly facilitated our understanding of cytoplasmic genome inheritance, its structural and functional diversity, interaction with nuclear genomes. Effective utilization these valuable experimental tools produced by combining given genomes from various related species has provided ample evidence supporting presence roles a genetic system controlling nucleus-cytoplasm compatibility operating particularly in lineages allopolyploid speciation. This review focused on current state knowledge system. It also emphasized necessity for further research toward more precise identification complex regulatory mechanism possible practical application agriculture.

Language: Английский

Citations

3
Compensatory Genetic and Transcriptional Cytonuclear Coordination in Allopolyploid Lager Yeast (Saccharomyces pastorianus) DOI Creative Commons
Keren Zhang, Juzuo Li, Li Guo

et al.

Molecular Biology and Evolution, Journal Year: 2022, Volume and Issue: 39(11)

Published: Oct. 19, 2022

Abstract Cytonuclear coordination between biparental-nuclear genomes and uniparental-cytoplasmic organellar in plants is often resolved by genetic transcriptional cytonuclear responses. Whether this mechanism also acts allopolyploid members of other kingdoms not clear. Additionally, interleaved cells/individuals within the same population underexplored. The yeast Saccharomyces pastorianus provides opportunity to explore coevolution during different growth stages from novel dimensions. Using S. cells multiple environment, we show that nuclear mitochondria-targeted genes have undergone both asymmetric gene conversion stage-specific biased expression favoring mitochondrial genome donor (Saccharomyces eubayanus). Our results suggest lager species entails an orchestrated compensatory evolutionary regulatory shift. common as well unique properties underlying allopolyploidy unicellular yeasts higher offers insights into mechanisms evolution associated with speciation.

Language: Английский

Citations

3
Asymmetric genome merging leads to gene expression novelty through nucleo-cytoplasmic disruptions and transcriptomic shock inChlamydomonastriploids DOI Creative Commons
Lucas Prost‐Boxoen, Quinten Bafort, Antoine Van de Vloet

et al.

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: Aug. 8, 2024

Abstract Genome merging is a common phenomenon in many organisms, causing wide range of consequences on phenotype, adaptation, and gene expression, among other effects, yet its broader implications are not well understood. Two genome expression remain poorly understood: dosage effects evolution expression. In this study, we employed Chlamydomonas reinhardtii as model to investigate the asymmetric by crossing diploid with haploid strain create novel triploid line. Five independent clonal lineages derived from line were evolved for 425 asexual generations laboratory natural selection (LNS) experiment. Utilizing fitness assays, qPCR, RNA-Seq, assessed immediate subsequent over time. Our findings reveal substantial alterations protein homeostasis (proteostasis) cytonuclear stoichiometry. Notably, exhibited level dominance transgressivity ( i.e. , higher or lower than either parent). Ongoing pattern “functional dominance” parent was observed, alongside remarkable stability patterns across generations. Despite major nucleo-cytoplasmic disruptions, enhanced detected strain. By comparing generations, our results indicate that proteostasis restoration critical component rapid adaptation following possibly systems.

Language: Английский

Citations

0