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Gene Duplication, Shifting Selection, and Dosage Balance of Silicon Transporter Proteins in Marine and Freshwater Diatoms

Brylka, Karolina LU ; PINSEEL, EVELINE ; RUCK, ELIZABETH ; Conley, Daniel LU and Alverson, Andrew LU (2023) In Genome Biology and Evolution 15(12).
Abstract
Numerous factors shape the evolution of protein-coding genes, including shifts in the strength or type of selection following
gene duplications or changes in the environment. Diatoms and other silicifying organisms use a family of silicon transporters
(SITs) to import dissolved silicon from the environment. Freshwaters contain higher silicon levels than oceans, and marine
diatoms have more efficient uptake kinetics and less silicon in their cell walls, making them better competitors for a scarce
resource. We compiled SITs from 37 diatom genomes to characterize shifts in selection following gene duplications and marine–
freshwater transitions. A deep gene duplication, which coincided with a whole-genome duplication, gave... (More)
Numerous factors shape the evolution of protein-coding genes, including shifts in the strength or type of selection following
gene duplications or changes in the environment. Diatoms and other silicifying organisms use a family of silicon transporters
(SITs) to import dissolved silicon from the environment. Freshwaters contain higher silicon levels than oceans, and marine
diatoms have more efficient uptake kinetics and less silicon in their cell walls, making them better competitors for a scarce
resource. We compiled SITs from 37 diatom genomes to characterize shifts in selection following gene duplications and marine–
freshwater transitions. A deep gene duplication, which coincided with a whole-genome duplication, gave rise to two
gene lineages. One of them (SIT1–2) is present in multiple copies in most species and is known to actively import silicon.
These SITs have evolved under strong purifying selection that was relaxed in freshwater taxa. Episodic diversifying selection
was detected but not associated with gene duplications or habitat shifts. In contrast, genes in the second SIT lineage (SIT3)
were present in just half the species, the result of multiple losses. Despite conservation of SIT3 in some lineages for the past
90–100 million years, repeated losses, relaxed selection, and low expression highlighted the dispensability of SIT3, consistent
with a model of deterioration and eventual loss due to relaxed selection on SIT3 expression. The extensive but relatively balanced
history of duplications and losses, together with paralog-specific expression patterns, suggest diatoms continuously
balance gene dosage and expression dynamics to optimize silicon transport across major environmental gradients. (Less)
Please use this url to cite or link to this publication:
author
; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
codon models, episodic selection, gene duplication, ohnolog, relaxed selection
in
Genome Biology and Evolution
volume
15
issue
12
article number
evad212
publisher
Oxford University Press
external identifiers
  • pmid:37996067
  • scopus:85179905979
ISSN
1759-6653
DOI
10.1093/gbe/evad212
language
English
LU publication?
yes
id
a2ab55ae-b52a-4a92-bc2c-e289fedb42c9
date added to LUP
2023-12-08 12:43:51
date last changed
2024-03-12 00:14:53
@article{a2ab55ae-b52a-4a92-bc2c-e289fedb42c9,
  abstract     = {{Numerous factors shape the evolution of protein-coding genes, including shifts in the strength or type of selection following<br/>gene duplications or changes in the environment. Diatoms and other silicifying organisms use a family of silicon transporters<br/>(SITs) to import dissolved silicon from the environment. Freshwaters contain higher silicon levels than oceans, and marine<br/>diatoms have more efficient uptake kinetics and less silicon in their cell walls, making them better competitors for a scarce<br/>resource. We compiled SITs from 37 diatom genomes to characterize shifts in selection following gene duplications and marine–<br/>freshwater transitions. A deep gene duplication, which coincided with a whole-genome duplication, gave rise to two<br/>gene lineages. One of them (SIT1–2) is present in multiple copies in most species and is known to actively import silicon.<br/>These SITs have evolved under strong purifying selection that was relaxed in freshwater taxa. Episodic diversifying selection<br/>was detected but not associated with gene duplications or habitat shifts. In contrast, genes in the second SIT lineage (SIT3)<br/>were present in just half the species, the result of multiple losses. Despite conservation of SIT3 in some lineages for the past<br/>90–100 million years, repeated losses, relaxed selection, and low expression highlighted the dispensability of SIT3, consistent<br/>with a model of deterioration and eventual loss due to relaxed selection on SIT3 expression. The extensive but relatively balanced<br/>history of duplications and losses, together with paralog-specific expression patterns, suggest diatoms continuously<br/>balance gene dosage and expression dynamics to optimize silicon transport across major environmental gradients.}},
  author       = {{Brylka, Karolina and PINSEEL, EVELINE and RUCK, ELIZABETH and Conley, Daniel and Alverson, Andrew}},
  issn         = {{1759-6653}},
  keywords     = {{codon models; episodic selection; gene duplication; ohnolog; relaxed selection}},
  language     = {{eng}},
  month        = {{11}},
  number       = {{12}},
  publisher    = {{Oxford University Press}},
  series       = {{Genome Biology and Evolution}},
  title        = {{Gene Duplication, Shifting Selection, and Dosage Balance of Silicon Transporter Proteins in Marine and Freshwater Diatoms}},
  url          = {{http://dx.doi.org/10.1093/gbe/evad212}},
  doi          = {{10.1093/gbe/evad212}},
  volume       = {{15}},
  year         = {{2023}},
}