Phylogenomics reveals convergent evolution of red-violet coloration in land plants and the origins of the anthocyanin biosynthetic pathway
Abstract
The flavonoids, one of the largest classes of plant secondary metabolites, are found in lineages that span the land plant phylogeny and play important roles in stress responses and as pigments. Perhaps the most well-studied flavonoids are the anthocyanins that have human health benefits and help plants attract pollinators, regulate hormone production, and confer resistance to abiotic and biotic stresses. The canonical biochemical pathway responsible for the production of these pigments is well-characterized for flowering plants yet its conservation across deep divergences in land plants remains debated and poorly understood. Many early land plants such as mosses, liverworts, and ferns produce flavonoid pigments, but their biosynthetic origins and homologies to the anthocyanin pathway remain uncertain. We conducted phylogenetic analyses using full genome sequences representing nearly all major green plant lineages to reconstruct the evolutionary history of the anthocyanin biosynthetic pathway then test the hypothesis that genes in this pathway are present in early land plants. We found that the entire pathway was not intact until the most recent common ancestor of seed plants and that orthologs of many downstream enzymes are absent from seedless plants including mosses, liverworts, and ferns. Our results also highlight the utility of phylogenetic inference, asmore »
- Authors:
-
- Duke Univ., Durham, NC (United States)
- Univ. of Colorado, Boulder, CO (United States)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- HudsonAlpha Institute of Biotechnology, Huntsville, AL (United States)
- HudsonAlpha Institute of Biotechnology, Huntsville, AL (United States); Department of Energy Joint Genome Institute, Berkeley, CA (United States)
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)
- OSTI Identifier:
- 1648893
- Alternate Identifier(s):
- OSTI ID: 1638887
- Grant/Contract Number:
- AC05-00OR22725; AC02-05CH11231; DEB-1737899
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Molecular Phylogenetics and Evolution
- Additional Journal Information:
- Journal Volume: 151; Journal ID: ISSN 1055-7903
- Publisher:
- Elsevier
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Phylogenomics; Anthocyanins; Plant pigments; Anthocyanin biosynthetic pathway; Flavonoids
Citation Formats
Piatkowski, Bryan T., Imwattana, Karn, Tripp, Erin A., Weston, David J., Healey, Adam, Schmutz, Jeremy, and Shaw, A. Jonathan. Phylogenomics reveals convergent evolution of red-violet coloration in land plants and the origins of the anthocyanin biosynthetic pathway. United States: N. p., 2020.
Web. doi:10.1016/j.ympev.2020.106904.
Piatkowski, Bryan T., Imwattana, Karn, Tripp, Erin A., Weston, David J., Healey, Adam, Schmutz, Jeremy, & Shaw, A. Jonathan. Phylogenomics reveals convergent evolution of red-violet coloration in land plants and the origins of the anthocyanin biosynthetic pathway. United States. https://doi.org/10.1016/j.ympev.2020.106904
Piatkowski, Bryan T., Imwattana, Karn, Tripp, Erin A., Weston, David J., Healey, Adam, Schmutz, Jeremy, and Shaw, A. Jonathan. Mon .
"Phylogenomics reveals convergent evolution of red-violet coloration in land plants and the origins of the anthocyanin biosynthetic pathway". United States. https://doi.org/10.1016/j.ympev.2020.106904. https://www.osti.gov/servlets/purl/1648893.
@article{osti_1648893,
title = {Phylogenomics reveals convergent evolution of red-violet coloration in land plants and the origins of the anthocyanin biosynthetic pathway},
author = {Piatkowski, Bryan T. and Imwattana, Karn and Tripp, Erin A. and Weston, David J. and Healey, Adam and Schmutz, Jeremy and Shaw, A. Jonathan},
abstractNote = {The flavonoids, one of the largest classes of plant secondary metabolites, are found in lineages that span the land plant phylogeny and play important roles in stress responses and as pigments. Perhaps the most well-studied flavonoids are the anthocyanins that have human health benefits and help plants attract pollinators, regulate hormone production, and confer resistance to abiotic and biotic stresses. The canonical biochemical pathway responsible for the production of these pigments is well-characterized for flowering plants yet its conservation across deep divergences in land plants remains debated and poorly understood. Many early land plants such as mosses, liverworts, and ferns produce flavonoid pigments, but their biosynthetic origins and homologies to the anthocyanin pathway remain uncertain. We conducted phylogenetic analyses using full genome sequences representing nearly all major green plant lineages to reconstruct the evolutionary history of the anthocyanin biosynthetic pathway then test the hypothesis that genes in this pathway are present in early land plants. We found that the entire pathway was not intact until the most recent common ancestor of seed plants and that orthologs of many downstream enzymes are absent from seedless plants including mosses, liverworts, and ferns. Our results also highlight the utility of phylogenetic inference, as compared to pairwise sequence similarity, in orthology assessment within large gene families that have complex duplication-loss histories. Here, we suggest that the production of red-violet flavonoid pigments widespread in seedless plants, including the 3-deoxyanthocyanins, requires the activity of novel, as-yet discovered enzymes, and represents convergent evolution of red-violet coloration across land plants.},
doi = {10.1016/j.ympev.2020.106904},
journal = {Molecular Phylogenetics and Evolution},
number = ,
volume = 151,
place = {United States},
year = {Mon Jul 06 00:00:00 EDT 2020},
month = {Mon Jul 06 00:00:00 EDT 2020}
}
Web of Science
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