Recurrent allopolyploidization events diversify eco-physiological traits in marsh orchids

AbstractWhole-genome duplication, in particular allopolyploidy, has shaped the evolution of angiosperms and other organisms. Structural reorganization of chromosomes and repatterning of gene expression is frequently observed in early generation allopolyploids, with potential ecological consequences. The relative contributions of environmental and intrinsic drivers to these changes are unknown. We show here that in marsh orchids (Dactylorhiza, Orchidaceae), recurrently-formed allopolyploids are characterized by distinct eco-physiologies matching their respective environments, providing us with an excellent study system to address this question. Here we integrate eco-physiological and transcriptomic comparative studies to reveal a complex suite of intertwined, pronounced differences between sibling allopolyploids. We show that Dactylorhiza majalis that is distributed in Central and Southern Europe favors meadows with mesic soils. Its sibling allopolyploid D. traunsteineri occurs in fens, characterized by soils depleted by macro- and micronutrients, mainly in previously glaciated European areas. We further uncover distinct features in their nutrient transport, leaf elemental chemistry, light-harvesting, photoprotection, and stomata activity, that appear all linked to their distinct ecologies, in particular soil chemistry differences at their native sites. Recurrent polyploidization hence enriches biodiversity through eco-physiological diversification, providing the opportunity for sibling allopolyploids to evolve as distinct evolutionary units, despite pervasive interspecific gene flow.Significance StatementWhole-genome duplication resulting in polyploidy has underpinned the evolution of flowering plants and other organisms, and is important for many crops. However, the ecological implications of polyploidy remain little understood. Here, we demonstrate that two sibling allopolyploid marsh orchid species prefer distinct habitats, and have evolved a suite of distinctive ecophysiological characters (e.g. nutrient transport, energy harvesting and photoprotection). We argue that the divergence of these characters in the nascent polyploids drove adaptation into distinct ecological niches (low nutrient fens versus meadows with mesic soils), generating ecological barriers that maintains distinct, independent lineages, even in the presence of interspecific gene flow.

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Interspecific introgression mediates adaptation to whole genome duplication

Nature Communications ◽

10.1038/s41467-019-13159-5 ◽

2019 ◽

Vol 10 (1) ◽

Cited By ~ 12

Author(s):

Sarah Marburger ◽

Patrick Monnahan ◽

Paul J. Seear ◽

Simon H. Martin ◽

Jordan Koch ◽

...

Keyword(s):

Gene Flow ◽

Opposite Direction ◽

Whole Genome Duplication ◽

Genome Duplication ◽

Levels Of Selection ◽

Whole Genome ◽

Interspecific Introgression ◽

Population Genomic ◽

Genomic Study ◽

Arabidopsis Arenosa

AbstractAdaptive gene flow is a consequential phenomenon across all kingdoms. Although recognition is increasing, there is no study showing that bidirectional gene flow mediates adaptation at loci that manage core processes. We previously discovered concerted molecular changes among interacting members of the meiotic machinery controlling crossover number upon adaptation to whole-genome duplication (WGD) in Arabidopsis arenosa. Here we conduct a population genomic study to test the hypothesis that adaptation to WGD has been mediated by adaptive gene flow between A. arenosa and A. lyrata. We find that A. lyrata underwent WGD more recently than A. arenosa, suggesting that pre-adapted alleles have rescued nascent A. lyrata, but we also detect gene flow in the opposite direction at functionally interacting loci under the most extreme levels of selection. These data indicate that bidirectional gene flow allowed for survival after WGD, and that the merger of these species is greater than the sum of their parts.

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Interspecific introgression mediates adaptation to whole genome duplication

10.1101/636019 ◽

2019 ◽

Cited By ~ 1

Author(s):

Sarah Marburger ◽

Patrick Monnahan ◽

Paul J. Seear ◽

Simon H. Martin ◽

Jordan Koch ◽

...

Keyword(s):

Gene Flow ◽

Whole Genome Duplication ◽

Genome Duplication ◽

Whole Genome ◽

Arabidopsis Lyrata ◽

Cellular Processes ◽

Interspecific Introgression ◽

Gene Coding ◽

Genomic Study ◽

Meiotic Stability

AbstractAdaptive gene flow is a consequential evolutionary phenomenon across all kingdoms of life. While recognition of widespread gene flow is growing, examples lack of bidirectional gene flow mediating adaptations at specific loci that cooperatively manage core cellular processes. We previously described concerted molecular changes among physically interacting members of the meiotic machinery controlling crossover number and distribution upon adaptation to whole genome duplication (WGD) in Arabidopsis arenosa. Here we conduct a population genomic study to test the hypothesis that escape from extinction following the trauma of WGD was mediated by adaptive gene flow between A. arenosa and its congener Arabidopsis lyrata. We show that A. lyrata underwent WGD more recently than A. arenosa, indicating that specific pre-adapted alleles donated by A. arenosa underwent selection and rescued the nascent A. lyrata tetraploids from early extinction. At the same time, we detect specific signals of gene flow in the opposite direction at other functionally interacting gene coding loci that display dramatic signatures of selective sweep in both tetraploid species. Cytological analysis shows that A. lyrata tetraploids exhibit similar levels of meiotic stability as A. arenosa tetraploids. Taken together, these data indicate that bidirectional gene flow allowed for an escape from extinction of the young autopolyploids, especially the rare tetraploid A. lyrata, and suggest that the merger of these species is greater than the sum of their parts.

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Faculty Opinions recommendation of Reciprocal gene loss following experimental whole-genome duplication causes reproductive isolation in yeast.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.10069956.10824063 ◽

2011 ◽

Author(s):

Santiago F Elena ◽

Stéphanie Bedhomme

Keyword(s):

Reproductive Isolation ◽

Whole Genome Duplication ◽

Gene Loss ◽

Genome Duplication ◽

Whole Genome

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Phylogenetic Analysis of T-Box Genes Demonstrates the Importance of Amphioxus for Understanding Evolution of the Vertebrate Genome

Genetics ◽

10.1093/genetics/156.3.1249 ◽

2000 ◽

Vol 156 (3) ◽

pp. 1249-1257

Author(s):

Ilya Ruvinsky ◽

Lee M Silver ◽

Jeremy J Gibson-Brown

Keyword(s):

Phylogenetic Analysis ◽

Whole Genome Duplication ◽

Genome Duplication ◽

Gene Families ◽

Vertebrate Evolution ◽

Whole Genome ◽

Vertebrate Genome ◽

T Box ◽

Genetic Complexity ◽

History Of

Abstract The duplication of preexisting genes has played a major role in evolution. To understand the evolution of genetic complexity it is important to reconstruct the phylogenetic history of the genome. A widely held view suggests that the vertebrate genome evolved via two successive rounds of whole-genome duplication. To test this model we have isolated seven new T-box genes from the primitive chordate amphioxus. We find that each amphioxus gene generally corresponds to two or three vertebrate counterparts. A phylogenetic analysis of these genes supports the idea that a single whole-genome duplication took place early in vertebrate evolution, but cannot exclude the possibility that a second duplication later took place. The origin of additional paralogs evident in this and other gene families could be the result of subsequent, smaller-scale chromosomal duplications. Our findings highlight the importance of amphioxus as a key organism for understanding evolution of the vertebrate genome.

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Comparative Mapping Between Coho Salmon (Oncorhynchus kisutch) and Three Other Salmonids Suggests a Role for Chromosomal Rearrangements in the Retention of Duplicated Regions Following a Whole Genome Duplication Event

G3 Genes|Genome|Genetics ◽

10.1534/g3.114.012294 ◽

2014 ◽

Vol 4 (9) ◽

pp. 1717-1730 ◽

Cited By ~ 37

Author(s):

M. Kodama ◽

M. S. O. Brieuc ◽

R. H. Devlin ◽

J. J. Hard ◽

K. A. Naish

Keyword(s):

Comparative Mapping ◽

Whole Genome Duplication ◽

Genome Duplication ◽

Coho Salmon ◽

Chromosomal Rearrangements ◽

Oncorhynchus Kisutch ◽

Duplication Event ◽

Whole Genome ◽

Genome Duplication Event ◽

Whole Genome Duplication Event

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Comparative regulomics supports pervasive selection on gene dosage following whole genome duplication

Genome Biology ◽

10.1186/s13059-021-02323-0 ◽

2021 ◽

Vol 22 (1) ◽

Author(s):

Gareth B. Gillard ◽

Lars Grønvold ◽

Line L. Røsæg ◽

Matilde Mengkrog Holen ◽

Øystein Monsen ◽

...

Keyword(s):

Genome Evolution ◽

Whole Genome Duplication ◽

Genome Stability ◽

Genome Duplication ◽

Gene Dosage ◽

Whole Genome ◽

Specific Expression ◽

Tissue Specific ◽

Genome Doubling ◽

Expression Evolution

Abstract Background Whole genome duplication (WGD) events have played a major role in eukaryotic genome evolution, but the consequence of these extreme events in adaptive genome evolution is still not well understood. To address this knowledge gap, we used a comparative phylogenetic model and transcriptomic data from seven species to infer selection on gene expression in duplicated genes (ohnologs) following the salmonid WGD 80–100 million years ago. Results We find rare cases of tissue-specific expression evolution but pervasive expression evolution affecting many tissues, reflecting strong selection on maintenance of genome stability following genome doubling. Ohnolog expression levels have evolved mostly asymmetrically, by diverting one ohnolog copy down a path towards lower expression and possible pseudogenization. Loss of expression in one ohnolog is significantly associated with transposable element insertions in promoters and likely driven by selection on gene dosage including selection on stoichiometric balance. We also find symmetric expression shifts, and these are associated with genes under strong evolutionary constraints such as ribosome subunit genes. This possibly reflects selection operating to achieve a gene dose reduction while avoiding accumulation of “toxic mutations”. Mechanistically, ohnolog regulatory divergence is dictated by the number of bound transcription factors in promoters, with transposable elements being one likely source of novel binding sites driving tissue-specific gains in expression. Conclusions Our results imply pervasive adaptive expression evolution following WGD to overcome the immediate challenges posed by genome doubling and to exploit the long-term genetic opportunities for novel phenotype evolution.

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Chromosome-level genome assembly of Ophiorrhiza pumila reveals the evolution of camptothecin biosynthesis

Nature Communications ◽

10.1038/s41467-020-20508-2 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Amit Rai ◽

Hideki Hirakawa ◽

Ryo Nakabayashi ◽

Shinji Kikuchi ◽

Koki Hayashi ◽

...

Keyword(s):

Genome Assembly ◽

Whole Genome Duplication ◽

Experimental Validation ◽

Genome Duplication ◽

Indole Alkaloids ◽

Whole Genome ◽

Comparative Genome Analysis ◽

Plant Genomes ◽

Genome Triplication ◽

Chromosome Level

AbstractPlant genomes remain highly fragmented and are often characterized by hundreds to thousands of assembly gaps. Here, we report chromosome-level reference and phased genome assembly of Ophiorrhiza pumila, a camptothecin-producing medicinal plant, through an ordered multi-scaffolding and experimental validation approach. With 21 assembly gaps and a contig N50 of 18.49 Mb, Ophiorrhiza genome is one of the most complete plant genomes assembled to date. We also report 273 nitrogen-containing metabolites, including diverse monoterpene indole alkaloids (MIAs). A comparative genomics approach identifies strictosidine biogenesis as the origin of MIA evolution. The emergence of strictosidine biosynthesis-catalyzing enzymes precede downstream enzymes’ evolution post γ whole-genome triplication, which occurred approximately 110 Mya in O. pumila, and before the whole-genome duplication in Camptotheca acuminata identified here. Combining comparative genome analysis, multi-omics analysis, and metabolic gene-cluster analysis, we propose a working model for MIA evolution, and a pangenome for MIA biosynthesis, which will help in establishing a sustainable supply of camptothecin.

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