Anthony A Snead, Corey R Quackenbush, Shawn Trojahn, Anna L McDonald, Luana S F Lins, Chris Cornelius, Paula E Adams, Dengke Ma, Yuying Hsu, Eric Haag, Frédéric Silvestre, Akira Kanamori, Ryan L Earley, Joanna L Kelley
{"title":"Embryonic thermal environments drive plasticity in gene expression.","authors":"Anthony A Snead, Corey R Quackenbush, Shawn Trojahn, Anna L McDonald, Luana S F Lins, Chris Cornelius, Paula E Adams, Dengke Ma, Yuying Hsu, Eric Haag, Frédéric Silvestre, Akira Kanamori, Ryan L Earley, Joanna L Kelley","doi":"10.1007/s10695-025-01522-x","DOIUrl":null,"url":null,"abstract":"<p><p>When embryos experience different environments than their parents, plasticity can enable the development of alternate phenotypes that confer higher fitness in the new conditions. Temperature-induced plasticity could be especially critical for species that inhabit areas with considerable thermal variation. We studied transcriptional variation in embryos of mangrove rivulus (Kryptolebias marmoratus)-a self-fertilizing hermaphroditic, eurythermal fish that resides in notoriously spatiotemporally variable mangrove forests-exposed to different thermal regimes during development. To study transcriptional plasticity, we first improved the genome assembly to chromosome length scaffolds (N50 of 28.17 Megabases). Whole transcriptome sequencing revealed that both temperature and developmental timing modulated embryonic gene expression. We found few differences in gene expression between embryos incubated in cold and warm conditions and assessed before the temperature-sensitive period of development, indicating high resistance to stochastic changes in gene expression early in development. Replicate embryos exposed to cold temperatures and sampled after the temperature-sensitive period showed less variation in gene expression than those sampled before, suggesting canalization of the plastic response. DNA replication/repair, organelle, and gas transport pathways were upregulated while nervous system development, cell signaling, and cell adhesion were downregulated in cold-exposed compared to warm-exposed embryos sampled after the temperature-sensitive period. These plastic shifts in gene expression could have major implications for reorganizing the phenotype (e.g., apoptosis, mitosis) in response to environmental changes occurring within a generation.</p>","PeriodicalId":12274,"journal":{"name":"Fish Physiology and Biochemistry","volume":"51 3","pages":"111"},"PeriodicalIF":2.5000,"publicationDate":"2025-06-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Fish Physiology and Biochemistry","FirstCategoryId":"97","ListUrlMain":"https://doi.org/10.1007/s10695-025-01522-x","RegionNum":3,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q3","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
When embryos experience different environments than their parents, plasticity can enable the development of alternate phenotypes that confer higher fitness in the new conditions. Temperature-induced plasticity could be especially critical for species that inhabit areas with considerable thermal variation. We studied transcriptional variation in embryos of mangrove rivulus (Kryptolebias marmoratus)-a self-fertilizing hermaphroditic, eurythermal fish that resides in notoriously spatiotemporally variable mangrove forests-exposed to different thermal regimes during development. To study transcriptional plasticity, we first improved the genome assembly to chromosome length scaffolds (N50 of 28.17 Megabases). Whole transcriptome sequencing revealed that both temperature and developmental timing modulated embryonic gene expression. We found few differences in gene expression between embryos incubated in cold and warm conditions and assessed before the temperature-sensitive period of development, indicating high resistance to stochastic changes in gene expression early in development. Replicate embryos exposed to cold temperatures and sampled after the temperature-sensitive period showed less variation in gene expression than those sampled before, suggesting canalization of the plastic response. DNA replication/repair, organelle, and gas transport pathways were upregulated while nervous system development, cell signaling, and cell adhesion were downregulated in cold-exposed compared to warm-exposed embryos sampled after the temperature-sensitive period. These plastic shifts in gene expression could have major implications for reorganizing the phenotype (e.g., apoptosis, mitosis) in response to environmental changes occurring within a generation.
期刊介绍:
Fish Physiology and Biochemistry is an international journal publishing original research papers in all aspects of the physiology and biochemistry of fishes. Coverage includes experimental work in such topics as biochemistry of organisms, organs, tissues and cells; structure of organs, tissues, cells and organelles related to their function; nutritional, osmotic, ionic, respiratory and excretory homeostasis; nerve and muscle physiology; endocrinology; reproductive physiology; energetics; biochemical and physiological effects of toxicants; molecular biology and biotechnology and more.