Evolution of red algal plastid genomes: ancient architectures, introns, horizontal gene transfer, and taxonomic utility of plastid markers.
Red algae have the most gene-rich plastid genomes known, but despite their evolutionary importance these genomes remain poorly sampled. Here we characterize three complete and one partial plastid genome from a diverse range of florideophytes. By unifying annotations across all available red algal pl...
Main Authors: | , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Public Library of Science (PLoS)
2013-01-01
|
Series: | PLoS ONE |
Online Access: | http://europepmc.org/articles/PMC3607583?pdf=render |
_version_ | 1819134092348751872 |
---|---|
author | Jan Janouškovec Shao-Lun Liu Patrick T Martone Wilfrid Carré Catherine Leblanc Jonas Collén Patrick J Keeling |
author_facet | Jan Janouškovec Shao-Lun Liu Patrick T Martone Wilfrid Carré Catherine Leblanc Jonas Collén Patrick J Keeling |
author_sort | Jan Janouškovec |
collection | DOAJ |
description | Red algae have the most gene-rich plastid genomes known, but despite their evolutionary importance these genomes remain poorly sampled. Here we characterize three complete and one partial plastid genome from a diverse range of florideophytes. By unifying annotations across all available red algal plastid genomes we show they all share a highly compact and slowly-evolving architecture and uniquely rich gene complements. Both chromosome structure and gene content have changed very little during red algal diversification, and suggest that plastid-to nucleus gene transfers have been rare. Despite their ancient character, however, the red algal plastids also contain several unprecedented features, including a group II intron in a tRNA-Met gene that encodes the first example of red algal plastid intron maturase - a feature uniquely shared among florideophytes. We also identify a rare case of a horizontally-acquired proteobacterial operon, and propose this operon may have been recruited for plastid function and potentially replaced a nucleus-encoded plastid-targeted paralogue. Plastid genome phylogenies yield a fully resolved tree and suggest that plastid DNA is a useful tool for resolving red algal relationships. Lastly, we estimate the evolutionary rates among more than 200 plastid genes, and assess their usefulness for species and subspecies taxonomy by comparison to well-established barcoding markers such as cox1 and rbcL. Overall, these data demonstrates that red algal plastid genomes are easily obtainable using high-throughput sequencing of total genomic DNA, interesting from evolutionary perspectives, and promising in resolving red algal relationships at evolutionarily-deep and species/subspecies levels. |
first_indexed | 2024-12-22T09:57:41Z |
format | Article |
id | doaj.art-262a5036d21943ed890afde1f240aee5 |
institution | Directory Open Access Journal |
issn | 1932-6203 |
language | English |
last_indexed | 2024-12-22T09:57:41Z |
publishDate | 2013-01-01 |
publisher | Public Library of Science (PLoS) |
record_format | Article |
series | PLoS ONE |
spelling | doaj.art-262a5036d21943ed890afde1f240aee52022-12-21T18:30:14ZengPublic Library of Science (PLoS)PLoS ONE1932-62032013-01-0183e5900110.1371/journal.pone.0059001Evolution of red algal plastid genomes: ancient architectures, introns, horizontal gene transfer, and taxonomic utility of plastid markers.Jan JanouškovecShao-Lun LiuPatrick T MartoneWilfrid CarréCatherine LeblancJonas CollénPatrick J KeelingRed algae have the most gene-rich plastid genomes known, but despite their evolutionary importance these genomes remain poorly sampled. Here we characterize three complete and one partial plastid genome from a diverse range of florideophytes. By unifying annotations across all available red algal plastid genomes we show they all share a highly compact and slowly-evolving architecture and uniquely rich gene complements. Both chromosome structure and gene content have changed very little during red algal diversification, and suggest that plastid-to nucleus gene transfers have been rare. Despite their ancient character, however, the red algal plastids also contain several unprecedented features, including a group II intron in a tRNA-Met gene that encodes the first example of red algal plastid intron maturase - a feature uniquely shared among florideophytes. We also identify a rare case of a horizontally-acquired proteobacterial operon, and propose this operon may have been recruited for plastid function and potentially replaced a nucleus-encoded plastid-targeted paralogue. Plastid genome phylogenies yield a fully resolved tree and suggest that plastid DNA is a useful tool for resolving red algal relationships. Lastly, we estimate the evolutionary rates among more than 200 plastid genes, and assess their usefulness for species and subspecies taxonomy by comparison to well-established barcoding markers such as cox1 and rbcL. Overall, these data demonstrates that red algal plastid genomes are easily obtainable using high-throughput sequencing of total genomic DNA, interesting from evolutionary perspectives, and promising in resolving red algal relationships at evolutionarily-deep and species/subspecies levels.http://europepmc.org/articles/PMC3607583?pdf=render |
spellingShingle | Jan Janouškovec Shao-Lun Liu Patrick T Martone Wilfrid Carré Catherine Leblanc Jonas Collén Patrick J Keeling Evolution of red algal plastid genomes: ancient architectures, introns, horizontal gene transfer, and taxonomic utility of plastid markers. PLoS ONE |
title | Evolution of red algal plastid genomes: ancient architectures, introns, horizontal gene transfer, and taxonomic utility of plastid markers. |
title_full | Evolution of red algal plastid genomes: ancient architectures, introns, horizontal gene transfer, and taxonomic utility of plastid markers. |
title_fullStr | Evolution of red algal plastid genomes: ancient architectures, introns, horizontal gene transfer, and taxonomic utility of plastid markers. |
title_full_unstemmed | Evolution of red algal plastid genomes: ancient architectures, introns, horizontal gene transfer, and taxonomic utility of plastid markers. |
title_short | Evolution of red algal plastid genomes: ancient architectures, introns, horizontal gene transfer, and taxonomic utility of plastid markers. |
title_sort | evolution of red algal plastid genomes ancient architectures introns horizontal gene transfer and taxonomic utility of plastid markers |
url | http://europepmc.org/articles/PMC3607583?pdf=render |
work_keys_str_mv | AT janjanouskovec evolutionofredalgalplastidgenomesancientarchitecturesintronshorizontalgenetransferandtaxonomicutilityofplastidmarkers AT shaolunliu evolutionofredalgalplastidgenomesancientarchitecturesintronshorizontalgenetransferandtaxonomicutilityofplastidmarkers AT patricktmartone evolutionofredalgalplastidgenomesancientarchitecturesintronshorizontalgenetransferandtaxonomicutilityofplastidmarkers AT wilfridcarre evolutionofredalgalplastidgenomesancientarchitecturesintronshorizontalgenetransferandtaxonomicutilityofplastidmarkers AT catherineleblanc evolutionofredalgalplastidgenomesancientarchitecturesintronshorizontalgenetransferandtaxonomicutilityofplastidmarkers AT jonascollen evolutionofredalgalplastidgenomesancientarchitecturesintronshorizontalgenetransferandtaxonomicutilityofplastidmarkers AT patrickjkeeling evolutionofredalgalplastidgenomesancientarchitecturesintronshorizontalgenetransferandtaxonomicutilityofplastidmarkers |