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Allelically and Differentially Expressed Genes After Infection of Edwardsiella ictaluri in Channel Catfish as Determined by Bulk Segregant RNA-Seq

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Abstract

Identification of genetic markers associated with resistance against enteric septicemia of catfish (ESC) is of great interest for genetic enhancement programs of catfish. In the present study, bulk segregant RNA-Seq analysis was applied to determine differentially expressed genes and alleles after ESC infection. Here we report three genomic regions on LG1, LG12, and LG26, containing significant single-nucleotide polymorphisms (SNPs). These genomic regions aligned well with quantitative trait loci (QTL) previously identified. Within the QTL regions, eleven genes were found to be differentially regulated between phenotypic bulks. Importantly, the QTL on linkage group 1 (LG1) were found to be expressed in the liver, whereas the QTL on LG12 and LG26 were expressed in the intestine, suggesting multiple mechanisms of ESC resistance. It is apparent that apolipoproteins may be important for ESC resistance as the QTL on LG1 included the 14-kDa apolipoprotein genes that are both allelically expressed and differentially expressed between the resistant and susceptible bulks. Traf2 and NCK-interacting protein kinase (TNIK) were found in the QTL on LG12, and it was downregulated in resistant fish, suggesting the importance of NCK downregulation in ESC resistance, as previously reported. In addition, we observed divergent gene expression patterns between the liver and intestine after infection. Immune/inflammatory-related processes were overrepresented from liver DEGs, while those DEGs identified from intestine were enriched for proteolysis and wounding processes. Taken together, the BSR-Seq analysis presented here advanced the knowledge of ESC resistance, providing information of not only positions of QTL but also genes and their differential expression between resistant and susceptible fish, making it one step closer to the identification of the causal genes for ESC resistance.

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References

  • Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc 

  • Anttila K, Dhillon RS, Boulding EG, Farrell AP, Glebe BD, Elliott JA, Wolters WR, Schulte PM (2013) Variation in temperature tolerance among families of Atlantic salmon (Salmo salar) is associated with hypoxia tolerance, ventricle size and myoglobin level. J Exp Biol 216:1183–1190

    CAS  PubMed  Google Scholar 

  • Bebak J, Wagner B (2012) Use of vaccination against enteric septicemia of catfish and columnaris disease by the US catfish industry. J Aquat Anim Health 24:30–36

    CAS  PubMed  Google Scholar 

  • Berbee JF, Havekes LM, Rensen PC (2005) Apolipoproteins modulate the inflammatory response to lipopolysaccharide. J Endotoxin Res 11:97–103

    CAS  PubMed  Google Scholar 

  • Concha MI, Smith VJ, Castro K, Bastías A, Romero A, Amthauer RJ (2004) Apolipoproteins AI and AII are potentially important effectors of innate immunity in the teleost fish Cyprinus carpio. FEBS J 271:2984–2990

    CAS  Google Scholar 

  • Dai P, Kong J, Wang S, Lu X, Luo K, Cao BX, Meng XH, Luan S (2018) Identification of SNPs associated with residual feed intake from the muscle of Litopenaeus vannamei using bulk segregant RNA-seq. Aquaculture 497:56–63

    CAS  Google Scholar 

  • Damås JK, Smith C, Øie E, Fevang B, Halvorsen B, Wæhre T, Boullier A, Breland U, Yndestad A, Ovchinnikova O (2007) Enhanced expression of the homeostatic chemokines CCL19 and CCL21 in clinical and experimental atherosclerosis: possible pathogenic role in plaque destabilization. Arterioscler Thromb Vasc Biol 27:614–620

    PubMed  Google Scholar 

  • Dunham RA, Elaswad A (2017) Catfish biology and farming. Annu Rev Anim Biosci 6:305–325

    PubMed  Google Scholar 

  • Geng X, Jiang C, Yang J, Wang L, Wu X, Wei W (2016) Rapid identification of candidate genes for seed weight using the SLAF-Seq method in Brassica napus. PLoS One 11:e0147580

  • Gomez D, Sunyer JO, Salinas I (2013) The mucosal immune system of fish: the evolution of tolerating commensals while fighting pathogens. Fish Shellfish Immunol 35:1729–1739

    CAS  PubMed  PubMed Central  Google Scholar 

  • Griffin B, Mitchell A (2007) Susceptibility of channel catfish, Ictalurus punctatus (Rafinesque), to Edwardsiella ictaluri challenge following copper sulphate exposure. J Fish Dis 30:581–585

    CAS  PubMed  Google Scholar 

  • Heymann F, Tacke F (2016) Immunology in the liver-from homeostasis to disease. Nat Rev Gastroenterol Hepatol 13:88–110

    CAS  PubMed  Google Scholar 

  • Hill JT, Demarest BL, Bisgrove BW, Gorsi B, Su YC, Yost HJ (2013) MMAPPR: mutation mapping analysis pipeline for pooled RNA-seq. Genome Res 23:687–697

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jia QJ, Wang JM, Zhu JH, Hua W, Shang Y, Yang JM, Liang ZS (2017) Toward identification of black lemma and pericarp gene Blp1 in barley combining bulked segregant analysis and specific-locus amplified fragment sequencing. Front Plant Sci 8:1414

    PubMed  PubMed Central  Google Scholar 

  • Johnston LD, Brown G, Gauthier D, Reece K, Kator H, Van Veld P (2008) Apolipoprotein AI from striped bass (Morone saxatilis) demonstrates antibacterial activity in vitro. Comp Biochem Physiol B Biochem Mol Biol 151:167–175

    PubMed  Google Scholar 

  • Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:1–13

    Google Scholar 

  • Kireeva ML, Mo FE, Yang GP, Lau LF (1996) Cyr61, a product of a growth factor-inducible immediate-early gene, promotes cell proliferation, migration, and adhesion. Mol Cell Biol 16:1326–1334

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kofler R, Pandey RV, Schlötterer C (2011) PoPoolation2: identifying differentiation between populations using sequencing of pooled DNA samples (Pool-Seq). Bioinform 27:3435–3436

    CAS  Google Scholar 

  • Lee KJ, Lim D, Yoo YH, Park EJ, Lee SH, Yadav BK, Lee YK, Park JH, Kim D, Park KH (2016) Paired Ig-like type 2 receptor-derived agonist ligands ameliorate inflammatory reactions by downregulating β1 integrin activity. Mol Cells 39:557

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li C, Zhang Y, Wang R, Lu J, Nandi S, Mohanty S, Terhune J, Liu ZJ, Peatman E (2012) RNA-seq analysis of mucosal immune responses reveals signatures of intestinal barrier disruption and pathogen entry following Edwardsiella ictaluri infection in channel catfish, Ictalurus punctatus. Fish Shellfish Immunol 32:816–827

    CAS  PubMed  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinform 25:2078–2079

    Google Scholar 

  • Li MM, Li BB, Guo GH, Chen YX, Xie JZ, Lu P, Wu QH, Zhang DY, Zhang HZ, Yang J, Zhang PP, Zhang Y, Liu ZY (2018) Mapping a leaf senescence gene els1 by BSR-Seq in common wheat. Crop J 6:236–243

    Google Scholar 

  • Li Y, Liu S, Qin Z, Waldbieser GC, Wang R, Sun L, Bao L, Danzmann RG, Dunham RA, Liu ZJ (2015) Construction of a high-density, high-resolution genetic map and its integration with BAC-based physical map in channel catfish. DNA Res 22:39–52

    PubMed  Google Scholar 

  • Li Y, Shi X, Hu J, Wu P, Qiu D, Qu Y, Xie J, Wu Q, Zhang H, Yang L, Liu H, Zhou Y, Liu Z, Li H (2020) Identification of a recessive gene PmQ conferring resistance to powdery mildew in wheat landrace Qingxinmai using BSR-Seq analysis. Plant Dis 104:743–751

    CAS  PubMed  Google Scholar 

  • Lin M, Sun S, Fang J, Qi X, Sun L, Zhong Y, Sun Y, Hong G, Wang R, Li Y (2021) BSR-Seq analysis provides insights into the cold stress response of Actinidia arguta F1 populations. BMC Genom 22:1–13

    Google Scholar 

  • Liu S, Yeh CT, Tang HM, Nettleton D, Schnable PS (2012) Gene mapping via bulked segregant RNA-Seq (BSR-Seq). PloS One 7:e36406

  • Liu ZJ, Liu S, Yao J, Bao L, Zhang J, Li Y, Jiang C, Sun L, Wang R, Zhang Y, Zhou T, Zeng Q, Fu Q, Gao S, Li N, Koren S, Jiang Y, Zimin A, Xu P, Phillippy AM, Geng X, Song L, Sun F, Li C, Wang X, Chen A, Jin Y, Yuan Z, Yang Y, Tan S, Peatman E, Lu J, Qin Z, Dunham RA, Li Z, Sonstegard T, Feng J, Danzmann RG, Schroeder S, Scheffler B, Duke MV, Ballard L, Kucuktas H, Kaltenboeck L, Liu H, Armbruster J, Xie Y, Kirby ML, Tian Y, Flanagan ME, Mu W, Waldbieser GC (2016) The channel catfish genome sequence provides insights into the evolution of scale formation in teleosts. Nat Commun 7:11757

    CAS  PubMed  PubMed Central  Google Scholar 

  • Marsland BJ, Bättig P, Bauer M, Ruedl C, Lässing U, Beerli RR, Dietmeier K, Ivanova L, Pfister T, Vogt L (2005) CCL19 and CCL21 induce a potent proinflammatory differentiation program in licensed dendritic cells. Immunity 22:493–505

    CAS  PubMed  Google Scholar 

  • Martin SA, Douglas A, Houlihan DF, Secombes CJ (2010) Starvation alters the liver transcriptome of the innate immune response in Atlantic salmon (Salmo salar). BMC Genom 11:1–20

    Google Scholar 

  • Martin SA, Blaney SC, Houlihan D, Secombes CJ (2006) Transcriptome response following administration of a live bacterial vaccine in Atlantic salmon (Salmo salar). Mol Immunol 43:1900–1911

    CAS  PubMed  Google Scholar 

  • Michelmore RW, Paran I, Kesseli R (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. PNAS USA 88:9828–9832

    CAS  PubMed  PubMed Central  Google Scholar 

  • Miller AC, Obholzer ND, Shah AN, Megason SG, Moens CB (2013) RNA-seq based mapping and candidate identification of mutations from forward genetic screens. Genome Res 23:679–686

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ourth DD, Chung KT (2004) Purification of antimicrobial factor from granules of channel catfish peripheral blood leucocytes. Biochem Biophys Res Commun 313:28–36

    CAS  PubMed  Google Scholar 

  • Peatman E, Baoprasertkul P, Terhune J, Xu P, Nandi S, Kucuktas H, Li P, Wang S, Somridhivej B, Dunham RA, Liu ZJ (2007) Expression analysis of the acute phase response in channel catfish (Ictalurus punctatus) after infection with a Gram-negative bacterium. Dev Comp Immunol 31:1183–1196

    CAS  PubMed  Google Scholar 

  • Pirillo A, Catapano AL, Norata GD (2015) HDL in infectious diseases and sepsis. In: von Eckardstein A, Kardassis D (eds) High density lipoproteins. Springer, Cham

  • Pruitt KD, Tatusova T, Maglott DR (2005) NCBI Reference Sequence (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 33:501–504

    Google Scholar 

  • Purcell MK, Marjara IS, Batts W, Kurath G, Hansen JD (2011) Transcriptome analysis of rainbow trout infected with high and low virulence strains of infectious hematopoietic necrosis virus. Fish Shellfish Immunol 30:84–93

    CAS  PubMed  Google Scholar 

  • Ramirez-Gonzalez RH, Segovia V, Bird N, Fenwick P, Holdgate S, Berry S, Jack P, Caccamo M, Uauy C (2015) RNA-Seq bulked segregant analysis enables the identification of high-resolution genetic markers for breeding in hexaploid wheat. Plant Biotechnol J 13:613–624

    CAS  PubMed  Google Scholar 

  • Sakamoto S, Yokoyama M, Aoki M, Suzuki K, Kakehi Y, Saito Y (2004) Induction and function of CYR61 (CCN1) in prostatic stromal and epithelial cells: CYR61 is required for prostatic cell proliferation. Prostate 61:305–317

    CAS  PubMed  Google Scholar 

  • Schneeberger K (2014) Using next-generation sequencing to isolate mutant genes from forward genetic screens. Nat Rev Genet 15:662–676

    CAS  PubMed  Google Scholar 

  • Shi H, Zhou T, Wang X, Yang Y, Wu C, Liu S, Bao L, Li N, Yuan Z, Jin Y, Tan S, Wang W, Zhong X, Qin G, Gao D, Dunham RA, Liu ZJ (2018) Genome-wide association analysis of intra-specific QTL associated with the resistance for enteric septicemia of catfish. Mol Gen Genomics 293:1365–1378

    CAS  Google Scholar 

  • Shi X, Wu P, Hu J, Qiu D, Qu Y, Li Y, Liu Y, Gebremariam TG, Xie J, Wu Q (2021) Molecular characterization of adult plant resistance loci against powdery mildew in winter wheat cultivar Liangxing 99 using BSR-Seq technology. Plant Dis. https://doi.org/10.1094/PDIS-03-21-0664-RE

    Article  PubMed  Google Scholar 

  • Small BC, Murdock CA, Bilodeau-Bourgeois AL, Peterson BC, Waldbieser GC (2008) Stability of reference genes for real-time PCR analyses in channel catfish (Ictalurus punctatus) tissues under varying physiological conditions. Comp Biochem Physiol B Biochem Mol Biol 151:296–304

    PubMed  Google Scholar 

  • Song X, Hu X, Sun B, Bo Y, Wu K, Xiao L, Gong C (2017) A transcriptome analysis focusing on inflammation-related genes of grass carp intestines following infection with Aeromonas hydrophila. Sci Rep 7:1–12

    Google Scholar 

  • Stanke M, Morgenstern B (2005) AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Res 33:465–467

    Google Scholar 

  • Su A, Song W, Xing J, Zhao Y, Zhang R, Li C, Duan M, Luo M, Shi Z, Zhao J (2016) Identification of genes potentially associated with the fertility instability of S-type cytoplasmic male sterility in maize via bulked segregant RNA-Seq. PLoS One 11:e0163489

  • Sun L, Tang H, Men X, Zhang Q, Sun X, Xing S (2019) RNA-seq and bulked segregant analysis of genes related to high growth in Ginkgo biloba half-sibling families. Am J Plant Sci 10:79–100

    CAS  Google Scholar 

  • Suzuki J, Denning DP, Imanishi E, Horvitz HR, Nagata S (2013) Xk-related protein 8 and CED-8 promote phosphatidylserine exposure in apoptotic cells. Science 341:403–406

    CAS  PubMed  Google Scholar 

  • Suzuki J, Imanishi E, Nagata S (2016) Xkr8 phospholipid scrambling complex in apoptotic phosphatidylserine exposure. PNAS USA 113:9509–9514

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tan S, Zhou T, Wang W, Jin Y, Wang X, Geng X, Luo J, Yuan Z, Yang Y, Shi H, Gao D, Dunham RA, Liu ZJ (2018) GWAS analysis using F2 interspecific hybrids reveals superior blue catfish alleles responsible for strong resistance against enteric septicemia of catfish. Mol Gen Genomics 293:1107–1120

    CAS  Google Scholar 

  • Tang HX, Li JH, Xing SY, Du SH, Wang ZT, Liu XJ, Sun LM (2015) RNA-seq and bulked segregant analysis of a gene related to high growth in Ginkgo biloba half-siblings. bioRxiv:034272

  • Torralba D, Baixauli F, Villarroya-Beltri C, Fernández-Delgado I, Latorre-Pellicer A, Acín-Pérez R, Martín-Cófreces NB, Jaso-Tamame ÁL, Iborra S, Jorge I (2018) Priming of dendritic cells by DNA-containing extracellular vesicles from activated T cells through antigen-driven contacts. Nat Commun 9:2658

    PubMed  PubMed Central  Google Scholar 

  • Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tucker CS, Hargreaves JA (2004) Biology and culture of channel catfish. Elsevier, London

    Google Scholar 

  • Turner SD (2014) qqman: an R package for visualizing GWAS results using QQ and manhattan plots. bioRxiv:005165

  • Villarroel F, Bastías A, Casado A, Amthauer R, Concha MI (2007) Apolipoprotein AI, an antimicrobial protein in Oncorhynchus mykiss: evaluation of its expression in primary defence barriers and plasma levels in sick and healthy fish. Fish Shellfish Immunol 23:197–209

    CAS  PubMed  Google Scholar 

  • Vinogradov E, Nossova L, Perry MB, Kay WW (2005) The structure of the antigenic O-polysaccharide of the lipopolysaccharide of Edwardsiella ictaluri strain MT104. Carbohydr Res 340:1509–1513

    CAS  PubMed  Google Scholar 

  • Wang R, Sun L, Bao L, Zhang J, Jiang Y, Yao J, Song L, Feng J, Liu S, Liu ZJ (2013) Bulk segregant RNA-seq reveals expression and positional candidate genes and allele-specific expression for disease resistance against enteric septicemia of catfish. BMC Genom 14:1–18

    Google Scholar 

  • Wang Y, Yu Y, Li S, Zhang X, Xiang J, Li F (2020) Sex-specific transcriptome sequencing of zoea I larvae and identification of sex-linked genes using bulked segregant analysis in Pacific white shrimp Litopenaeus vannamei. Mar Biotechnol 22:423–432

    CAS  Google Scholar 

  • Wen J, Zhong H, Xiao J, Zhou Y, Chen Z, Zeng L, Chen D, Sun Y, Zhao J, Wang F (2016) A transcriptome resource for pharaoh cuttlefish (Sepia pharaonis) after ink ejection by brief pressing. Mar Genomics 28:53–56

    PubMed  Google Scholar 

  • Wolters WR, Johnson MR (1994) Enteric septicemia resistance in blue catfish and three channel catfish strains. J Aquat Anim Health 6:329–334

    Google Scholar 

  • Wolters WR, Wise DJ, Klesius PH (1996) Survival and antibody response of channel catfish, blue catfish, and channel catfish female x blue catfish male hybrids after exposure to Edwardsiella ictaluri. J Aquat Anim Health 8:249–254

    Google Scholar 

  • Wu N, Song YL, Wang B, Zhang XY, Zhang XJ, Wang YL, Cheng YY, Chen DD, Xia XQ, Lu YS, Zhang YA (2016) Fish gut-liver immunity during homeostasis or inflammation revealed by integrative transcriptome and proteome studies. Sci Rep 6:1–17

    Google Scholar 

  • Wynne JW, O’sullivan MG, Cook MT, Stone G, Nowak BF, Lovell DR, Elliott NG (2008) Transcriptome analyses of amoebic gill disease-affected Atlantic salmon (Salmo salar) tissues reveal localized host gene suppression. Mar Biotechnol 10:388–403

    CAS  Google Scholar 

  • Yan W, Chen Z, Lu J, Xu C, Xie G, Li Y, Deng XW, He H, Tang X (2017) Simultaneous identification of multiple causal mutations in rice. Front Plant Sci 7:2055

    PubMed  PubMed Central  Google Scholar 

  • Yang Y, Fu Q, Zhou T, Li Y, Liu S, Zeng Q, Wang X, Jin Y, Tian C, Qin Z (2017) Analysis of apolipoprotein genes and their involvement in disease response of channel catfish after bacterial infection. Dev Comp Immunol 67:464–470

    CAS  PubMed  Google Scholar 

  • Yang Y, Yu H, Li H, Wang A (2016) Transcriptome profiling of grass carp (Ctenopharyngodon idellus) infected with Aeromonas hydrophila. Fish Shellfish Immunol 51:329–336

    PubMed  Google Scholar 

  • Yu G, Wang LG, Han Y, He QY (2012) clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS 16:284–287

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng Q, Fu Q, Li Y, Waldbieser GC, Bosworth B, Liu S, Yang Y, Bao L, Yuan Z, Li N, Liu ZJ (2017) Development of a 690 K SNP array in catfish and its application for genetic mapping and validation of the reference genome sequence. Sci Rep 7:1–14

    Google Scholar 

  • Zhou T, Liu S, Geng X, Jin Y, Jiang C, Bao L, Yao J, Zhang Y, Zhang J, Sun L, Wang X, Li N, Tan S, Liu ZJ (2017) GWAS analysis of QTL for enteric septicemia of catfish and their involved genes suggest evolutionary conservation of a molecular mechanism of disease resistance. Mol Gen Genomics 292:231–242

    CAS  Google Scholar 

  • Zhou T, Yuan Z, Tan S, Jin Y, Yang Y, Shi H, Wang W, Niu D, Gao L, Jiang W (2018) A review of molecular responses of catfish to bacterial diseases and abiotic stresses. Front physiol 9:1113

    PubMed  PubMed Central  Google Scholar 

  • Zhu J, Chao L, Ao QW, Tan Y, Luo YJ, Guo Y, Lan GQ, Jiang H, Gan X (2015) Trancriptomic profiling revealed the signatures of acute immune response in tilapia (Oreochromis niloticus) following Streptococcus iniae challenge. Fish Shellfish Immunol 46:346–353

    CAS  PubMed  Google Scholar 

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Funding

This project was supported by the USDA Agriculture and Food Research Initiative, Animal Genomics, Genetics and Breeding Program (grant number 2017-67015-26295) and Animal Reproduction Program (grant number 2019-67015-29409). Yulin Jin is supported by a scholarship from the China Scholarship Council.

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Authors and Affiliations

  1. The Fish Molecular Genetics and Biotechnology Laboratory, Aquatic Genomics Unit, School of Fisheries, Aquaculture and Aquatic Sciences, Auburn University, Auburn, AL, 36849, USA

    Yulin Jin, Tao Zhou, Wansheng Jiang, Ning Li, Xiaoyan Xu, Suxu Tan, Huitong Shi, Yujia Yang, Zihao Yuan, Wenwen Wang, Guyu Qin, Shikai Liu & Rex Dunham

  2. Department of Marine Biology & Biotechnology, College of Ocean and Earth Sciences, Xiamen University, Xiamen, China

    Tao Zhou

  3. Department of Biology, College of Arts and Sciences, Syracuse University, Syracuse, NY, 13244, USA

    Dongya Gao & Zhanjiang Liu

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  1. Yulin Jin
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Jin, Y., Zhou, T., Jiang, W. et al. Allelically and Differentially Expressed Genes After Infection of Edwardsiella ictaluri in Channel Catfish as Determined by Bulk Segregant RNA-Seq. Mar Biotechnol 24, 174–189 (2022). https://doi.org/10.1007/s10126-022-10094-3

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