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The immediate metabolomic effects of whole‐genome duplication in the greater duckweed, Spirodela polyrhiza

Tian Wu (UGent) , Quinten Bafort (UGent) , Frederik Mortier (UGent) , Fabricio De Almeida Silva (UGent) , Annelore Natran (UGent) and Yves Van de Peer (UGent)
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Abstract
Premise: In plants, whole-genome duplication (WGD) is a common mutation with profound evolutionary potential. Given the costs associated with a superfluous genome copy, polyploid establishment is enigmatic. However, in the right environment, immediate phenotypic changes following WGD can facilitate establishment. Metabolite abundances are the direct output of the cell's regulatory network and determine much of the impact of environmental and genetic change on the phenotype. While it is well known that an increase in the bulk amount of genetic material can increase cell size, the impact of gene dosage multiplication on the metabolome remains largely unknown. Methods: We used untargeted metabolomics on four genetically distinct diploid-neoautotetraploid pairs of the greater duckweed, Spirodela polyrhiza, to investigate how WGD affects metabolite abundances per cell and per biomass. Results: Autopolyploidy increased metabolite levels per cell, but the response of individual metabolites varied considerably. However, the impact on metabolite level per biomass was restricted because the increased cell size reduced the metabolite concentration per cell. Nevertheless, we detected both quantitative and qualitative effects of WGD on the metabolome. Many effects were strain-specific, but some were shared by all four strains. Conclusions: The nature and impact of metabolic changes after WGD depended strongly on the genotype. Dosage effects have the potential to alter the plant metabolome qualitatively and quantitatively, but were largely balanced out by the reduction in metabolite concentration due to an increase in cell size in this species.
Keywords
Araceae, Lemnaceae, Spirodela polyrhiza, comparative metabolomics, dosage effects, duckweed, polyploidy, whole genome duplication (WGD), PLANT SECONDARY METABOLITES, FLAVONOID CHEMISTRY, POLYPLOIDY, EVOLUTION, GENE, DNA, DISCOVERY, CYTOTYPES, PLOIDY, ORIGIN

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Citation

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MLA
Wu, Tian, et al. “The Immediate Metabolomic Effects of Whole‐genome Duplication in the Greater Duckweed, Spirodela Polyrhiza.” AMERICAN JOURNAL OF BOTANY, vol. 111, no. 8, 2024, doi:10.1002/ajb2.16383.
APA
Wu, T., Bafort, Q., Mortier, F., De Almeida Silva, F., Natran, A., & Van de Peer, Y. (2024). The immediate metabolomic effects of whole‐genome duplication in the greater duckweed, Spirodela polyrhiza. AMERICAN JOURNAL OF BOTANY, 111(8). https://doi.org/10.1002/ajb2.16383
Chicago author-date
Wu, Tian, Quinten Bafort, Frederik Mortier, Fabricio De Almeida Silva, Annelore Natran, and Yves Van de Peer. 2024. “The Immediate Metabolomic Effects of Whole‐genome Duplication in the Greater Duckweed, Spirodela Polyrhiza.” AMERICAN JOURNAL OF BOTANY 111 (8). https://doi.org/10.1002/ajb2.16383.
Chicago author-date (all authors)
Wu, Tian, Quinten Bafort, Frederik Mortier, Fabricio De Almeida Silva, Annelore Natran, and Yves Van de Peer. 2024. “The Immediate Metabolomic Effects of Whole‐genome Duplication in the Greater Duckweed, Spirodela Polyrhiza.” AMERICAN JOURNAL OF BOTANY 111 (8). doi:10.1002/ajb2.16383.
Vancouver
1.
Wu T, Bafort Q, Mortier F, De Almeida Silva F, Natran A, Van de Peer Y. The immediate metabolomic effects of whole‐genome duplication in the greater duckweed, Spirodela polyrhiza. AMERICAN JOURNAL OF BOTANY. 2024;111(8).
IEEE
[1]
T. Wu, Q. Bafort, F. Mortier, F. De Almeida Silva, A. Natran, and Y. Van de Peer, “The immediate metabolomic effects of whole‐genome duplication in the greater duckweed, Spirodela polyrhiza,” AMERICAN JOURNAL OF BOTANY, vol. 111, no. 8, 2024.
@article{01J5DK5M6HWMV9DWDWE361DABX,
  abstract     = {{Premise: In plants, whole-genome duplication (WGD) is a common mutation with profound evolutionary potential. Given the costs associated with a superfluous genome copy, polyploid establishment is enigmatic. However, in the right environment, immediate phenotypic changes following WGD can facilitate establishment. Metabolite abundances are the direct output of the cell's regulatory network and determine much of the impact of environmental and genetic change on the phenotype. While it is well known that an increase in the bulk amount of genetic material can increase cell size, the impact of gene dosage multiplication on the metabolome remains largely unknown.

Methods: We used untargeted metabolomics on four genetically distinct diploid-neoautotetraploid pairs of the greater duckweed, Spirodela polyrhiza, to investigate how WGD affects metabolite abundances per cell and per biomass.

Results: Autopolyploidy increased metabolite levels per cell, but the response of individual metabolites varied considerably. However, the impact on metabolite level per biomass was restricted because the increased cell size reduced the metabolite concentration per cell. Nevertheless, we detected both quantitative and qualitative effects of WGD on the metabolome. Many effects were strain-specific, but some were shared by all four strains.

Conclusions: The nature and impact of metabolic changes after WGD depended strongly on the genotype. Dosage effects have the potential to alter the plant metabolome qualitatively and quantitatively, but were largely balanced out by the reduction in metabolite concentration due to an increase in cell size in this species.}},
  articleno    = {{e16383}},
  author       = {{Wu, Tian and Bafort, Quinten and Mortier, Frederik and De Almeida Silva, Fabricio and Natran, Annelore and Van de Peer, Yves}},
  issn         = {{0002-9122}},
  journal      = {{AMERICAN JOURNAL OF BOTANY}},
  keywords     = {{Araceae,Lemnaceae,Spirodela polyrhiza,comparative metabolomics,dosage effects,duckweed,polyploidy,whole genome duplication (WGD),PLANT SECONDARY METABOLITES,FLAVONOID CHEMISTRY,POLYPLOIDY,EVOLUTION,GENE,DNA,DISCOVERY,CYTOTYPES,PLOIDY,ORIGIN}},
  language     = {{eng}},
  number       = {{8}},
  pages        = {{15}},
  title        = {{The immediate metabolomic effects of whole‐genome duplication in the greater duckweed, Spirodela polyrhiza}},
  url          = {{http://doi.org/10.1002/ajb2.16383}},
  volume       = {{111}},
  year         = {{2024}},
}

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