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      The genome of the golden apple snail Pomacea canaliculata provides insight into stress tolerance and invasive adaptation

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          Abstract

          Background

          The golden apple snail ( Pomacea canaliculata) is a freshwater snail listed among the top 100 worst invasive species worldwide and a noted agricultural and quarantine pest that causes great economic losses. It is characterized by fast growth, strong stress tolerance, a high reproduction rate, and adaptation to a broad range of environments.

          Results

          Here, we used long-read sequencing to produce a 440-Mb high-quality, chromosome-level assembly of the P. canaliculata genome. In total, 50 Mb (11.4%) repeat sequences and 21,533 gene models were identified in the genome. The major findings of this study include the recent explosion of DNA/hAT-Charlie transposable elements, the expansion of the P450 gene family, and the constitution of the cellular homeostasis system, which contributes to ecological plasticity in stress adaptation. In addition, the high transcriptional levels of perivitelline genes in the ovary and albumen gland promote the function of nutrient supply and defense ability in eggs. Furthermore, the gut metagenome also contains diverse genes for food digestion and xenobiotic degradation.

          Conclusions

          These findings collectively provide novel insights into the molecular mechanisms of the ecological plasticity and high invasiveness.

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          Most cited references64

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          Cellular strategies of protein quality control.

          Eukaryotic cells must contend with a continuous stream of misfolded proteins that compromise the cellular protein homeostasis balance and jeopardize cell viability. An elaborate network of molecular chaperones and protein degradation factors continually monitor and maintain the integrity of the proteome. Cellular protein quality control relies on three distinct yet interconnected strategies whereby misfolded proteins can either be refolded, degraded, or delivered to distinct quality control compartments that sequester potentially harmful misfolded species. Molecular chaperones play a critical role in determining the fate of misfolded proteins in the cell. Here, we discuss the spatial and temporal organization of cellular quality control strategies and their implications for human diseases linked to protein misfolding and aggregation.
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            Transmembrane transport of endo- and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins.

            Multidrug Resistance Proteins (MRPs), together with the cystic fibrosis conductance regulator (CFTR/ABCC7) and the sulfonylurea receptors (SUR1/ABCC8 and SUR2/ABCC9) comprise the 13 members of the human "C" branch of the ATP binding cassette (ABC) superfamily. All C branch proteins share conserved structural features in their nucleotide binding domains (NBDs) that distinguish them from other ABC proteins. The MRPs can be further divided into two subfamilies "long" (MRP1, -2, -3, -6, and -7) and "short" (MRP4, -5, -8, -9, and -10). The short MRPs have a typical ABC transporter structure with two polytropic membrane spanning domains (MSDs) and two NBDs, while the long MRPs have an additional NH2-terminal MSD. In vitro, the MRPs can collectively confer resistance to natural product drugs and their conjugated metabolites, platinum compounds, folate antimetabolites, nucleoside and nucleotide analogs, arsenical and antimonial oxyanions, peptide-based agents, and, under certain circumstances, alkylating agents. The MRPs are also primary active transporters of other structurally diverse compounds, including glutathione, glucuronide, and sulfate conjugates of a large number of xeno- and endobiotics. In vivo, several MRPs are major contributors to the distribution and elimination of a wide range of both anticancer and non-anticancer drugs and metabolites. In this review, we describe what is known of the structure of the MRPs and the mechanisms by which they recognize and transport their diverse substrates. We also summarize knowledge of their possible physiological functions and evidence that they may be involved in the clinical drug resistance of various forms of cancer.
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              Adaptation to deep-sea chemosynthetic environments as revealed by mussel genomes.

              Hydrothermal vents and methane seeps are extreme deep-sea ecosystems that support dense populations of specialized macro-benthos such as mussels. But the lack of genome information hinders the understanding of the adaptation of these animals to such inhospitable environments. Here we report the genomes of a deep-sea vent/seep mussel (Bathymodiolus platifrons) and a shallow-water mussel (Modiolus philippinarum). Phylogenetic analysis shows that these mussel species diverged approximately 110.4 million years ago. Many gene families, especially those for stabilizing protein structures and removing toxic substances from cells, are highly expanded in B. platifrons, indicating adaptation to extreme environmental conditions. The innate immune system of B. platifrons is considerably more complex than that of other lophotrochozoan species, including M. philippinarum, with substantial expansion and high expression levels of gene families that are related to immune recognition, endocytosis and caspase-mediated apoptosis in the gill, revealing presumed genetic adaptation of the deep-sea mussel to the presence of its chemoautotrophic endosymbionts. A follow-up metaproteomic analysis of the gill of B. platifrons shows methanotrophy, assimilatory sulfate reduction and ammonia metabolic pathways in the symbionts, providing energy and nutrients, which allow the host to thrive. Our study of the genomic composition allowing symbiosis in extremophile molluscs gives wider insights into the mechanisms of symbiosis in other organisms such as deep-sea tubeworms and giant clams.
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                Author and article information

                Journal
                Gigascience
                Gigascience
                gigascience
                GigaScience
                Oxford University Press
                2047-217X
                09 August 2018
                September 2018
                09 August 2018
                : 7
                : 9
                : giy101
                Affiliations
                [1 ]Agricultural Genomics Institute, Chinese Academy of Agricultural Sciences, Pengfei Road Shenzhen, Guangdong, 518120, China
                [2 ]BGI-Shenzhen, Shenzhen, Guangdong, 518083, China
                Author notes
                Correspondence address. Bo Liu, Agricultural Genomic Institute, Chinese Academy of Agricultural Sciences, Shenzhen, Guangdong, 518120, China. E-mail: lb_bobo@ 123456aliyun.com
                Correspondence address. Wei Fan, E-mail: fanwei@ 123456caas.cn

                These authors contributed equally to this work.

                Author information
                http://orcid.org/0000-0001-5036-8733
                Article
                giy101
                10.1093/gigascience/giy101
                6129957
                30107526
                d4a0e509-25b3-40b4-834e-25aa3af63c57
                © The Author(s) 2018. Published by Oxford University Press.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 03 August 2018
                : 15 May 2018
                : 12 February 2018
                Page count
                Pages: 13
                Funding
                Funded by: National Key Research and Development Program of China
                Award ID: 2016YFC1200600
                Funded by: Shenzhen Science and Technology 10.13039/501100010877
                Award ID: JCYJ20150630165133395
                Funded by: Fund of Key Laboratory of Shenzhen
                Award ID: ZDSYS20141118170111640
                Funded by: Agricultural Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences 10.13039/100007540
                Categories
                Research

                golden apple snail,pomacea canaliculata,genome,adaptive evolution,stress tolerance,p450,reproduction,perivitelline,metagenome

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