دورية أكاديمية

An initial comparative genomic autopsy of wasting disease in sea stars.

التفاصيل البيبلوغرافية
العنوان: An initial comparative genomic autopsy of wasting disease in sea stars.
المؤلفون: Ruiz-Ramos DV; Department of Life and Environmental Sciences, University of California, Merced, CA, USA., Schiebelhut LM; Department of Life and Environmental Sciences, University of California, Merced, CA, USA., Hoff KJ; Institute for Computer Science and Mathematics, University of Greifswald, Greifswald, Germany.; Center for Functional Genomics of Microbes, University of Greifswald, Greifswald, Germany., Wares JP; Department of Genetics and the Odum School of Ecology, University of Georgia, Athens, GA, USA., Dawson MN; Department of Life and Environmental Sciences, University of California, Merced, CA, USA.
المصدر: Molecular ecology [Mol Ecol] 2020 Mar; Vol. 29 (6), pp. 1087-1102. Date of Electronic Publication: 2020 Mar 17.
نوع المنشور: Journal Article; Research Support, Non-U.S. Gov't; Research Support, U.S. Gov't, Non-P.H.S.
اللغة: English
بيانات الدورية: Publisher: Blackwell Scientific Publications Country of Publication: England NLM ID: 9214478 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1365-294X (Electronic) Linking ISSN: 09621083 NLM ISO Abbreviation: Mol Ecol Subsets: MEDLINE
أسماء مطبوعة: Original Publication: Oxford, UK : Blackwell Scientific Publications, c1992-
مواضيع طبية MeSH: Starfish/*genetics , Wasting Syndrome/*veterinary, Animals ; California ; Forensic Sciences ; Genome ; Genome, Mitochondrial ; Genomics ; Pacific Ocean ; Transcriptome
مستخلص: Beginning in 2013, sea stars throughout the Eastern North Pacific were decimated by wasting disease, also known as "asteroid idiopathic wasting syndrome" (AIWS) due to its elusive aetiology. The geographic extent and taxonomic scale of AIWS meant events leading up to the outbreak were heterogeneous, multifaceted, and oftentimes unobserved; progression from morbidity to death was rapid, leaving few tell-tale symptoms. Here, we take a forensic genomic approach to discover candidate genes that may help explain sea star wasting syndrome. We report the first genome and annotation for Pisaster ochraceus, along with differential gene expression (DGE) analyses in four size classes, three tissue types, and in symptomatic and asymptomatic individuals. We integrate nucleotide polymorphisms associated with survivors of the wasting disease outbreak, DGE associated with temperature treatments in P. ochraceus, and DGE associated with wasting in another asteroid Pycnopodia helianthoides. In P. ochraceus, we found DGE across all tissues, among size classes, and between asymptomatic and symptomatic individuals; the strongest wasting-associated DGE signal was in pyloric caecum. We also found previously identified outlier loci co-occur with differentially expressed genes. In cross-species comparisons of symptomatic and asymptomatic individuals, consistent responses distinguish genes associated with invertebrate innate immunity and chemical defence, consistent with context-dependent stress responses, defensive apoptosis, and tissue degradation. Our analyses thus highlight genomic constituents that may link suspected environmental drivers (elevated temperature) with intrinsic differences among individuals (age/size, alleles associated with susceptibility) that elicit organismal responses (e.g., coelomocyte proliferation) and manifest as sea star wasting mass mortality.
(© 2020 John Wiley & Sons Ltd.)
References: Alker, A. P., Smith, G. W., & Kim, K. (2001). Characterization of Aspergillus sydowii (Thom et Church), a fungal pathogen of Caribbean sea fan corals. Hydrobiologia, 460(1-3), 105-111.
Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215, 403-410.
Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., … Sherlock, G. (2000). Gene ontology: Tool for the unification of biology. Nature Genetics, 25, 25-29.
Bao, W., Kojima, K. K., & Kohany, O. (2015). Repbase Update, a database of repetitive elements in eukaryotic genomes. Mobile DNA, 6(1), 11.
Bates, A. E., Hilton, B. J., & Harley, C. D. (2009). Effects of temperature, season and locality on wasting disease in the keystone predatory sea star Pisaster ochraceus. Diseases of Aquatic Organisms, 86(3), 245-251.
Bay, R. A., Harrigan, R. J., Le Underwood, V., Gibbs, H. L., Smith, T. B., & Ruegg, K. (2018). Genomic signals of selection predict climate-driven population declines in a migratory bird. Science, 359(6371), 83-86.
Bernt, M., Donath, A., Jühling, F., Externbrink, F., Florentz, C., Fritzsch, G., … Stadler, P. F. (2013). MITOS: Improved de novo metazoan mitochondrial genome annotation. Molecular Phylogenetics and Evolution, 69(2), 313-319.
Blok, M. J., Spruijt, L., de Coo, I. F. M., Schoonderwoerd, K., Hendrickx, A., & Smeets, H. J. (2007). Mutations in the ND5 subunit of complex I of the mitochondrial DNA are a frequent cause of oxidative phosphorylation disease. Journal of Medical Genetics, 44(4), e74-e74.
Bond, N. A., Cronin, M. F., Freeland, H., & Mantua, N. (2015). Causes and impacts of the 2014 warm anomaly in the NE Pacific. Geophysical Research Letters, 42(9), 3414-3420.
Burge, C. A., Friedman, C. S., Getchell, R., House, M., Lafferty, K. D., Mydlarz, L. D., … Kiryu, I. (2016). Complementary approaches to diagnosing marine diseases: A union of the modern and the classic. Philosophical Transactions of the Royal Society B: Biological Sciences, 371(1689), 20150207.
Burge, C. A., Griffin, F. J., & Friedman, C. S. (2006). Mortality and herpesvirus infections of the Pacific oyster Crassostrea gigas in Tomales Bay, California, USA. Diseases of Aquatic Organisms, 72(1), 31-43.
Burge, C. A., Kim, C. J. S., Lyles, J. M., & Harvell, C. D. (2013). Special issue oceans and humans health: The ecology of marine opportunists. Microbial Ecology, 65(4), 869-879.
Burge, C. A., Mark Eakin, C., Friedman, C. S., Froelich, B., Hershberger, P. K., Hofmann, E. E., … Harvell, C. D. (2014). Climate change influences on marine infectious diseases: Implications for management and society. The Annual Review of Marine Science, 6, 249-277.
Burt, J. M., Tinker, M. T., Okamoto, D. K., Demes, K. W., Holmes, K., & Salomon, A. K. (2018). Sudden collapse of a mesopredator reveals its complementary role in mediating rocky reef regime shifts. Proceedings of the Royal Society B: Biological Sciences, 285(1883), 20180553.
Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., & Madden, T. L. (2009). blast+: Architecture and applications. BMC Bioinformatics, 10(1), 421.
Canapa, A., Barucca, M., Biscotti, M. A., Forconi, M., & Olmo, E. (2015). Transposons, genome size, and evolutionary insights in animals. Cytogenetic and Genome Research, 147(4), 217-239.
Castro, K. M., Cobb, J. S., Gomez-Chiarri, M., & Tlusty, M. (2012). Epizootic shell disease in American lobsters Homarus americanus in southern New England: Past, present and future. Diseases of Aquatic Organisms, 100(2), 149-158.
Chandler, V. K., & Wares, J. P. (2017). RNA expression and disease tolerance are associated with a “keystone mutation” in the ochre sea star Pisaster ochraceus. PeerJ, 5, e3696.
Chapman, J. A., Ho, I., Sunkara, S., Luo, S., Schroth, G. P., & Rokhsar, D. S. (2011). Meraculous: De novo genome assembly with short paired-end reads. PLoS ONE, 6(8), e23501.
Chapman, R. W., Mancia, A., Beal, M., Veloso, A., Rathburn, C., Blair, A., … Sanger, D. (2011). The transcriptomic responses of the eastern oyster, Crassostrea virginica, to environmental conditions. Molecular Ecology, 20(7), 1431-1449.
Charif, D., & Lobry, J. R. (2007). seqinr 1.0-2: A contributed package to the R project for statistical computing devoted to biological sequences retrieval and analysis. In U. Bastolla, M. Porto, H. E. Roman, & M. Vendruscolo (Eds.), Structural approaches to sequence evolution. Biological and medical physics, biomedical engineering (pp. 207-232). Springer.
Chen, N. (2004). Using RepeatMasker to identify repetitive elements in genomic sequences. Current Protocols in Bioinformatics, 5(1), 4.10.1-4.10.14.
Coghlan, A. (2011). Little book of R for Bioinformatics. Cambridge, UK: Welcome Trust Sanger Institute.
De Wit, P., Rogers-Bennett, L., Kudela, R. M., & Palumbi, S. R. (2014). Forensic genomics as a novel tool for identifying the causes of mass mortality events. Nature Communications, 5, 3652.
Dubey, J. P., Zarnke, R., Thomas, N. J., Wong, S. K., Bonn, W. V., Briggs, M., … Thulliez, P. (2003). Toxoplasma gondii, Neospora caninum, Sarcocystis neurona, and Sarcocystis canis-like infections in marine mammals. Veterinary Parasitology, 116(4), 275-296.
Duggins, D. O. (1983). Starfish predation and the creation of mosaic patterns in a kelp-dominated community. Ecology, 64(6), 1610-1619.
Eisenlord, M. E., Groner, M. L., Yoshioka, R. M., Elliott, J., Maynard, J., Fradkin, S., … van Hooidonk, R. (2016). Ochre star mortality during the 2014 wasting disease epizootic: Role of population size structure and temperature. Philosophical Transactions of the Royal Society B: Biological Sciences, 371(1689), 20150212.
Elliott, T. A., & Gregory, T. R. (2015). What’s in a genome? The C-value enigma and the evolution of eukaryotic genome content. Philosophical Transactions of the Royal Society B: Biological Sciences, 370(1678), 20140331.
Fey, S. B., Siepielski, A. M., Nusslé, S., Cervantes-Yoshida, K., Hwan, J. L., Huber, E. R., … Carlson, S. M. (2015). Recent shifts in the occurrence, cause, and magnitude of animal mass mortality events. Proceedings of the National Academy of Sciences, 112(4), 1083-1088.
Fuess, L. E., Eisenlord, M. E., Closek, C. J., Tracy, A. M., Mauntz, R., Gignoux-Wolfsohn, S., … Roberts, S. B. (2015). Up in arms: Immune and nervous system response to sea star wasting disease. PLoS ONE, 10(7), e0133053.
Gardner, G. R., Harshbarger, J. C., Lake, J. L., Sawyer, T. K., Price, K. L., Stephenson, M. D., … Togstad, H. A. (1995). Association of prokaryotes with symptomatic appearance of withering syndrome in black abalone Haliotis cracherodii. Journal of Invertebrate Pathology, 66(2), 111-120.
Gokudan, S., Muta, T., Tsuda, R., Koori, K., Kawahara, T., Seki, N., … Kawabata, S.-I. (1999). Horseshoe crab acetyl group-recognizing lectins involved in innate immunity are structurally related to fibrinogen. Proceedings of the National Academy of Sciences, 96(18), 10086-10091.
Goymer, P. (2007). Genetic variation: Synonymous mutations break their silence. Nature Reviews Genetics, 8(2), 92.
Gravem, S. A., & Morgan, S. G. (2017). Shifts in intertidal zonation and refuge use by prey after mass mortalities of two predators. Ecology, 98(4), 1006-1015.
Gudenkauf, B. M., & Hewson, I. (2015). Metatranscriptomic analysis of Pycnopodia helianthoides (Asteroidea) affected by sea star wasting disease. PLoS ONE, 10(5), e0128150.
Harley, C. D. G., Pankey, M. S., Wares, J. P., Grosberg, R. K., & Wonham, M. J. (2006). Color polymorphism and genetic structure in the sea star Pisaster ochraceus. The Biological Bulletin, 211(3), 248-262.
Harvell, D., Altizer, S., Cattadori, I. M., Harrington, L., & Weil, E. (2009). Climate change and wildlife diseases: When does the host matter the most? Ecology, 90(4), 912-920.
Harvell, D., Montecino-Latorre, D., Caldwell, J. M., Burt, J. M., Bosley, K., Keller, A., … Pontier, O. (2019). Disease epidemic and a marine heat wave are associated with the continental-scale collapse of a pivotal predator (Pycnopodia helianthoides). Science. Advances, 5(1), eaau7042.
Hewson, I., Bistolas, K. S. I., Quijano Cardé, E. M., Button, J. B., Foster, P. J., Flanzenbaum, J. M., … Lewis, C. K. (2018). Investigating the complex association between viral ecology, environment, and Northeast Pacific Sea Star Wasting. Frontiers in Marine Science, 5, 77.
Hewson, I., Button, J. B., Gudenkauf, B. M., Miner, B., Newton, A. L., Gaydos, J. K., … Harvell, C. D. (2014). Densovirus associated with sea-star wasting disease and mass mortality. Proceedings of the National Academy of Sciences, 111(48), 17278-17283.
Hibino, T., Loza-Coll, M., Messier, C., Majeske, A. J., Cohen, A. H., Terwilliger, D. P., … Rast, J. P. (2006). The immune gene repertoire encoded in the purple sea urchin genome. Developmental Biology, 300(1), 349-365.
Hoff, K. J. (2020). MakeHub: Fully automated generation of UCSC Genome Browser Assembly Hubs. Genomics, Proteomics & Bioinformatics, 17(2019), 546-549.
Hoff, K. J., Lange, S., Lomsadze, A., Borodovsky, M., & Stanke, M. (2015). braker1: Unsupervised RNA-Seq-based genome annotation with genemark-et and augustus. Bioinformatics, 32(5), 767-769.
Hoff, K. J., Lomsadze, A., Borodovsky, M., & Stanke, M. (2019). Whole-genome annotation with braker. Methods in Molecular Biology, 1962, 65-95.
Hu, Z.-L., Bao, J., & Reecy, J. M. (2008). CateGOrizer: A web-based program to batch analyze gene on-tology classification categories. Online Journal of Bioinformatics, 9, 108-112.
Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2008). Bioinformatics enrichment tools: Paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Research, 37(1), 1-13.
Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols, 4(1), 44.
Jackson, E. W., Pepe-Ranney, C., Debenport, S. J., Buckley, D. H., & Hewson, I. (2018). The microbial landscape of sea stars and the anatomical and interspecies variability of their microbiome. Frontiers in Microbiology, 9, 1829.
Kamogashira, T., Fujimoto, C., & Yamasoba, T. (2015). Reactive oxygen species, apoptosis, and mitochondrial dysfunction in hearing loss. BioMed Research International, 2015, 617207.
Kent, W. J., Sugnet, C. W., Furey, T. S., Roskin, K. M., Pringle, T. H., Zahler, A. M., & Haussler, D. (2002). The human genome browser at UCSC. Genome Research, 12(6), 996-1006.
Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R., & Salzberg, S. L. (2013). tophat2: Accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biology, 14(4), R36.
Kohl, W. T., McClure, T. I., & Miner, B. G. (2016). Decreased temperature facilitates short-term sea star wasting disease survival in the keystone intertidal sea star Pisaster ochraceus. PLoS ONE, 11(4), e0153670.
Lafferty, K. D., & Hofmann, E. E. (2016). Marine disease impacts, diagnosis, forecasting, management and policy. The Royal Society. Philosophical Transactions of the Royal Society B: Biological Sciences, 371(1689), 20150200.
Langmead, B., Trapnell, C., Pop, M., & Salzberg, S. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology, 10, R25.
Lasky, J. R., Des Marais, D. L., Lowry, D. B., Povolotskaya, I., McKay, J. K., Richards, J. H., … Juenger, T. E. (2014). Natural variation in abiotic stress responsive gene expression and local adaptation to climate in Arabidopsis thaliana. Molecular Biology and Evolution, 31(9), 2283-2296.
Lessios, H. A. (2016). The great Diadema antillarum die-off: 30 years later. Annual Review of Marine Science, 8(1), 267-283.
Li, H., & Durbin, R. (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25(14), 1754-1760.
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., … Durbin, R. (2009). The sequence alignment/map format and samtools. Bioinformatics, 25, 2078-2079.
Lieberman-Aiden, E., Van Berkum, N. L., Williams, L., Imakaev, M., Ragoczy, T., Telling, A., … Dorschner, M. O. (2009). Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science, 326(5950), 289-293.
Lomsadze, A., Burns, P. D., & Borodovsky, M. (2014). Integration of mapped RNA-Seq reads into automatic training of eukaryotic gene finding algorithm. Nucleic Acids Research, 42(15), e119-e119.
Mah, C. L., & Blake, D. B. (2012). Global diversity and phylogeny of the Asteroidea (Echinodermata). PLoS ONE, 7(4), e35644.
Matsubara, M., Komatsu, M., Araki, T., Asakawa, S., Yokobori, S., Watanabe, K., & Wada, H. (2005). The phylogenetic status of Paxillosida (Asteroidea) based on complete mitochondrial DNA sequences. Molecular Phylogenetics and Evolution, 36(3), 598-605.
McCarthy, D. J., Chen, Y., & Smyth, G. K. (2012). Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Research, 40(10), 4288-4297.
Menge, B. A. (1983). Components of predation intensity in the low zone of the New England rocky intertidal region. Oecologia, 58(2), 141-155.
Menge, B. A., Cerny-Chipman, E. B., Johnson, A., Sullivan, J., Gravem, S., & Chan, F. (2016). Sea star wasting disease in the keystone predator Pisaster ochraceus in Oregon: Insights into differential population impacts, recovery, predation rate, and temperature effects from long-term research. PLoS ONE, 11(5), e0153994.
Miner, C. M., Burnaford, J. L., Ambrose, R. F., Antrim, L., Bohlmann, H., Blanchette, C. A., … Raimondi, P. T. (2018). Large-scale impacts of sea star wasting disease (SSWD) on intertidal sea stars and implications for recovery. PLoS ONE, 13(3), e0192870.
Montecino-Latorre, D., Eisenlord, M. E., Turner, M., Yoshioka, R., Harvell, C. D., Pattengill-Semmens, C. V., … Gaydos, J. K. (2016). Devastating transboundary impacts of sea star wasting disease on subtidal asteroids. PLoS ONE, 11(10), e0163190.
Morgulis, A., Gertz, E. M., Schäffer, A. A., & Agarwala, R. (2005). WindowMasker: Window-based masker for sequenced genomes. Bioinformatics, 22(2), 134-141.
Oberst, A., Bender, C., & Green, D. R. (2008). Living with death: The evolution of the mitochondrial pathway of apoptosis in animals. Cell Death and Differentiation, 15(7), 1139.
Paine, R. T. (1974). Intertidal community structure. Oecologia, 15(2), 93-120.
Pancer, Z. (2000). Dynamic expression of multiple scavenger receptor cysteine-rich genes in coelomocytes of the purple sea urchin. Proceedings of the National Academy of Sciences, 97(24), 13156-13161.
Putnam, N. H., O'Connell, B. L., Stites, J. C., Rice, B. J., Blanchette, M., Calef, R., … Green, R. E. (2016). Chromosome-scale shotgun assembly using an in vitro method for long-range linkage. Genome Research, 26(3), 342-350.
Quinlan, A. R., & Hall, I. M. (2010). bedtools: A flexible suite of utilities for comparing genomic features. Bioinformatics, 26(6), 841-842.
Raimundo, N., Song, L., Shutt, T. E., McKay, S. E., Cotney, J., Guan, M.-X., … Shadel, G. S. (2012). Mitochondrial stress engages E2F1 apoptotic signaling to cause deafness. Cell, 148(4), 716-726.
Ralston, A., & Shaw, K. (2008). Gene expression regulates cell differentiation. National Education, 1(1), 127-131.
Ramírez-Gómez, F., & García-Arrarás, J. E. (2010). Echinoderm immunity. Invertebrate Survival Journal, 7(2), 211-220.
Saotome, K., & Komatsu, M. (2002). Chromosomes of Japanese starfishes. Zoological Science, 19(10), 1095-1104.
Schiebelhut, L. M., Puritz, J. B., & Dawson, M. N. (2018). Decimation by sea star wasting disease and rapid genetic change in a keystone species, Pisaster ochraceus. Proceedings of the National Academy of Sciences, 115(27), 7069-7074.
Schultz, J. A., Cloutier, R. N., & Côté, I. M. (2016). Evidence for a trophic cascade on rocky reefs following sea star mass mortality in British Columbia. PeerJ, 4, e1980.
Shadel, G. S. (2008). Expression and maintenance of mitochondrial DNA: New insights into human disease pathology. The American Journal of Pathology, 172(6), 1445-1456.
Short, F. T., Muehlstein, L. K., & Porter, D. (1987). Eelgrass wasting disease: Cause and recurrence of a marine epidemic. The Biological Bulletin, 173(3), 557-562.
Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V., & Zdobnov, E. M. (2015). BUSCO: Assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics, 31(19), 3210-3212.
Sodergren, E., Weinstock, G. M., Davidson, E. H., Cameron, R. A., Gibbs, R. A., Angerer, R. C., … Burke, R. D. (2006). The genome of the sea urchin Strongylocentrotus purpuratus. Science, 314(5801), 941-952.
Stanke, M., Diekhans, M., Baertsch, R., & Haussler, D. (2008). Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics, 24(5), 637-644.
Supek, F., Bosnjak, M., Skunca, N., & Smuc, T. (2011). REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS ONE, 6, e21800.
Tait, S. W., & Green, D. R. (2010). Mitochondria and cell death: Outer membrane permeabilization and beyond. Nature Reviews Molecular Cell Biology, 11(9), 621.
The Gene Ontology Consortium. (2016). Expansion of the Gene Ontology knowledgebase and resources. Nucleic Acids Research, 45(D1), D331-D338.
The UniProt Consortium. (2016). UniProt: The universal protein knowledgebase. Nucleic Acids Research, 45(D1), D158-D169.
Tijssen, P., Pénzes, J. J., Yu, Q., Pham, H. T., & Bergoin, M. (2016). Diversity of small, single-stranded DNA viruses of invertebrates and their chaotic evolutionary past. Journal of Invertebrate Pathology, 140, 83-96.
Tracy, A. M., Pielmeier, M. L., Yoshioka, R. M., Heron, S. F., & Harvell, C. D. (2019). Increases and decreases in marine disease reports in an era of global change. Proceedings of the Royal Society B, 286(1912), 20191718.
Uniprot Consortium (2014). UniProt: A hub for protein information. Nucleic Acids Research, 43(D1), D204-D212.
Wang, Y., Ning, X., Gao, P., Wu, S., Sha, M., Lv, M., … Jiang, Z. (2017). Inflammasome activation triggers caspase-1-mediated cleavage of cGAS to regulate responses to DNA virus infection. Immunity, 46(3), 393-404.
Wares, J. P., & Schiebelhut, L. M. (2016). What doesn’t kill them makes them stronger: An association between elongation factor 1-α overdominance in the sea star Pisaster ochraceus and “sea star wasting disease”. PeerJ, 4, e1876.
Wu, T. D., Reeder, J., Lawrence, M., Becker, G., & Brauer, M. J. (2016). GMAP and GSNAP for genomic sequence alignment: Enhancements to speed, accuracy, and functionality. Methods in Molecular Biology, 1418, 283-334.
Yasuda, N., Hamaguchi, M., Sasaki, M., Nagai, S., Saba, M., & Nadaoka, K. (2006). Complete mitochondrial genome sequences for Crown-of-thorns starfish Acanthaster planci and Acanthaster brevispinus. BMC Genomics, 7(1), 17.
Yin, T., Cook, D., & Lawrence, M. (2012). ggbio: An R package for extending the grammar of graphics for genomic data. Genome Biology, 13(8), R77.
Zapico, S. C., & Ubelaker, D. H. (2013). MtDNA mutations and their role in aging, diseases and forensic sciences. Aging and Disease, 4(6), 364.
فهرسة مساهمة: Keywords: asteroid idiopathic wasting syndrome (AIWS); disease; gene expression; genome; mass mortality; sea star wasting disease (SSWD)
تواريخ الأحداث: Date Created: 20200219 Date Completed: 20210301 Latest Revision: 20210301
رمز التحديث: 20240628
DOI: 10.1111/mec.15386
PMID: 32069379
قاعدة البيانات: MEDLINE
الوصف
تدمد:1365-294X
DOI:10.1111/mec.15386