Abstract
The Australian freshwater crayfish species, Cherax quadricarinatus Von Martens, 1868, is an important commercial and invasive species that is also being increasingly used as a model organism to address important and interesting questions in crustacean biology. Through deep sequencing of the transcriptome of C. quadricarinatus from the hepatopancreas and four other tissues, we examine the evolution of endogenously transcribed cellulase genes and provide new insights into controversial issues regarding the nutritional biology of crayfishes. A cluster assembly approach yielded one of the highest quality transcriptome assemblies for a decapod crustacean to date. A total of 206,341,872 reads with an average read length of 80 bp were generated from sequencing the transcriptomes from the heart, kidney, hepatopancreas, nerve, and testis tissues. The assembled transcriptome contains a total of 44,525 transcripts. A total of 65 transcripts coding for carbohydrate-active enzymes (CAZy) were identified based on hidden Markov model (HMM), and a majority of them display high relative transcript abundance in the hepatopancreas tissue, supporting their role in nutrient digestion. Comprehensive phylogenetic analyses of proteins belonging to two main glycosyl hydrolase families (GH9 and GH5) suggest shared ancestry of C. quadricarinatus cellulases with other characterized crustacean cellulases. Our study significantly expands the number of known crustacean-derived CAZy-coding transcripts. More importantly, the surprising level of evolutionary diversification of these proteins in C. quadricarinatus suggests that these enzymes may have been of critical importance in the adaptation of freshwater crayfishes to new plant-based food sources as part of their successful invasion of freshwater systems from marine ancestors.
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Abdu, U., Davis, C., Khalaila, I., & Sagi, A. (2002). The vitellogenin cDNA of Cherax quadricarinatus encodes a lipoprotein with calcium binding ability, and its expression is induced following the removal of the androgenic gland in a sexually plastic system. General and Comparative Endocrinology, 127(3), 263–272. doi:10.1016/S0016-6480(02)00053-9.
Ahyong, S., & Yeo, D. J. (2007). Feral populations of the Australian Red-Claw crayfish (Cherax quadricarinatus von Martens) in water supply catchments of Singapore. Biological Invasions, 9(8), 943–946. doi:10.1007/s10530-007-9094-0.
Akashi, H., & Eyre-Walker, A. (1998). Translational selection and molecular evolution. Current Opinion in Genetics & Development, 8(6), 688–693. doi:10.1016/S0959-437X(98)80038-5.
Alföldi, J., & Lindblad-Toh, K. (2013). Comparative genomics as a tool to understand evolution and disease. Genome Research, 23(7), 1063–1068.
Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215(3), 403–410. doi:10.1016/S0022-2836(05)80360-2.
Amemiya, C. T., Alfoldi, J., Lee, A. P., Fan, S., Philippe, H., MacCallum, I., et al. (2013). The African coelacanth genome provides insights into tetrapod evolution. [Article]. Nature, 496(7445), 311–316. doi:10.1038/nature12027. http://www.nature.com/nature/journal/v496/n7445/abs/nature12027.html#supplementary-information .
Aspeborg, H., Coutinho, P., Wang, Y., Brumer, H., & Henrissat, B. (2012). Evolution, substrate specificity and subfamily classification of glycoside hydrolase family 5 (GH5). BMC Evolutionary Biology, 12(1), 186.
Austin, C. (1996). Systematics of the freshwater crayfish genus Cherax Erichson (Decapoda: Parastacidae) in Northern and Eastern Australia: electrophoretic and morphological variation. Australian Journal of Zoology, 44(3), 259–296. doi:10.1071/ZO9960259.
Austin, C., & Knott, B. (1996). Systematics of the freshwater crayfish genus Cherax Erichson (Decapoda: Parastacidae) in South-Western Australia: electrophoretic, morphological and habitat variation. Australian Journal of Zoology, 44(3), 223–258. doi:10.1071/ZO9960223.
Bolger, A. M., Lohse, M., & Usadel, B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. doi:10.1093/bioinformatics/btu170.
Bracken-Grissom, H. D., Ahyong, S. T., Wilkinson, R. D., Feldmann, R. M., Schweitzer, C. E., Breinholt, J. W., et al. (2014). The emergence of lobsters: phylogenetic relationships, morphological evolution and divergence time comparisons of an ancient group (Decapoda: Achelata, Astacidea, Glypheidea, Polychelida). Systematic Biology. doi:10.1093/sysbio/syu008.
Byrne, K. A., Lehnert, S. A., Johnson, S. E., & Moore, S. S. (1999). Isolation of a cDNA encoding a putative cellulase in the red claw crayfish Cherax quadricarinatus. Gene, 239(2), 317–324. doi:10.1016/S0378-1119(99)00396-0.
Chen, R. (2015). A paradigm shift in biomass technology from complete to partial cellulose hydrolysis: lessons learned from nature. Bioengineered. doi:10.1080/21655979.2014.1004019.
Chen, H., & Boutros, P. (2011). VennDiagram: a package for the generation of highly-customizable Venn and Euler diagrams in R. BMC Bioinformatics, 12(1), 35.
Clarke, T., Garb, J., Hayashi, C., Haney, R., Lancaster, A., Corbett, S., et al. (2014). Multi-tissue transcriptomics of the black widow spider reveals expansions, co-options, and functional processes of the silk gland gene toolkit. BMC Genomics, 15(1), 365.
Colbourne, J. K., Pfrender, M. E., Gilbert, D., Thomas, W. K., Tucker, A., Oakley, T. H., et al. (2011). The ecoresponsive genome of daphnia pulex. Science, 331(6017), 555–561. doi:10.1126/science.1197761.
Consortium, i. K. (2013). The i5K initiative: advancing arthropod genomics for knowledge, human health, agriculture, and the environment. Journal of Heredity, 104(5), 595–600. doi:10.1093/jhered/est050.
Crawford, A. C., Kricker, J. A., Anderson, A. J., Richardson, N. R., & Mather, P. B. (2004). Structure and function of a cellulase gene in redclaw crayfish, Cherax quadricarinatus. Gene, 340(2), 267–274. doi:10.1016/j.gene.2004.06.060.
Criscuolo, A., & Gribaldo, S. (2010). BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evolutionary Biology, 10(1), 210.
Dammannagoda, L. K., Pavasovic, A., Prentis, P. J., Hurwood, D. A., & Mather, P. B. (2015). Expression and characterization of digestive enzyme genes from hepatopancreatic transcripts from redclaw crayfish (Cherax quadricarinatus). Aquaculture Nutrition. doi:10.1111/anu.12211.
Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2011). ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics, 27(8), 1164–1165. doi:10.1093/bioinformatics/btr088.
Davidson, N., & Oshlack, A. (2014). Corset: enabling differential gene expression analysis for de novo assembled transcriptomes. Genome Biology, 15(7), 410.
Davison, A., & Blaxter, M. (2005). Ancient origin of glycosyl hydrolase family 9 cellulase genes. Molecular Biology and Evolution, 22(5), 1273–1284. doi:10.1093/molbev/msi107.
Eaton, D. A. R., & Ree, R. H. (2013). Inferring phylogeny and introgression using RADseq data: an example from flowering plants (Pedicularis: Orobanchaceae). Systematic Biology, 62(5), 689–706. doi:10.1093/sysbio/syt032.
Fang, D., Wang, Q., Wang, J., He, L., Liu, L., & Wang, Y. (2011). A novel DDX5 gene in the freshwater crayfish Cherax quadricarinatus is highly expressed during ontogenesis and spermatogenesis. Genetics and Molecular Research, 10(4), 3963–3975.
Fernández, M. S., Bustos, C., Luquet, G., Saez, D., Neira-Carrillo, A., Corneillat, M., et al. (2012). Proteoglycan occurrence in Gastrolith of the crayfish Cherax quadricarinatus (Malacostraca: Decapoda). Journal of Crustacean Biology, 32(5), 802–815. doi:10.1163/193724012x649804.
Fisher, S. G., & Likens, G. E. (1973). Energy flow in bear brook, New Hampshire: an integrative approach to stream ecosystem metabolism. Ecological Monographs, 43(4), 421–439. doi:10.2307/1942301.
Gan, H. M., Tan, M. H., & Austin, C. M. (2014). The complete mitogenome of the red claw crayfish Cherax quadricarinatus (Von Martens, 1868) (Crustacea: Decapoda: Parastacidae). Mitochondrial DNA, 0(0), 1–2, doi:doi:10.3109/19401736.2014.895997.
Glazer, L., Tom, M., Weil, S., Roth, Z., Khalaila, I., Mittelman, B., et al. (2013). Hemocyanin with phenoloxidase activity in the chitin matrix of the crayfish gastrolith. The Journal of Experimental Biology, 216(10), 1898–1904. doi:10.1242/jeb.080945.
Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J. Z., Thompson, D. A., Amit, I., et al. (2011). Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology, 29(7), 644–652. doi:10.1038/nbt.1883. http://www.nature.com/nbt/journal/v29/n7/abs/nbt.1883.html#supplementary-information .
Guindon, S., & Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52(5), 696–704. doi:10.1080/10635150390235520.
Hayakijkosol, O., La Fauce, K., & Owens, L. (2011). Experimental infection of redclaw crayfish (Cherax quadricarinatus) with Macrobrachium rosenbergii nodavirus, the aetiological agent of white tail disease. Aquaculture, 319(1–2), 25–29. doi:10.1016/j.aquaculture.2011.06.023.
Hayward, A., Cornwallis, C. K., & Jern, P. (2015). Pan-vertebrate comparative genomics unmasks retrovirus macroevolution. Proceedings of the National Academy of Sciences, 112(2), 464–469. doi:10.1073/pnas.1414980112.
Huang, Q.-S., Yan, J.-H., Tang, J.-Y., Tao, Y.-M., Xie, X.-L., Wang, Y., et al. (2010). Cloning and tissue expressions of seven chitinase family genes in Litopenaeus vannamei. Fish & Shellfish Immunology, 29(1), 75–81. doi:10.1016/j.fsi.2010.02.014.
Huner, J. V. (1994). Freshwater crayfish aquaculture in North America, Europe, and Australia: Families Astacidae, Cambaridae, and Parastacidae. New York: Food products press.
James, J., Slater, F. M., Vaughan, I. P., Young, K. A., & Cable, J. (2014). Comparing the ecological impacts of native and invasive crayfish: could native species’ translocation do more harm than good? Oecologia, 1–8, doi:10.1007/s00442-014-3195-0.
Jarvis, E. D., Mirarab, S., Aberer, A. J., Li, B., Houde, P., Li, C., et al. (2014). Whole-genome analyses resolve early branches in the tree of life of modern birds. Science, 346(6215), 1320–1331. doi:10.1126/science.1253451.
Johnston, K., Robson, B. J., & Fairweather, P. G. (2011). Trophic positions of omnivores are not always flexible: evidence from four species of freshwater crayfish. Austral Ecology, 36(3), 269–279. doi:10.1111/j.1442-9993.2010.02147.x.
Jones, P., Binns, D., Chang, H.-Y., Fraser, M., Li, W., McAnulla, C., et al. (2014). InterProScan 5: genome-scale protein function classification. Bioinformatics, 30(9), 1236–1240. doi:10.1093/bioinformatics/btu031.
Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30(4), 772–780. doi:10.1093/molbev/mst010.
Kolde, R. (2012). pheatmap: Pretty heatmaps. R package version 0.6, 1.
Langmead, B., & Salzberg, S. L. (2012). Fast gapped-read alignment with Bowtie 2. [Brief Communication]. Nature Methods, 9(4), 357–359. doi:10.1038/nmeth.1923. http://www.nature.com/nmeth/journal/v9/n4/abs/nmeth.1923.html#supplementary-information .
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(3), R25.
Larson, E. R., & Olden, J. D. (2012). Using avatar species to model the potential distribution of emerging invaders. Global Ecology and Biogeography, 21(11), 1114–1125. doi:10.1111/j.1466-8238.2012.00758.x.
Li, B., & Dewey, C. (2011). RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics, 12(1), 323.
Li, W., Jaroszewski, L., & Godzik, A. (2001). Clustering of highly homologous sequences to reduce the size of large protein databases. Bioinformatics, 17(3), 282–283. doi:10.1093/bioinformatics/17.3.282.
Linton, S. M., Greenaway, P., & Towle, D. (2006). Endogenous production of endo-β-1,4-glucanase by decapod crustaceans. Journal of Comparative Physiology B, 176(4), 339–348. doi:10.1007/s00360-005-0056-5.
Linton, S. M., Cameron, M. S., Gray, M. C., Donald, J. A., Saborowski, R., von Bergen, M., et al. (2015). A glycosyl hydrolase family 16 gene is responsible for the endogenous production of β-1,3-glucanases within decapod crustaceans. Gene, 569(2), 203–217. doi:10.1016/j.gene.2015.05.056.
Liu, H. P., Chen, R. Y., Zhang, Q. X., Peng, H., & Wang, K.-J. (2011). Differential gene expression profile from haematopoietic tissue stem cells of red claw crayfish, Cherax quadricarinatus, in response to WSSV infection. Developmental & Comparative Immunology, 35(7), 716–724. doi:10.1016/j.dci.2011.02.015.
Lodge, D. M., Deines, A., Gherardi, F., Yeo, D. C. J., Arcella, T., Baldridge, A. K., et al. (2012). Global introductions of crayfishes: evaluating the impact of species invasions on ecosystem services. Annual Review of Ecology, Evolution, and Systematics, 43(1), 449–472. doi:10.1146/annurev-ecolsys-111511-103919.
Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P. M., & Henrissat, B. (2014). The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Research, 42(D1), D490–D495. doi:10.1093/nar/gkt1178.
Lv, J., Liu, P., Wang, Y., Gao, B., Chen, P., & Li, J. (2013). Transcriptome analysis of Portunus trituberculatus in response to salinity stress provides insights into the molecular basis of osmoregulation. PLoS ONE, 8(12), e82155. doi:10.1371/journal.pone.0082155.
Ma, H., Ma, C., Li, S., Jiang, W., Li, X., Liu, Y., et al. (2014). Transcriptome analysis of the mud crab (Scylla paramamosain) by 454 deep sequencing: assembly, annotation, and marker discovery. PLoS ONE, 9(7), e102668. doi:10.1371/journal.pone.0102668.
Martin, A. J., Rich, T. H., Poore, G. C. B., Schultz, M. B., Austin, C. M., Kool, L., et al. (2008). Fossil evidence in Australia for oldest known freshwater crayfish of Gondwana. Gondwana Research, 14(3), 287–296. doi:10.1016/j.gr.2008.01.002.
McCormack, J. E., Harvey, M. G., Faircloth, B. C., Crawford, N. G., Glenn, T. C., & Brumfield, R. T. (2013). A phylogeny of birds based on over 1,500 loci collected by target enrichment and high-throughput sequencing. PLoS ONE, 8(1), e54848. doi:10.1371/journal.pone.0054848.
Mitchell, B. D., Anderson, T., De Silva, S. S., Collins, R. O., Chavez, J. R., Jones, P. L., et al. (1995). A conceptual production model for freshwater crayfish pond culture incorporating detrital forage. Aquaculture Research, 26(2), 117–127. doi:10.1111/j.1365-2109.1995.tb00891.x.
Momot, W. T. (1995). Redefining the role of crayfish in aquatic ecosystems. Reviews in Fisheries Science, 3(1), 33–63. doi:10.1080/10641269509388566.
Muhire, B. M., Varsani, A., & Martin, D. P. (2014). SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS ONE, 9(9), e108277. doi:10.1371/journal.pone.0108277.
Nguyen, K. Y., Sakuna, K., Kinobe, R., & Owens, L. (2014). Ivermectin blocks the nuclear location signal of parvoviruses in crayfish, Cherax quadricarinatus. Aquaculture, 420–421, 288–294. doi:10.1016/j.aquaculture.2013.11.022.
Nyström, P. E. R., Brönmark, C., & Granéli, W. (1996). Patterns in benthic food webs: a role for omnivorous crayfish? Freshwater Biology, 36(3), 631–646. doi:10.1046/j.1365-2427.1996.d01-528.x.
Oakley, T. H., Wolfe, J. M., Lindgren, A. R., & Zaharoff, A. K. (2013). Phylotranscriptomics to bring the understudied into the fold: monophyletic ostracoda, fossil placement, and pancrustacean phylogeny. Molecular Biology and Evolution, 30(1), 215–233. doi:10.1093/molbev/mss216.
Ong, S.-S., Bhassu, S., Kwong, Q. B., Mather, P., Simarani, K., & Othman, R. Y. (2015). Identification of a putative cellulase gene in the giant freshwater prawn, Macrobrachium rosenbergii (De Man, 1879). Aquaculture Research. doi:10.1111/are.12818.
Pallavicini, A., Canapa, A., Barucca, M., Alfoldi, J., Biscotti, M., Buonocore, F., et al. (2013). Analysis of the transcriptome of the Indonesian coelacanth Latimeria menadoensis. BMC Genomics, 14(1), 538.
Pamuru, R. R., Rosen, O., Manor, R., Chung, J. S., Zmora, N., Glazer, L., et al. (2012). Stimulation of molt by RNA interference of the molt-inhibiting hormone in the crayfish Cherax quadricarinatus. General and Comparative Endocrinology, 178(2), 227–236. doi:10.1016/j.ygcen.2012.05.007.
Parkyn, S. M., Collier, K. J., & Hicks, B. J. (2001). New Zealand stream crayfish: functional omnivores but trophic predators? Freshwater Biology, 46(5), 641–652. doi:10.1046/j.1365-2427.2001.00702.x.
Parra, G., Bradnam, K., & Korf, I. (2007). CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics, 23(9), 1061–1067. doi:10.1093/bioinformatics/btm071.
Peng, Y., Leung, H. C. M., Yiu, S.-M., Lv, M.-J., Zhu, X.-G., & Chin, F. Y. L. (2013). IDBA-tran: a more robust de novo de Bruijn graph assembler for transcriptomes with uneven expression levels. Bioinformatics, 29(13), i326–i334. doi:10.1093/bioinformatics/btt219.
Porter, M. L., Pérez-Losada, M., & Crandall, K. A. (2005). Model-based multi-locus estimation of decapod phylogeny and divergence times. Molecular Phylogenetics and Evolution, 37(2), 355–369. doi:10.1016/j.ympev.2005.06.021.
Price, M. N., Dehal, P. S., & Arkin, A. P. (2010). FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS ONE, 5(3), e9490. doi:10.1371/journal.pone.0009490.
Richman, N. I., Böhm, M., Adams, S. B., Alvarez, F., Bergey, E. A., Bunn, J. J. S., et al. (2015). Multiple drivers of decline in the global status of freshwater crayfish (Decapoda: Astacidea). Philosophical Transactions of the Royal Society, B: Biological Sciences, 370(1662), 20140060. doi:10.1098/rstb.2014.0060.
Roth, B. M., Hein, C. L., & Vander Zanden, M. J. (2006). Using bioenergetics and stable isotopes to assess the trophic role of rusty crayfish (Orconectes rusticus) in lake littoral zones. Canadian Journal of Fisheries and Aquatic Sciences, 63(2), 335–344. doi:10.1139/f05-217.
Rubin, C.-J., Megens, H.-J., Barrio, A. M., Maqbool, K., Sayyab, S., Schwochow, D., et al. (2012). Strong signatures of selection in the domestic pig genome. Proceedings of the National Academy of Sciences, 109(48), 19529–19536. doi:10.1073/pnas.1217149109.
Sagi, A., & Khalaila, I. (2001). The Crustacean androgen: a hormone in an isopod and androgenic activity in decapods. American Zoologist, 41(3), 477–484. doi:10.1093/icb/41.3.477.
Sahoo, P. K., Kar, B., Mohapatra, A., & Mohanty, J. (2013). De novo whole transcriptome analysis of the fish louse, Argulus siamensis: first molecular insights into characterization of Toll downstream signalling molecules of crustaceans. Experimental Parasitology, 135(3), 629–641. doi:10.1016/j.exppara.2013.09.018.
Salame, M. J., & Rouse, D. B. (2000). Forage-based feeding in commercial red claw ponds in Ecuador. Journal of Applied Aquaculture, 10(3), 83–90. doi:10.1300/J028v10n03_07.
Saoud, I. P., Ghanawi, J., Thompson, K. R., & Webster, C. D. (2013). A review of the culture and diseases of Redclaw crayfish Cherax quadricarinatus (Von Martens 1868). Journal of the World Aquaculture Society, 44(1), 1–29. doi:10.1111/jwas.12011.
Scientists G. C.o. (2014). The Global Invertebrate Genomics Alliance (GIGA): developing community resources to study diverse invertebrate genomes. Journal of Heredity, 105(1), 1–18. doi:10.1093/jhered/est084.
Shechter, A., Aflalo, E. D., Davis, C., & Sagi, A. (2005). Expression of the reproductive female-specific vitellogenin gene in endocrinologically induced male and intersex Cherax quadricarinatus crayfish. Biology of Reproduction, 73(1), 72–79. doi:10.1095/biolreprod.104.038554.
Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22(21), 2688–2690. doi:10.1093/bioinformatics/btl446.
Tan, S. H., Degnan, B. M., & Lehnert, S. A. (2000). The Penaeus monodon Chitinase 1 gene is differentially expressed in the Hepatopancreas during the molt cycle. Marine Biotechnology, 2(2), 126–135. doi:10.1007/s101269900016.
Tank, J. L., Rosi-Marshall, E. J., Griffiths, N. A., Entrekin, S. A., & Stephen, M. L. (2010). A review of allochthonous organic matter dynamics and metabolism in streams. Journal of the North American Benthological Society, 29(1), 118–146. doi:10.1899/08-170.1.
Toon, A., Pérez-Losada, M., Schweitzer, C. E., Feldmann, R. M., Carlson, M., & Crandall, K. A. (2010). Gondwanan radiation of the Southern Hemisphere crayfishes (Decapoda: Parastacidae): evidence from fossils and molecules. Journal of Biogeography, 37(12), 2275–2290. doi:10.1111/j.1365-2699.2010.02374.x.
Vannote, R. L., Minshall, G. W., Cummins, K. W., Sedell, J. R., & Cushing, C. E. (1980). The river continuum concept. Canadian Journal of Fisheries and Aquatic Sciences, 37(1), 130–137. doi:10.1139/f80-017.
Ward, L. D., & Kellis, M. (2012). Evidence of abundant purifying selection in humans for recently acquired regulatory functions. Science, 337(6102), 1675–1678. doi:10.1126/science.1225057.
Weinländer, M., & Füreder, L. (2011). Crayfish as trophic agents: effect of Austropotamobius torrentium on zoobenthos structure and function in small forest streams. Knowledge and Management of Aquatic Ecosystems, 401.
Whitledge, G. W., & Rabeni, C. F. (1997). Energy sources and ecological role of crayfishes in an Ozark stream: insights from stable isotopes and gut analysis. Canadian Journal of Fisheries and Aquatic Sciences, 54(11), 2555–2563. doi:10.1139/f97-173.
Yang, Y., & Smith, S. A. (2014). Orthology inference in non-model organisms using transcriptomes and low-coverage genomes: improving accuracy and matrix occupancy for phylogenomics. Molecular Biology and Evolution. doi:10.1093/molbev/msu245.
Yin, Y., Mao, X., Yang, J., Chen, X., Mao, F., & Xu, Y. (2012). dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Research, 40(Web Server issue), W445–W451. doi:10.1093/nar/gks479.
You, X., Bian, C., Zan, Q., Xu, X., Liu, X., Chen, J., et al. (2014). Mudskipper genomes provide insights into the terrestrial adaptation of amphibious fishes. [Article]. Nat Commun, 5, doi:10.1038/ncomms6594.
Yudkovski, Y., Glazer, L., Shechter, A., Reinhardt, R., Chalifa-Caspi, V., Sagi, A., et al. (2010). Multi-transcript expression patterns in the gastrolith disk and the hypodermis of the crayfish Cherax quadricarinatus at premolt. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, 5(2), 171–177. doi:10.1016/j.cbd.2010.03.010.
Zhang, S., Jiang, S., Xiong, Y., Fu, H., Sun, S., Qiao, H., et al. (2014). Six chitinases from oriental river prawn Macrobrachium nipponense: cDNA characterization, classification and mRNA expression during post-embryonic development and moulting cycle. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 167, 30–40. doi:10.1016/j.cbpb.2013.09.009.
Zhernakova, A., Elbers, C. C., Ferwerda, B., Romanos, J., Trynka, G., Dubois, P. C., et al. (2010). Evolutionary and functional analysis of celiac risk loci reveals SH2B3 as a protective factor against bacterial infection. The American Journal of Human Genetics, 86(6), 970–977. doi:10.1016/j.ajhg.2010.05.004.
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Funding for this study was provided by the Monash University Malaysia (MUM) Tropical Medicine and Biology Multidisciplinary Platform.
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HMG and CMA conceived and designed the study. HMG, HYG, and YPL performed the sequencing of transcriptomes, and MHT analyzed the data. MHT, HMG, CMA, LJC, MBS, and ADM discussed the results and wrote the manuscript. All authors read and approved the final manuscript.
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Tan, M.H., Gan, H.M., Gan, H.Y. et al. First comprehensive multi-tissue transcriptome of Cherax quadricarinatus (Decapoda: Parastacidae) reveals unexpected diversity of endogenous cellulase. Org Divers Evol 16, 185–200 (2016). https://doi.org/10.1007/s13127-015-0237-3
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DOI: https://doi.org/10.1007/s13127-015-0237-3