A chromosome-level genome for the nudibranch gastropod Berghia stephanieae helps parse clade-specific gene expression in novel and conserved phenotypes

Abstract Background How novel phenotypes originate from conserved genes, processes, and tissues remains a major question in biology. Research that sets out to answer this question often focuses on the conserved genes and processes involved, an approach that explicitly excludes the impact of genetic...

Full description

Bibliographic Details
Main Authors: Jessica A. Goodheart, Robin A. Rio, Neville F. Taraporevala, Rose A. Fiorenza, Seth R. Barnes, Kevin Morrill, Mark Allan C. Jacob, Carl Whitesel, Park Masterson, Grant O. Batzel, Hereroa T. Johnston, M. Desmond Ramirez, Paul S. Katz, Deirdre C. Lyons
Format: Article
Language:English
Published: BMC 2024-01-01
Series:BMC Biology
Subjects:
Online Access:https://doi.org/10.1186/s12915-024-01814-3
_version_ 1797349754354532352
author Jessica A. Goodheart
Robin A. Rio
Neville F. Taraporevala
Rose A. Fiorenza
Seth R. Barnes
Kevin Morrill
Mark Allan C. Jacob
Carl Whitesel
Park Masterson
Grant O. Batzel
Hereroa T. Johnston
M. Desmond Ramirez
Paul S. Katz
Deirdre C. Lyons
author_facet Jessica A. Goodheart
Robin A. Rio
Neville F. Taraporevala
Rose A. Fiorenza
Seth R. Barnes
Kevin Morrill
Mark Allan C. Jacob
Carl Whitesel
Park Masterson
Grant O. Batzel
Hereroa T. Johnston
M. Desmond Ramirez
Paul S. Katz
Deirdre C. Lyons
author_sort Jessica A. Goodheart
collection DOAJ
description Abstract Background How novel phenotypes originate from conserved genes, processes, and tissues remains a major question in biology. Research that sets out to answer this question often focuses on the conserved genes and processes involved, an approach that explicitly excludes the impact of genetic elements that may be classified as clade-specific, even though many of these genes are known to be important for many novel, or clade-restricted, phenotypes. This is especially true for understudied phyla such as mollusks, where limited genomic and functional biology resources for members of this phylum have long hindered assessments of genetic homology and function. To address this gap, we constructed a chromosome-level genome for the gastropod Berghia stephanieae (Valdés, 2005) to investigate the expression of clade-specific genes across both novel and conserved tissue types in this species. Results The final assembled and filtered Berghia genome is comparable to other high-quality mollusk genomes in terms of size (1.05 Gb) and number of predicted genes (24,960 genes) and is highly contiguous. The proportion of upregulated, clade-specific genes varied across tissues, but with no clear trend between the proportion of clade-specific genes and the novelty of the tissue. However, more complex tissue like the brain had the highest total number of upregulated, clade-specific genes, though the ratio of upregulated clade-specific genes to the total number of upregulated genes was low. Conclusions Our results, when combined with previous research on the impact of novel genes on phenotypic evolution, highlight the fact that the complexity of the novel tissue or behavior, the type of novelty, and the developmental timing of evolutionary modifications will all influence how novel and conserved genes interact to generate diversity.
first_indexed 2024-03-08T12:34:58Z
format Article
id doaj.art-f375f31b80ac46ca8abf0fdfde41d0ae
institution Directory Open Access Journal
issn 1741-7007
language English
last_indexed 2024-03-08T12:34:58Z
publishDate 2024-01-01
publisher BMC
record_format Article
series BMC Biology
spelling doaj.art-f375f31b80ac46ca8abf0fdfde41d0ae2024-01-21T12:35:28ZengBMCBMC Biology1741-70072024-01-0122112110.1186/s12915-024-01814-3A chromosome-level genome for the nudibranch gastropod Berghia stephanieae helps parse clade-specific gene expression in novel and conserved phenotypesJessica A. Goodheart0Robin A. Rio1Neville F. Taraporevala2Rose A. Fiorenza3Seth R. Barnes4Kevin Morrill5Mark Allan C. Jacob6Carl Whitesel7Park Masterson8Grant O. Batzel9Hereroa T. Johnston10M. Desmond Ramirez11Paul S. Katz12Deirdre C. Lyons13Division of Invertebrate Zoology, American Museum of Natural HistoryBioengineering Department, Stanford UniversityScripps Institution of Oceanography, University of California San DiegoScripps Institution of Oceanography, University of California San DiegoScripps Institution of Oceanography, University of California San DiegoScripps Institution of Oceanography, University of California San DiegoScripps Institution of Oceanography, University of California San DiegoScripps Institution of Oceanography, University of California San DiegoScripps Institution of Oceanography, University of California San DiegoScripps Institution of Oceanography, University of California San DiegoScripps Institution of Oceanography, University of California San DiegoDepartment of Biology, University of Massachusetts AmherstDepartment of Biology, University of Massachusetts AmherstScripps Institution of Oceanography, University of California San DiegoAbstract Background How novel phenotypes originate from conserved genes, processes, and tissues remains a major question in biology. Research that sets out to answer this question often focuses on the conserved genes and processes involved, an approach that explicitly excludes the impact of genetic elements that may be classified as clade-specific, even though many of these genes are known to be important for many novel, or clade-restricted, phenotypes. This is especially true for understudied phyla such as mollusks, where limited genomic and functional biology resources for members of this phylum have long hindered assessments of genetic homology and function. To address this gap, we constructed a chromosome-level genome for the gastropod Berghia stephanieae (Valdés, 2005) to investigate the expression of clade-specific genes across both novel and conserved tissue types in this species. Results The final assembled and filtered Berghia genome is comparable to other high-quality mollusk genomes in terms of size (1.05 Gb) and number of predicted genes (24,960 genes) and is highly contiguous. The proportion of upregulated, clade-specific genes varied across tissues, but with no clear trend between the proportion of clade-specific genes and the novelty of the tissue. However, more complex tissue like the brain had the highest total number of upregulated, clade-specific genes, though the ratio of upregulated clade-specific genes to the total number of upregulated genes was low. Conclusions Our results, when combined with previous research on the impact of novel genes on phenotypic evolution, highlight the fact that the complexity of the novel tissue or behavior, the type of novelty, and the developmental timing of evolutionary modifications will all influence how novel and conserved genes interact to generate diversity.https://doi.org/10.1186/s12915-024-01814-3NoveltyLineage-restricted genesNudibranchiaGastropodaDifferential gene expression
spellingShingle Jessica A. Goodheart
Robin A. Rio
Neville F. Taraporevala
Rose A. Fiorenza
Seth R. Barnes
Kevin Morrill
Mark Allan C. Jacob
Carl Whitesel
Park Masterson
Grant O. Batzel
Hereroa T. Johnston
M. Desmond Ramirez
Paul S. Katz
Deirdre C. Lyons
A chromosome-level genome for the nudibranch gastropod Berghia stephanieae helps parse clade-specific gene expression in novel and conserved phenotypes
BMC Biology
Novelty
Lineage-restricted genes
Nudibranchia
Gastropoda
Differential gene expression
title A chromosome-level genome for the nudibranch gastropod Berghia stephanieae helps parse clade-specific gene expression in novel and conserved phenotypes
title_full A chromosome-level genome for the nudibranch gastropod Berghia stephanieae helps parse clade-specific gene expression in novel and conserved phenotypes
title_fullStr A chromosome-level genome for the nudibranch gastropod Berghia stephanieae helps parse clade-specific gene expression in novel and conserved phenotypes
title_full_unstemmed A chromosome-level genome for the nudibranch gastropod Berghia stephanieae helps parse clade-specific gene expression in novel and conserved phenotypes
title_short A chromosome-level genome for the nudibranch gastropod Berghia stephanieae helps parse clade-specific gene expression in novel and conserved phenotypes
title_sort chromosome level genome for the nudibranch gastropod berghia stephanieae helps parse clade specific gene expression in novel and conserved phenotypes
topic Novelty
Lineage-restricted genes
Nudibranchia
Gastropoda
Differential gene expression
url https://doi.org/10.1186/s12915-024-01814-3
work_keys_str_mv AT jessicaagoodheart achromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT robinario achromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT nevilleftaraporevala achromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT roseafiorenza achromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT sethrbarnes achromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT kevinmorrill achromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT markallancjacob achromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT carlwhitesel achromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT parkmasterson achromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT grantobatzel achromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT hereroatjohnston achromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT mdesmondramirez achromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT paulskatz achromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT deirdreclyons achromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT jessicaagoodheart chromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT robinario chromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT nevilleftaraporevala chromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT roseafiorenza chromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT sethrbarnes chromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT kevinmorrill chromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT markallancjacob chromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT carlwhitesel chromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT parkmasterson chromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT grantobatzel chromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT hereroatjohnston chromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT mdesmondramirez chromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT paulskatz chromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes
AT deirdreclyons chromosomelevelgenomeforthenudibranchgastropodberghiastephanieaehelpsparsecladespecificgeneexpressioninnovelandconservedphenotypes