Journal Article

DNA methyltransferase 3a mediates developmental thermal plasticity

Seebacher, Frank, Loughland, Isabella, Little, Alexander

2021

Overview

Background Thermal plasticity is pivotal for evolution in changing climates and in mediating resilience to its potentially negative effects. The efficacy to respond to environmental change depends on underlying mechanisms. DNA methylation induced by DNA methyltransferase 3 enzymes in the germline or during early embryonic development may be correlated with responses to environmental change. This developmental plasticity can interact with reversible acclimation within adult organisms, which would increase the speed of response and could alleviate potential mismatches between parental or early embryonic environments and those experienced at later life stages. Our aim was to determine whether there is a causative relationship between DNMT3 enzyme and developmental thermal plasticity and whether either or both interact with short-term acclimation to alter fitness and thermal responses in zebrafish ( Danio rerio ). Results We developed a novel DNMT3a knock-out model to show that sequential knock-out of DNA methyltransferase 3a isoforms (DNMT3aa −/− and DNMT3aa −/− ab −/− ) additively decreased survival and increased deformities when cold developmental temperatures in zebrafish offspring mismatched warm temperatures experienced by parents. Interestingly, short-term cold acclimation of parents before breeding rescued DNMT3a knock-out offspring by restoring survival at cold temperatures. DNMT3a knock-out genotype interacted with developmental temperatures to modify thermal performance curves in offspring, where at least one DNMT3a isoform was necessary to buffer locomotion from increasing temperatures. The thermal sensitivity of citrate synthase activity, an indicator of mitochondrial density, was less severely affected by DNMT3a knock-out, but there was nonetheless a significant interaction between genotype and developmental temperatures. Conclusions Our results show that DNMT3a regulates developmental thermal plasticity and that the phenotypic effects of different DNMT3a isoforms are additive. However, DNMT3a interacts with other mechanisms, such as histone (de)acetylation, induced during short-term acclimation to buffer phenotypes from environmental change. Interactions between these mechanisms make phenotypic compensation for climate change more efficient and make it less likely that thermal plasticity incurs a cost resulting from environmental mismatches.

• Publisher: BioMed Central,BioMed Central Ltd,Springer Nature B.V,BMC
• Subject: Acclimation / Acclimatization / Acetylation / Adaptation, Physiological - genetics / Analysis / Animals / Animals, Genetically Modified - genetics / Animals, Genetically Modified - growth & development / Animals, Genetically Modified - physiology / Biomedical and Life Sciences / Breeding / Buffers / Citrate synthase / Climate Change / Cold acclimation / Cost of plasticity / Danio rerio / Deoxyribonucleic acid / Developmental plasticity / Developmental stages / DNA / DNA (Cytosine-5-)-Methyltransferases - genetics / DNA (Cytosine-5-)-Methyltransferases - metabolism / DNA methylation / DNA methyltransferase / DNA Methyltransferase 3A / Embryogenesis / Embryonic development / Embryonic growth stage / Environmental changes / Epigenetic inheritance / Epigenetics / Female / Gene expression / Genetic aspects / Genotype & phenotype / Genotypes / Histones / Isoforms / Life Sciences / Locomotion / Male / Metabolism / Methods / Methyltransferases / Mitochondria / Observations / Offspring / Phenotype / Phenotypes / Phenotypic plasticity / Physiology / Plastic properties / Plasticity / Research Article / Survival / Thermotolerance - genetics / Transgenerational plasticity / Zebra fish / Zebrafish / Zebrafish - genetics / Zebrafish - growth & development / Zebrafish - physiology / Zebrafish Proteins - genetics / Zebrafish Proteins - metabolism