Insight into the Recent Genome Duplication of the Halophilic Yeast Hortaea werneckii: Combining an Improved Genome with Gene Expression and Chromatin Structure

Abstract Extremophilic organisms demonstrate the flexibility and adaptability of basic biological processes by highlighting how cell physiology adapts to environmental extremes. Few eukaryotic extremophiles have been well studied and only a small number are amenable to laboratory cultivation and manipulation. A detailed characterization of the genome architecture of such organisms is important to illuminate how they adapt to environmental stresses. One excellent example of a fungal extremophile is the halophile Hortaea werneckii (Pezizomycotina, Dothideomycetes, Capnodiales), a yeast-like fungus able to thrive at near-saturating concentrations of sodium chloride and which is also tolerant to both UV irradiation and desiccation. Given its unique lifestyle and its remarkably recent whole genome duplication, H. werneckii provides opportunities for testing the role of genome duplications and adaptability to extreme environments. We previously assembled the genome of H. werneckii using short-read sequencing technology and found a remarkable degree of gene duplication. Technology limitations, however, precluded high-confidence annotation of the entire genome. We therefore revisited the H. wernickii genome using long-read, single-molecule sequencing and provide an improved genome assembly which, combined with transcriptome and nucleosome analysis, provides a useful resource for fungal halophile genomics. Remarkably, the ∼50 Mb H. wernickii genome contains 15,974 genes of which 95% (7608) are duplicates formed by a recent whole genome duplication (WGD), with an average of 5% protein sequence divergence between them. We found that the WGD is extraordinarily recent, and compared to Saccharomyces cerevisiae, the majority of the genome’s ohnologs have not diverged at the level of gene expression of chromatin structure.

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A high‐quality walnut genome assembly reveals extensive gene expression divergences after whole‐genome duplication

Plant Biotechnology Journal ◽

10.1111/pbi.13350 ◽

2020 ◽

Vol 18 (9) ◽

pp. 1848-1850 ◽

Cited By ~ 2

Author(s):

Junpei Zhang ◽

Wenting Zhang ◽

Feiyang Ji ◽

Jie Qiu ◽

Xiaobo Song ◽

...

Keyword(s):

Gene Expression ◽

Genome Assembly ◽

Whole Genome Duplication ◽

Genome Duplication ◽

Whole Genome ◽

High Quality

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Diversified regulation of circadian clock gene expression following whole genome duplication

PLoS Genetics ◽

10.1371/journal.pgen.1009097 ◽

2020 ◽

Vol 16 (10) ◽

pp. e1009097

Author(s):

Alexander C. West ◽

Marianne Iversen ◽

Even H. Jørgensen ◽

Simen R. Sandve ◽

David G. Hazlerigg ◽

...

Keyword(s):

Gene Expression ◽

Circadian Clock ◽

Whole Genome Duplication ◽

Clock Gene ◽

Genome Duplication ◽

Whole Genome ◽

Circadian Clock Gene ◽

Clock Gene Expression

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Effects of whole genome duplication on cell size and gene expression in mouse embryonic stem cells

Journal of Reproduction and Development ◽

10.1262/jrd.2016-037 ◽

2016 ◽

Vol 62 (6) ◽

pp. 571-576 ◽

Cited By ~ 5

Author(s):

Hiroyuki IMAI ◽

Wataru FUJII ◽

Ken Takeshi KUSAKABE ◽

Yasuo KISO ◽

Kiyoshi KANO

Keyword(s):

Gene Expression ◽

Stem Cells ◽

Embryonic Stem Cells ◽

Cell Size ◽

Whole Genome Duplication ◽

Genome Duplication ◽

Embryonic Stem ◽

Mouse Embryonic Stem Cells ◽

Whole Genome

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Evolution of gene expression after whole-genome duplication: New insights from the spotted gar genome

Journal of Experimental Zoology Part B Molecular and Developmental Evolution ◽

10.1002/jez.b.22770 ◽

2017 ◽

Vol 328 (7) ◽

pp. 709-721 ◽

Cited By ~ 30

Author(s):

Jeremy Pasquier ◽

Ingo Braasch ◽

Peter Batzel ◽

Cedric Cabau ◽

Jérome Montfort ◽

...

Keyword(s):

Gene Expression ◽

Whole Genome Duplication ◽

Genome Duplication ◽

Whole Genome ◽

Spotted Gar

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Genomic novelty and process-level convergence in adaptation to whole genome duplication

10.1101/2020.01.31.929109 ◽

2020 ◽

Cited By ~ 1

Author(s):

Magdalena Bohutínská ◽

Mark Alston ◽

Patrick Monnahan ◽

Terezie Mandáková ◽

Sian Bray ◽

...

Keyword(s):

Cell Cycle ◽

Whole Genome Duplication ◽

Genome Duplication ◽

Cell Physiology ◽

Whole Genome ◽

Sudden Increase ◽

A Genome ◽

Arabidopsis Arenosa ◽

Process Level ◽

Insight Into

AbstractWhole genome duplication (WGD) occurs across kingdoms and can promote adaptation. However, a sudden increase in chromosome number, as well as changes in physiology, are traumatic to conserved processes. Previous work in Arabidopsis arenosa revealed a coordinated genomic response to WGD, involving physically interacting meiosis proteins, as well as changes related to cell cycle and ion homeostasis. Here we ask: is this coordinated shift in the same processes repeated in another species following WGD? To answer this, we resequenced and cytologically assessed replicated populations from a diploid/autotetraploid system, Cardamine amara, and test the hypothesis that gene and process-level convergence will be prevalent between these two WGDs adaptation events. Interestingly, we find that gene-level convergence is negligible, with no more in common than would be expected by chance. This was most clear at meiosis-related genes, consistent with our cytological assessment of somewhat lower meiotic stability in C. amara, despite establishment and broad occurrence of the autotetraploid in nature. In contrast, obvious convergence at the level of functional processes, including meiotic cell cycle, chromosome organisation and stress signalling was evident. This indicates that the two autotetraploids survived challenges attendant to WGD via contrasting solutions, modifying different players from similar processes. Overall, this work gives the first insight into the salient adaptations required to cope with a genome-doubled state and brings the first genomic evidence that autopolyploids can utilize multiple trajectories to achieve adaptation to WGD. We speculate that this flexibility increases the likelihood a nascent polyploid overcomes early stringent challenges to later access the spectrum of evolutionary opportunities of polyploidy.Significance statementWhole genome duplication (WGD) is a tremendous mutation and an important evolutionary force. It also presents immediate changes to meiosis and cell physiology that nascent polyploids must overcome to survive. Given the dual facts that WGD adaptation is difficult, but many lineages nevertheless survive WGD, we ask: how constrained are the evolutionary responses to a genome-doubled state? We previously identified candidate genes for WGD adaptation in Arabidopsis arenosa, which has natural diploid and tetraploid variants. Here we test for evolutionary convergence in adaptation to WGD in a species 17 million years distant, Cardamine amara. This work gives the first genomic insight into of how autopolyploids utilize multiple adaptive trajectories to manage a genome-doubled state.

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Bioinformatic analysis of chromatin organization and biased expression of duplicated genes between two poplars with a common whole-genome duplication

Horticulture Research ◽

10.1038/s41438-021-00494-2 ◽

2021 ◽

Vol 8 (1) ◽

Author(s):

Le Zhang ◽

Jingtian Zhao ◽

Hao Bi ◽

Xiangyu Yang ◽

Zhiyang Zhang ◽

...

Keyword(s):

Gene Expression ◽

Whole Genome Duplication ◽

Genome Duplication ◽

Expression Patterns ◽

Regulation Of Gene Expression ◽

Populus Euphratica ◽

Epigenetic Modifications ◽

Chromatin Organization ◽

Whole Genome ◽

Duplicated Genes

AbstractThe nonrandom three-dimensional organization of chromatin plays an important role in the regulation of gene expression. However, it remains unclear whether this organization is conserved and whether it is involved in regulating gene expression during speciation after whole-genome duplication (WGD) in plants. In this study, high-resolution interaction maps were generated using high-throughput chromatin conformation capture (Hi-C) techniques for two poplar species, Populus euphratica and Populus alba var. pyramidalis, which diverged ~14 Mya after a common WGD. We examined the similarities and differences in the hierarchical chromatin organization between the two species, including A/B compartment regions and topologically associating domains (TADs), as well as in their DNA methylation and gene expression patterns. We found that chromatin status was strongly associated with epigenetic modifications and gene transcriptional activity, yet the conservation of hierarchical chromatin organization across the two species was low. The divergence of gene expression between WGD-derived paralogs was associated with the strength of chromatin interactions, and colocalized paralogs exhibited strong similarities in epigenetic modifications and expression levels. Thus, the spatial localization of duplicated genes is highly correlated with biased expression during the diploidization process. This study provides new insights into the evolution of chromatin organization and transcriptional regulation during the speciation process of poplars after WGD.

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Diversified regulation of circadian clock gene expression following whole genome duplication

10.1101/2020.03.22.002162 ◽

2020 ◽

Author(s):

Alexander C. West ◽

Marianne Iversen ◽

Even H. Jørgensen ◽

Simen R. Sandve ◽

David G. Hazlerigg ◽

...

Keyword(s):

Gene Expression ◽

Whole Genome Duplication ◽

Clock Gene ◽

Genome Duplication ◽

Clock Genes ◽

Expression Patterns ◽

Whole Genome ◽

Functional Diversification ◽

Clock Gene Expression ◽

Multiple Copies

AbstractAcross taxa, circadian control of physiology and behavior arises from cell-autonomous oscillations in gene expression, governed by a networks of so-called ‘clock genes’, collectively forming transcription-translation feedback loops. In modern vertebrates, these networks contain multiple copies of clock gene family members, which arose through whole genome duplication (WGD) events during evolutionary history. It remains unclear to what extent multiple copies of clock gene family members are functionally redundant or have allowed for functional diversification. We addressed this problem through an analysis of clock gene expression in the Atlantic salmon, a representative of the salmonids, a group which has undergone at least 4 rounds of WGD since the base of the vertebrate lineage, giving an unusually large complement of clock genes. By comparing expression patterns across multiple tissues, and during development, we present evidence for gene- and tissue-specific divergence in expression patterns, consistent with functional diversification of clock gene duplicates. In contrast to mammals, we found no evidence for coupling between cortisol and circadian gene expression, but cortisol mediated non-circadian regulated expression of a subset of clock genes in the salmon gill was evident. This regulation is linked to changes in gill function necessary for the transition from fresh- to sea-water in anadromous fish. Overall, this analysis emphasises the potential for a richly diversified clock gene network to serve a mixture of circadian and non-circadian functions in vertebrate groups with complex genomes.Author SummaryThe generation of daily (circadian) rhythms in behaviour and physiology depends on the activities of networks of so-called clock genes. In vertebrates, these have become highly complex due to a process known as whole genome duplication, which has occurred repeatedly during evolutionary history, giving rise to additional copies of key elements of the clock gene network. It remains unclear whether this results in functional redundancy, or whether it has permitted new roles for clock genes to emerge. Here, based on studies in the Atlantic salmon, a species with an unusually large complement of clock genes, we present evidence in favour of the latter scenario. We observe marked tissue-specific, and developmentally-dependent differences in the expression patterns of duplicated copies of key clock genes, and we identify a subset of clock genes whose expression is associated with the physiological preparation to migrate to sea, but is independent of circadian regulation. Associated with this, cortisol secretion is uncoupled from circadian organisation, contrasting with the situation in mammals. Our results indicate that whole genome duplication has permitted clock genes to diversify into non-circadian functions, and raise interesting questions about the ubiquity of mammal-like coupling between circadian and endocrine function.

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