Abstract
Biological response to rapid changing environments is an outstanding research question in ecology and evolution. Biological invasions provide excellent “natural” experiments to study such a complex response process, as invaders often encounter rapidly changing environments during biological invasions. The regulation of heat shock proteins (Hsp) is a common pathway responsible for various environmental stresses; however, the comprehensive study on Hsp system across the whole genome and potential roles in determining invasion success are still largely unexplored. Here, we used a marine invasive model ascidian, Ciona savignyi, to investigate transcriptional response of Hsp-related genes to harsh environments. We identified 32 genes, including three Hsp20, six Hsp40, ten Hsp60, eight Hsp70, three Hsp90, one Hsp100, and one heat shock transcription factor (Hsf), across the whole genome of C. savignyi. We further characterized gene structure and protein motifs, and identified potential heat shock elements (HSEs) in promoters of Hsp genes. The expression analysis showed that most Hsp genes, but not all, were involved in transcriptional response to temperature and salinity challenges in a duration- and stress-specific pattern, and the maximum amplitude of induction occurred in Hsp70-4 after 1-h of high temperature treatment. However, the Hsf gene was scarcely induced and limited interactions were predicted between Hsp and Hsf genes. Our study provide the first systematic genome-wide analysis of Hsp and Hsf family in the marine invasive model ascidian, and our results are expected to dissect Hsp-based molecular mechanisms responsible for extreme environmental adaptation using Ciona as a model system.
Highlights
Nowadays, species are frequently subjected to various suboptimal environmental challenges owing to multiple factors such as global climate change, range expansion, and environmental pollution caused by human activities (Hoffmann and Sgrò, 2011; Zhan et al, 2015)
The prediction of subcellular localization revealed that the only CsHsf acting as transcriptional factor was predicted to be localized in the nucleus, while CsHsp were present in various cytosolic compartments, mostly in cytoplasm and some in endoplasmic reticulum (ER), mitochondria and nucleus (Table 1)
A total of 10 CsHsp60 were identified, BLAST analysis revealed that nine cytosolic CsHsp60 showed high similarity to eight different subunits (α, β, γ, δ, ε, ζ, η, and θ) of chaperonins containing T-complex polypeptide 1/TCP1 ring complex (CCT/TRiC), which formed hetero-oligomers to function as a whole, while the remaining mitochondrial CsHsp60-8 represented another subfamily of chaperonins
Summary
Species are frequently subjected to various suboptimal environmental challenges owing to multiple factors such as global climate change, range expansion (e.g., biological invasions), and environmental pollution caused by human activities (Hoffmann and Sgrò, 2011; Zhan et al, 2015). Deep investigations on rapid adaptation to environmental challenges, to extreme environments that species frequently encounter are critical to assess impacts of rapid environmental changes on species’ geographical distributions and evolutionary fates (Seneviratne et al, 2014). Among known underlying mechanisms for rapid and flexible stress responses, heat shock proteins (Hsp), as a group of evolutionarily conserved protein families, is one of the crucial molecular pathways that facilitate organisms to cope with environmental fluctuations through correcting protein folding and/or maintaining protein homeostasis (Feder and Hofmann, 1999; Morimoto, 2002). This work has been well conducted in model species, such as Mus musculus, Danio rerio, Caenorhabditis elegans, and Drosophila (Borchel et al, 2017) It remains largely unexploited in aquatic invaders, where they encounter frequently extreme environments during invasions (Zhan et al, 2015). The comprehensive study of Hsp-related genes in invasive species, as well as their roles in invasion success, can help dissect ecological and evolutionary mechanisms responsible for extreme environmental adaptation
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