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Histone post-translational modifications (PTMs) are epigenetic marks that play a critical role in the expression and maintenance of DNA, but they remain largely uninvestigated in non-model organisms due to technical challenges. To begin alleviating this issue, we developed a workflow for histone PTM analysis in the Mozambique tilapia (Oreochromis mossambicus), being a widespread and environmentally hardy fish, using mass spectrometry methods. By incorporating multiple protein digestion methods into the preparation of each sample, we reliably quantified 503 biologically relevant histone PTMs. All of these histone PTMs, collectively referred to as the global histone PTM landscape, were characterized in the gills, kidney, and testes of this fish. By comparing the global histone PTM landscape between the three tissues, we found that 90.46% of histone PTMs were tissue-dependent. The workflow and tools for histone PTM analysis described in this study are now publicly available and enable comprehensive investigation into the influence of environmental stress on histone PTMs in non-model organisms. Given the functionality and flexibility of histone PTMs, we anticipate that the study of histone PTMs in ecologically relevant contexts will provide ground-breaking insights into comparative physiology and evolution. 

Histone post-translational modifications (PTMs) are epigenetic marks that operate within the central dogma of molecular biology: upon an environmental stimulus, the histone PTMs surrounding DNA can be changed in a way that modifies gene expression, and, therefore, the abundance and composition of RNA and proteins within cells (1). Once a change is induced, histone PTMs can offer organisms resilience to their environments through processes such as developmental plasticity (2, 3). The purpose of this study was to investigate whether histone PTMs mediate developmental plasticity in Mozambique tilapia facing salinity challenges. To this aim, we exposed fish to either freshwater or hypersalinity during their early critical window of development, then continued to raise the fish in either freshwater or seawater, respectively, for 18 months. Once the fish reached adulthood, we acclimated them to either freshwater or seawater. Following salinity treatments, we quantified 343 histone PTMs in the gills of each fish. We show here that histone PTMs differ dramatically between fish exposed to distinct environmental conditions for 18 months, and that the majority of histone PTM alterations persist for at least four weeks. However, histone PTMs respond minimally to salinity acclimation during adulthood. These results challenge our prior assumptions regarding the timescale of the histone PTM response, demonstrating that it does not necessarily precede the proteomic response or acclimation. Although this finding complicates our interpretation of developmental plasticity, it signifies that histone PTMs reflect prolonged exposure to environmental conditions. 

Histone post-translational modifications (PTMs) are epigenetic marks that can be induced by environmental stress and elicit heritable patterns of gene expression. To investigate this process in an ecological context, we characterized the influence of salinity stress on histone PTMs within the gills, kidney, and testes of Mozambique tilapia (Oreochromis mossambicus). A total of 503 histone PTMs were quantified in each tissue sample and compared between freshwater-adapted fish exposed to salinity treatments that varied in intensity and duration. Three salinity-responsive histone PTMs were identified in this study. When freshwater-adapted fish were exposed to seawater for two hours, the relative abundance of H1K16ub significantly increased in the gills. Long-term salinity stress elicited changes in an additional two histone PTMs in the testes. When freshwater-adapted fish were exposed to a pulse of severe salinity stress, where salinity reached a maximum of 82.5 g/kg, the relative abundance of H3K14ac and H3K18ub decreased significantly in the testes. This study demonstrates that specific types of salinity stress can alter histone PTMs in Mozambique tilapia, both in an osmoregulatory organ and in the germ line. These results signify a potential for histone PTMs to be involved in salinity acclimation and adaptation in euryhaline fishes, thereby adding to a growing body of evidence that epigenetic mechanisms are involved in such processes. 

ABSTRACT Organisms mount the cellular stress response whenever environmental parameters exceed the range that is conducive to maintaining homeostasis. This response is critical for survival in emergency situations because it protects macromolecular integrity and, therefore, cell/organismal function. From an evolutionary perspective, the cellular stress response counteracts severe stress by accelerating adaptation via a process called stress-induced evolution. In this Review, we summarize five key physiological mechanisms of stress-induced evolution. Namely, these are stress-induced changes in: (1) mutation rates, (2) histone post-translational modifications, (3) DNA methylation, (4) chromoanagenesis and (5) transposable element activity. Through each of these mechanisms, organisms rapidly generate heritable phenotypes that may be adaptive, maladaptive or neutral in specific contexts. Regardless of their consequences to individual fitness, these mechanisms produce phenotypic variation at the population level. Because variation fuels natural selection, the physiological mechanisms of stress-induced evolution increase the likelihood that populations can avoid extirpation and instead adapt under the stress of new environmental conditions.