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Cytonuclear Interactions in Polyploid Species
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Cytonuclear Interactions in Polyploid Species

A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Population and Evolutionary Genetics and Genomics".

Deadline for manuscript submissions: closed (31 December 2019) | Viewed by 10630

Special Issue Editors

Prof. France Dufresne

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Guest Editor
Universite du Quebec a Rimouski, Department of Biology, Rimouski, QC G5L 3A1, Canada
Interests: evolutionary biology; genetics; model organisms; poliploidy; allopolyploidy; cytonuclear interactions
Dr. Jennifer Tate

E-Mail Website
Guest Editor
Institute of Fundamental Sciences, Massey University, Palmerston North 4442, New Zealand
Interests: plant speciation; molecular phylogenetics; hybridization; polyploidy; whole genome duplication
Dr. Daniel Sloan

E-Mail Website
Guest Editor
Department of Biology, Colorado State University, Fort Collins, CO 80523, USA
Interests: molecular evolution and genomics; biological diversity; genome evolution; plant systems; DNA sequencing

Special Issue Information

Dear Colleagues,

Polyploidy is widespread in plants and less frequent in animals but serves as an important speciation mechanism in both groups. Polyploidy is accompanied by drastic changes in genome organization including differential patterns of gene loss, gene silencing, genome-wide expression dominance, and epigenetic reprogramming. One underexplored dimension of polyploid evolution is cytonuclear interactions. Allopolyploid animals must ensure coordination between the effectively haploid and typically uniparentally inherited mitochondrial genome and the duplicated biparentally inherited nuclear genome. In allopolyploid plants, an additional cytoplasmic genome (the plastome) must interact with the duplicated nuclear genome. Whole genome duplication may lead to a stochiometric imbalance between these interacting genomes and perturb the assembly of enzyme complexes and the proper functioning of mitochondria and chloroplasts. Recent studies have shown compensatory mechanisms in young plant polyploids with organelle-targeting nuclear genes returning to a single copy following polyploidization. In animals, the mitochondrial genome is typically inherited maternally and numerous cases of hybrid breakdown and incompatibilities have been traced to the disruption of cytonuclear coordination in diploids. However, not much is known about how doubling the nuclear genome perturbs interactions with the mitochondrial genome in polyploid animals or plants. As polyploidy allows new interactions between highly divergent cytoplasmic and nuclear genomes, cytonuclear interactions may be more challenging in allopolyploids than in diploid hybrids.

This Special Issue aims to explore and contrast coordination and coevolution between cytoplasmic and nuclear genomes in both plant and animal polyploids.

Prof. France Dufresne
Dr. Jennifer Tate
Dr. Daniel Sloan
Guest Editors

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Keywords

  • polyploidy
  • evolution
  • allopolyploidy
  • cytonuclear interactions
  • mitochondria
  • stoichiometry
  • dosage compensation
  • genome organization
  • animal models
  • plant models

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Published Papers (3 papers)

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Research

10 pages, 1993 KiB  
Article
Repetitive DNA Restructuring Across Multiple Nicotiana Allopolyploidisation Events Shows a Lack of Strong Cytoplasmic Bias in Influencing Repeat Turnover
by Steven Dodsworth, Maïté S. Guignard, Oscar A. Pérez-Escobar, Monika Struebig, Mark W. Chase and Andrew R. Leitch
Genes 2020, 11(2), 216; https://doi.org/10.3390/genes11020216 - 19 Feb 2020
Cited by 5 | Viewed by 3118
Abstract
Allopolyploidy is acknowledged as an important force in plant evolution. Frequent allopolyploidy in Nicotiana across different timescales permits the evaluation of genome restructuring and repeat dynamics through time. Here we use a clustering approach on high-throughput sequence reads to identify the main classes [...] Read more.
Allopolyploidy is acknowledged as an important force in plant evolution. Frequent allopolyploidy in Nicotiana across different timescales permits the evaluation of genome restructuring and repeat dynamics through time. Here we use a clustering approach on high-throughput sequence reads to identify the main classes of repetitive elements following three allotetraploid events, and how these are inherited from the closest extant relatives of the maternal and paternal subgenome donors. In all three cases, there was a lack of clear maternal, cytoplasmic bias in repeat evolution, i.e., lack of a predicted bias towards maternal subgenome-derived repeats, with roughly equal contributions from both parental subgenomes. Different overall repeat dynamics were found across timescales of <0.5 (N. rustica L.), 4 (N. repanda Willd.) and 6 (N. benthamiana Domin) Ma, with nearly additive, genome upsizing, and genome downsizing, respectively. Lower copy repeats were inherited in similar abundance to the parental subgenomes, whereas higher copy repeats contributed the most to genome size change in N. repanda and N. benthamiana. Genome downsizing post-polyploidisation may be a general long-term trend across angiosperms, but at more recent timescales there is species-specific variance as found in Nicotiana. Full article
(This article belongs to the Special Issue Cytonuclear Interactions in Polyploid Species)
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19 pages, 3894 KiB  
Article
Robust Cytonuclear Coordination of Transcription in Nascent Arabidopsis thaliana Autopolyploids
by Jeremy E. Coate, W. Max Schreyer, David Kum and Jeff J. Doyle
Genes 2020, 11(2), 134; https://doi.org/10.3390/genes11020134 - 28 Jan 2020
Cited by 14 | Viewed by 3759
Abstract
Polyploidy is hypothesized to cause dosage imbalances between the nucleus and the other genome-containing organelles (mitochondria and plastids), but the evidence for this is limited. We performed RNA-seq on Arabidopsis thaliana diploids and their derived autopolyploids to quantify the degree of inter-genome coordination [...] Read more.
Polyploidy is hypothesized to cause dosage imbalances between the nucleus and the other genome-containing organelles (mitochondria and plastids), but the evidence for this is limited. We performed RNA-seq on Arabidopsis thaliana diploids and their derived autopolyploids to quantify the degree of inter-genome coordination of transcriptional responses to nuclear whole genome duplication in two different organs (sepals and rosette leaves). We show that nuclear and organellar genomes exhibit highly coordinated responses in both organs. First, organelle genome copy number increased in response to nuclear whole genome duplication (WGD), at least partially compensating for altered nuclear genome dosage. Second, transcriptional output of the different cellular compartments is tuned to maintain diploid-like levels of relative expression among interacting genes. In particular, plastid genes and nuclear genes whose products are plastid-targeted show coordinated down-regulation, such that their expression levels relative to each other remain constant across ploidy levels. Conversely, mitochondrial genes and nuclear genes with mitochondrial targeting show either constant or coordinated up-regulation of expression relative to other nuclear genes. Thus, cytonuclear coordination is robust to changes in nuclear ploidy level, with diploid-like balance in transcript abundances achieved within three generations after nuclear whole genome duplication. Full article
(This article belongs to the Special Issue Cytonuclear Interactions in Polyploid Species)
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11 pages, 3502 KiB  
Article
Nuclear–Cytoplasmic Coevolution Analysis of RuBisCO in Synthesized Cucumis Allopolyploid
by Yufei Zhai, Xiaqing Yu, Zaobing Zhu, Panqiao Wang, Ya Meng, Qinzheng Zhao, Ji Li and Jinfeng Chen
Genes 2019, 10(11), 869; https://doi.org/10.3390/genes10110869 - 30 Oct 2019
Cited by 10 | Viewed by 2991
Abstract
Allopolyploids are often faced with the challenge of maintaining well-coordination between nuclear and cytoplasmic genes inherited from different species. The synthetic allotetraploid Cucumis × hytivus is a useful model to explore cytonuclear coevolution. In this study, the sequences and expression of cytonuclear enzyme [...] Read more.
Allopolyploids are often faced with the challenge of maintaining well-coordination between nuclear and cytoplasmic genes inherited from different species. The synthetic allotetraploid Cucumis × hytivus is a useful model to explore cytonuclear coevolution. In this study, the sequences and expression of cytonuclear enzyme complex RuBisCO as well as its content and activity in C. × hytivus were compared to its parents to explore plastid–nuclear coevolution. The plastome-coded rbcL gene sequence was confirmed to be stable maternal inheritance, and parental copy of nuclear rbcS genes were both preserved in C. × hytivus. Thus, the maternal plastid may interact with the biparentally inherited rbcS alleles. The expression of the rbcS gene of C-homoeologs (paternal) was significantly higher than that of H-homoeologs (maternal) in C. × hytivus (HHCC). Protein interaction prediction analysis showed that the rbcL protein has stronger binding affinity to the paternal copy of rbcS protein than that of maternal copy in C. × hytivus, which might explain the transcriptional bias of the rbcS homoeologs. Moreover, both the activity and content of RuBisCO in C. × hytivus showed mid-parent heterosis. In summary, our results indicate a paternal transcriptional bias of the rbcS genes in C. × hytivus, and we found new nuclear–cytoplasmic combination may be one of the reasons for allopolyploids heterosis. Full article
(This article belongs to the Special Issue Cytonuclear Interactions in Polyploid Species)
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