Nuclear–Cytoplasmic Coevolution Analysis of RuBisCO in Synthesized Cucumis Allopolyploid

Zhai, Yufei; Yu, Xiaqing; Zhu, Zhanguo; Wang, Panqiao; Yang, Meng; Zhao, Qinzheng; Li, Ji; Chen, Jinfeng

doi:10.3390/genes10110869

Cited by 14 publications

(26 citation statements)

References 45 publications

(52 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…2020). Similar observations were made for synthetic allopolyploids from Cucumis (Zhai et al . 2019), rice (Wang et al .…”

Section: Introductionsupporting

confidence: 84%

“…The recently formed allotetraploid Tragopogon miscellus also exhibited maternal bias for cytonuclear related genes, but only for a subset of the naturally occurring T. miscellus individuals surveyed and none of the synthetic individuals (Sehrish et al 2015;Shan et al 2020). Similar observations were made for synthetic allopolyploids from Cucumis (Zhai et al 2019), rice (Wang et al 2017a), and in both the recent natural and newly synthesized forms of allopolyploid Brassica (Ferreira de Carvalho et al 2019), suggesting that cytonuclear coordination may not occur immediately in nascent polyploid species.…”

Section: Introductionsupporting

confidence: 56%

“…Smet et al 2013;Li et al 2016) and the expectation that any paternal cytonuclear homoeologs that exhibit deleterious interactions should evolve rapidly when not immediately lost(Rand et al 2004;Sloan et al 2014;Bock et al 2014). Evidence from homoploid hybrids(Turelli and Moyle 2007;Greiner et al 2011;Bock et al 2014) suggests that stabilizing cytonuclear interactions is key to establishing a successful lineage, and surveys of Rubisco in diverse plant lineages(Gong et al 2012(Gong et al , 2014 report differential homoeolog retention, biased expression, and asymmetric gene conversion favoring maternal homoeologs, although exceptions exist(Wang et al 2017a;Zhai et al 2019).…”

mentioning

confidence: 99%

See 2 more Smart Citations

Variation in cytonuclear expression accommodation among allopolyploid plants

Grover

Forsythe

Sharbrough

et al. 2022

Preprint

View full text Add to dashboard Cite

Cytonuclear coevolution is a common feature among plants, which coordinates gene expression and protein products between the nucleus and organelles. Consequently, lineage-specific differences may result in incompatibilities between the nucleus and cytoplasm in hybrid taxa. Allopolyploidy is also a common phenomenon in plant evolution. The hybrid nature of allopolyploids may result in cytonuclear incompatibilities, but the massive nuclear redundancy created during polyploidy affords additional avenues for resolving cytonuclear conflict (i.e., cytonuclear accommodation). Here we evaluate expression changes in organelle-targeted nuclear genes for six allopolyploid lineages that represent four genera (i.e., Arabidopsis, Arachis, Chenopodium, and Gossypium) and encompass a range in polyploid ages. Because incompatibilities between the nucleus and cytoplasm could potentially result in biases toward the maternal homoeolog and/or maternal expression level, we evaluate patterns of homoeolog usage, expression bias, and expression level dominance in cytonuclear genes relative to the background of non-cytonuclear expression changes and to the diploid parents. Although we find subsets of cytonuclear genes in most lineages that match our expectations of maternal preference, these observations are not consistent among either allopolyploids or categories of organelle-targeted genes. Our results indicate that cytonuclear expression accommodation may be a subtle and/or variable phenomenon that does not capture the full range of mechanisms by which allopolyploid plants resolve nuclear-cytoplasmic incompatibilities.

show abstract

“…2020). Similar observations were made for synthetic allopolyploids from Cucumis (Zhai et al . 2019), rice (Wang et al .…”

Section: Introductionsupporting

confidence: 84%

Section: Introductionsupporting

confidence: 56%

mentioning

confidence: 99%

See 1 more Smart Citation

Variation in cytonuclear expression accommodation among allopolyploid plants

Grover

Forsythe

Sharbrough

et al. 2022

Preprint

View full text Add to dashboard Cite

show abstract

“…At a more granular level, Gong et al (2012 , 2014) studied RuBisCO in allopolyploids of five different model genera, Arabidopsis, Arachis, Brassica, Gossypium , and Nicotiana , demonstrating that paternal copies of the nuclear-encoded small subunit ( rbcS ) experience gene conversion such that their sequences became maternal-like, and also that there was preferential expression of the maternal rbcS copies. These putative coevolutionary responses were not found, however, in some other genera, e.g., Tragopogon ( Sehrish et al, 2015 ) and Cucumis ( Zhai et al, 2019 ).…”

Section: Combinatorial Genomic and Expression-level Responsesmentioning

confidence: 77%

Genomics of Evolutionary Novelty in Hybrids and Polyploids

2020

View full text Add to dashboard Cite

It has long been recognized that hybridization and polyploidy are prominent processes in plant evolution. Although classically recognized as significant in speciation and adaptation, recognition of the importance of interspecific gene flow has dramatically increased during the genomics era, concomitant with an unending flood of empirical examples, with or without genome doubling. Interspecific gene flow is thus increasingly thought to lead to evolutionary innovation and diversification, via adaptive introgression, homoploid hybrid speciation and allopolyploid speciation. Less well understood, however, are the suite of genetic and genomic mechanisms set in motion by the merger of differentiated genomes, and the temporal scale over which recombinational complexity mediated by gene flow might be expressed and exposed to natural selection. We focus on these issues here, considering the types of molecular genetic and genomic processes that might be set in motion by the saltational event of genome merger between two diverged species, either with or without genome doubling, and how these various processes can contribute to novel phenotypes. Genetic mechanisms include the infusion of new alleles and the genesis of novel structural variation including translocations and inversions, homoeologous exchanges, transposable element mobilization and novel insertional effects, presence-absence variation and copy number variation. Polyploidy generates massive transcriptomic and regulatory alteration, presumably set in motion by disrupted stoichiometries of regulatory factors, small RNAs and other genome interactions that cascade from single-gene expression change up through entire networks of transformed regulatory modules. We highlight both these novel combinatorial possibilities and the range of temporal scales over which such complexity might be generated, and thus exposed to natural selection and drift.

show abstract

“…For example, Tragopogon miscellus exhibits maternally biased expression of rbcS , while its reciprocally formed congener Tragopogon mirus does not [58]. Synthetic allotetraploid rice showed little evidence of maternally biased expression of rbcS [59], and synthetic allopolyploid Cucumis x hytivus displayed paternally biased expression of rbcS [61]. Generalizing rules of cytonuclear biology from these handful of somewhat contradictory studies is made even more difficult because they have all only considered a single cytonuclear complex.…”

Section: Introductionmentioning

confidence: 99%

Global patterns of subgenome evolution in organelle-targeted genes of six allotetraploid angiosperms

Sharbrough

Conover

Gyorfy

et al. 2021

Preprint

View full text Add to dashboard Cite

Whole-genome duplications (WGDs), in which the number of nuclear genome copies is elevated as a result of autopolyploidy or allopolyploidy, are a prominent process of diversification in eukaryotes. The genetic and evolutionary forces that WGD imposes upon cytoplasmic genomes are not well understood, despite the central role that cytonuclear interactions play in eukaryotic function and fitness. Cellular respiration and photosynthesis depend upon successful interaction between the 3000+ nuclear-encoded proteins destined for the mitochondria or plastids and the gene products of cytoplasmic genomes in multi-subunit complexes such as OXPHOS, organellar ribosomes, Photosystems I and II, and Rubisco. Allopolyploids are thus faced with the critical task of coordinating interactions between nuclear and cytoplasmic genes that were inherited from different species. Because cytoplasmic genomes share a more recent history of common descent with the maternal nuclear subgenome than the paternal subgenome, evolutionary “mismatches” between the paternal subgenome and the cytoplasmic genomes in allopolyploids might lead to accelerated rates of evolution in the paternal homoeologs of allopolyploids, either through relaxed purifying selection or strong directional selection to rectify these mismatches. We tested this hypothesis in maternal vs. paternal copies of organelle-targeted genes in six allotetraploids: Brachypodium hybridum, Chenopodium quinoa, Coffea arabica, Gossypium hirsutum, Nicotiana tabacum, and Triticum dicoccoides. We report evidence that allopolyploid subgenomes exhibit unequal rates of protein-sequence evolution, but we did not observe global effects of cytonuclear incompatibilities on paternal homoeologs of organelle-targeted genes. Analyses of gene content revealed mixed evidence for whether organelle-targeted genes re-diploidize more rapidly than non-organelle-targeted genes. Together, these global analyses provide insights into the complex evolutionary dynamics of allopolyploids, showing that allopolyploid subgenomes have separate evolutionary trajectories despite sharing the same nucleus, generation time, and ecological context.AUTHOR SUMMARYWhole genome duplication, in which the size and content of the nuclear genome is instantly doubled, represents one of the most profound forms of mutational change. The consequences of duplication events are equally monumental, especially considering that almost all eukaryotes have undergone whole genome duplications during their evolutionary history. While myriad genetic, cellular, organismal, and ecological effects of whole genome duplications have been extensively documented, relatively little attention has been paid to the diminutive but essential “other” genomes present inside the cell, those of chloroplasts and mitochondria. In this study, we compared the evolutionary patterns of >340,000 genes from 23 species to test whether whole genome duplications are associated with genetic mismatches between the nuclear, mitochondrial, and chloroplast genomes. We discovered tremendous differences between duplicated copies of nuclear genomes; however, mitochondria-nuclear and chloroplast-nuclear mismatches do not appear to be common following whole genome duplications. Together these genomic data represent the most extensive analysis yet performed on how polyploids maintain the delicate and finely tuned balance between the nuclear, mitochondrial, and chloroplast genomes.

show abstract

Nuclear–Cytoplasmic Coevolution Analysis of RuBisCO in Synthesized Cucumis Allopolyploid

Cited by 14 publications

References 45 publications

Variation in cytonuclear expression accommodation among allopolyploid plants

Variation in cytonuclear expression accommodation among allopolyploid plants

Genomics of Evolutionary Novelty in Hybrids and Polyploids

Global patterns of subgenome evolution in organelle-targeted genes of six allotetraploid angiosperms

Contact Info

Product

Resources

About