Accelerated evolution at chaperone promoters among Antarctic notothenioid fishes

Bogan, Samuel N.; Place, Sean P.

doi:10.1186/s12862-019-1524-y

Cited by 10 publications

(7 citation statements)

References 90 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The main objective of this study was to test for evidence of gene duplication of inducible and constitutive HSP genes within the genome of the Antarctic notothenioid, T. bernacchii. Our results show evidence of gene duplication within the hsp70 and hsp40 super families, which supports our hypothesis that duplication events may be a key mechanism that enabled relaxed purifying selection and subsequent alterations of the highly conserved regulatory regions of inducible HSP genes observed in cryonotothens closely related to T. bernacchii [30].…”

Section: Discussionsupporting

confidence: 87%

“…Given that newly duplicated genes are under somewhat more relaxed selective pressures [12,28,29], it is plausible that retention of gene duplicates enabled alterations in the regulatory regions of the inducible HSP genes, enabling de novo regulation of such highly conserved gene products. This potential evolutionary mechanism has been further supported by a recent study performed by Bogan and Place [30], which provides evidence that notothens within the Antarctic clade, including trematomids closely related to T. bernacchii, displayed accelerated evolution and reduced purifying selection at promoter regions for several HSP genes.…”

Section: Introductionmentioning

confidence: 61%

“…Additionally, although previous studies have not observed the rapid upregulation of these genes during short-term cellular stress in notothenioid fish [ 18 , 22 , 23 ], there is some evidence that suggests the inducible isoform of hsp 90 is still responsive to long-term thermal stress, suggesting notothenioid fish may have retained some of the normal regulatory control of this gene family [ 23 ]. The slight evolutionary conservation of hsp90 expression may also explain why previous research examining hsp 90 showed lower proportions of accelerated evolution in Antarctic notothens [ 30 ].…”

Section: Discussionmentioning

confidence: 99%

“…As a consequence to gene duplicate retention and relaxed purifying selection, increased copy number could have then facilitated divergence in the cis-regulatory sequences of these genes, further canalizing the constitutive expression of ancestrally inducible HSPs and allowing for the proactive “front-loading” of chaperones for more efficient protein folding in such a demanding environment. Evidence of relaxed purifying selection of promoter regions of HSPs has been reported in notothenioids, including members within the Trematomus genus in which T. bernacchii belongs [ 30 ]. Of the HSP genes characterized in that study, promoter regions for 9 of the 10 HSP genes displayed evidence of accelerated mutation, however, we were only able to generate evidence of duplication in one of those hsp70 isoforms , hspa 13.…”

Section: Discussionmentioning

confidence: 99%

See 3 more Smart Citations

Characterizing Gene Copy Number of Heat Shock Protein Gene Families in the Emerald Rockcod, Trematomus bernacchii

Tercero

Place

2020

Genes

Self Cite

View full text Add to dashboard Cite

The suborder Notothenioidae is comprised of Antarctic fishes, several of which have lost their ability to rapidly upregulate heat shock proteins in response to thermal stress, instead adopting a pattern of expression resembling constitutive genes. Given the cold-denaturing effect that sub-zero waters have on proteins, evolution in the Southern Ocean has likely selected for increased expression of molecular chaperones. These selective pressures may have also enabled retention of gene duplicates, bolstering quantitative output of cytosolic heat shock proteins (HSPs). Given that newly duplicated genes are under more relaxed selection, it is plausible that gene duplication enabled altered regulation of such highly conserved genes. To test for evidence of gene duplication, copy number of various isoforms within major heat shock gene families were characterized via qPCR and compared between the Antarctic notothen, Trematomus bernacchii, which lost the inducible heat shock response, and the non-Antarctic notothen, Notothenia angustata, which maintains an inducible heat shock response. The results indicate duplication of isoforms within the hsp70 and hsp40 super families have occurred in the genome of T. bernacchii. The findings suggest gene duplications may have been critical in maintaining protein folding efficiency in the sub-zero waters and provided an evolutionary mechanism of alternative regulation of these conserved gene families.

show abstract

Section: Discussionsupporting

confidence: 87%

Section: Introductionmentioning

confidence: 61%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

See 2 more Smart Citations

Characterizing Gene Copy Number of Heat Shock Protein Gene Families in the Emerald Rockcod, Trematomus bernacchii

Tercero

Place

2020

Genes

Self Cite

View full text Add to dashboard Cite

show abstract

“…A recent study of changes in gene expression in rainbowfish (Melanotaenia sp.) showed that plasticity of 23 genes is under divergent selection for tolerance to heat stress, and notably among these genes were those encoding heat shock proteins (Sandoval-Castillo et al, 2020) a family of genes that Antarctic notothenioids lack the capacity to modulate (Bilyk et al, 2018;Bogan and Place, 2019).…”

Section: Discussionmentioning

confidence: 99%

Resilience of cardiac performance in Antarctic notothenioid fishes in a warming climate

O’Brien

Joyce

Crockett

et al. 2021

Journal of Experimental Biology

View full text Add to dashboard Cite

Warming in the region of the Western Antarctic Peninsula is occurring at an unprecedented rate, which may threaten the survival of Antarctic notothenioid fishes. Herein, we review studies characterizing thermal tolerance and cardiac performance in notothenioids – a group that includes both red-blooded species and the white-blooded, haemoglobinless icefishes – as well as the relevant biochemistry associated with cardiac failure during an acute temperature ramp. Because icefishes do not feed in captivity, making long-term acclimation studies unfeasible, we focus only on the responses of red-blooded notothenioids to warm acclimation. With acute warming, hearts of the white-blooded icefish Chaenocephalus aceratus display persistent arrhythmia at a lower temperature (8°C) compared with those of the red-blooded Notothenia coriiceps (14°C). When compared with the icefish, the enhanced cardiac performance of N. coriiceps during warming is associated with greater aerobic capacity, higher ATP levels, less oxidative damage and enhanced membrane integrity. Cardiac performance can be improved in N. coriiceps with warm acclimation to 5°C for 6–9 weeks, accompanied by an increase in the temperature at which cardiac failure occurs. Also, both cardiac mitochondrial and microsomal membranes are remodelled in response to warm acclimation in N. coriiceps, displaying homeoviscous adaptation. Overall, cardiac performance in N. coriiceps is malleable and resilient to warming, yet thermal tolerance and plasticity vary among different species of notothenioid fishes; disruptions to the Antarctic ecosystem driven by climate warming and other anthropogenic activities endanger the survival of notothenioids, warranting greater protection afforded by an expansion of marine protected areas.

show abstract

The cellular stress response and temperature: Function, regulation, and evolution

Somero

2020

J Exp Zool Pt A

150

View full text Add to dashboard Cite

The cellular stress response (CSR) is critical for enabling organisms to cope with thermal damage to proteins, nucleic acids, and membranes. It is a graded response whose properties vary with the degree of cellular damage. Molecular damage has positive, as well as negative, function‐perturbing effects. Positive effects include crucial regulatory interactions that orchestrate involvement of the different components of the CSR. Thermally unfolded proteins signal for rapid initiation of transcription of genes encoding heat shock proteins (HSPs), central elements of the heat shock response (HSR). Thermal disruption of messenger RNA (mRNA) secondary structures in untranslated regions leads to the culling of the mRNA pool: thermally labile mRNAs for housekeeping proteins are degraded by exonucleases; heat‐resistant mRNAs for stress proteins like HSPs then can monopolize the translational apparatus. Thus, proteins and RNA function as “cellular thermometers,” and evolved differences in their thermal stabilities enable rapid initiation of the CSR whenever cell temperature rises significantly above the normal thermal range of a species. Covalent DNA damage, which may result from increased production of reactive oxygen species, is temperature‐dependent; its extent may determine cellular survival. High levels of stress that exceed capacities for molecular repair can lead to proteolysis, inhibition of cell division, and programmed cell death (apoptosis). Onset of these processes may occur later in the stress period, after initiation of the HSR, to allow HSPs opportunity to restore protein homeostasis. Delay of these energy costly processes may also result from shortfalls in availability of adenosine triphosphate and reducing power during times of peak stress.

show abstract

Accelerated evolution at chaperone promoters among Antarctic notothenioid fishes

Cited by 10 publications

References 90 publications

Characterizing Gene Copy Number of Heat Shock Protein Gene Families in the Emerald Rockcod, Trematomus bernacchii

Characterizing Gene Copy Number of Heat Shock Protein Gene Families in the Emerald Rockcod, Trematomus bernacchii

Resilience of cardiac performance in Antarctic notothenioid fishes in a warming climate

The cellular stress response and temperature: Function, regulation, and evolution

Contact Info

Product

Resources

About