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Integrative Transcriptomic Analysis Reveals the Immune bioRxiv preprint doi: https://doi.org/10.1101/2020.11.10.375915; this version posted March 28, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. [在此处键入] Integrative Transcriptomic Analysis Reveals the Immune Mechanism for A CyHV-3-Resistant Common Carp Strain 1 Zhiying Jia1,2，7†, Nan Wu3,4†, Xiaona Jiang1，7, Heng Li3,4, Jiaxin Sun1，7, Mijuan Shi3, 2 Chitao Li1，7, Xuesong Hu1，7, Yanlong Ge1，7, Weidong Ye3,4, Ying Tang3, Junwei Shan3, 5, 3 Yingyin Cheng3, Xiao-Qin Xia3,4,6*, Lianyu Shi1,7* 4 1Heilongjiang River Fisheries Research Institute, Chinese Academy of Fishery 5 Sciences, Harbin, China 6 2Key Laboratory of Aquatic Genomics, Ministry of Agriculture, Chinese Academy of 7 Fishery Sciences, Beijing, China 8 3Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, China 9 4University of Chinese Academy of Sciences, Beijing, China 10 5 College of Fisheries and Life Science, Dalian Ocean University, Dalian, China 11 6The Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing, 12 China 13 7 National and Local Joint Engineering Laboratory for Freshwater Fish Breeding, 14 Harbin, China 15 16 † Co-first author. 17 * Correspondence: 18 Lianyu Shi 19 [email protected] 20 Xiao-Qin Xia 21 [email protected] 22 Word count: 5652 23 Number of figures: 7 24 Keywords: transcriptome, lncRNA, CyHV-3, resistant immune mechanism, common 25 carp 26 bioRxiv preprint doi: https://doi.org/10.1101/2020.11.10.375915; this version posted March 28, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. CyHV-3 Resistant Immune Mechanism 27 ABSTRACT 28 Anti-disease breeding is becoming the most promising solution to cyprinid 29 herpesvirus-3 (CyHV-3) infection, the major threat to common carp aquaculture. 30 Virus challenging studies suggested that a breeding strain of common carp is resistant 31 to this disease. This study illustrates the immune mechanisms involved in anti-CyHV- 32 3 ability. An integrative analysis of the protein-coding genes and long non-coding 33 RNAs (lncRNAs) using transcriptomic data was performed. Tissues from the head 34 kidney of common carp were extracted at day 0 (the healthy control) and day 7 after 35 CyHV-3 infection (the survivors), and used to analyze the transcriptome through both 36 Illumina and PacBio sequencing. Following analysis of the GO terms and KEGG 37 pathways involved, the immune-related terms and pathways were merged. In order to 38 dig out details in the immune aspect, The DEGs were filtered using the current 39 common carp immune gene library. Immune gene categories and their corresponding 40 genes in different comparison groups were revealed. Also, the immunological Gene 41 Ontology terms for lncRNA modulation were retained. The weighted gene co- 42 expression network analysis was used to reveal the regulation of immune genes by 43 lncRNA. The results demonstrated that the breeding carp strain develops marked 44 resistance to CyHV-3 through a specific innate immune mechanism. The featured 45 biological processes were autophagy, phagocytosis, cytotoxicity, and virus blockage 46 by lectins and MUC3. Moreover, the immune suppressive signals, such as suppression 47 of IL21R on STAT3, PI3K mediated inhibition on inflammation by dopamine upon 48 infection, as well as the inhibition of NLRC3 on STING during a steady state. 49 Possible susceptible factors for CyHV-3, such as ITGB1, TLR18, and CCL4, were 50 also revealed from the non-breeding strain. The results of this study also suggested 51 that Nramp and PAI regulated by LncRNA could facilitate virus infection and 52 proliferation for infected cells respectively, while T cell leukemia homeobox 3 53 (TLX3) as well as galectin 3 function by lncRNA may play a role in the resistance 54 mechanism. Therefore, immune factors that are immunogenetically insensitive or 55 susceptible to CyHV-3 infection have been revealed. 56 57 INTRODUCTION 58 Cyprinid herpesvirus-3 (CyHV-3) infection is a major threat to common carp 59 aquaculture (1), leading to widespread mortality and substantial economic loss. 60 CyHV-3 is thought to cause death by weakening the host’s immune system, resulting 61 in susceptibility to pathogenic microbes (1). In common carp, clinical signs of the 62 disease develop rapidly and may induce morbidity and mortality within a period of 6 63 to 10 days following infection (2). 64 65 Carp that survive a primary infection with CyHV-3 can be resistant to future infection 66 with this virus. Since latency and persistent carrying of CyHV-3 exist in carp (2-4), 67 genetic backgrounds are crucial in developing an understanding resistance against the 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.11.10.375915; this version posted March 28, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. CyHV-3 Resistant Immune Mechanism 68 virus. Experimental infections of carp from pure lines or crosses have indicated the 69 existence of genetic background of resistance by divergent survival rates (2). For 70 example, a markedly higher expression of immune-related genes involved in pathogen 71 recognition, complement activation, major histocompatibility complex class I (MHC 72 I)-restricted antigen presentation, and the development of adaptive mucosal immunity 73 was noted in the more resistant R3 line. Higher activation of CD8+ T cells was also 74 observed (5). The diallelic cross of four European carp lines, including Polish ‘K’ and 75 ‘R6’, Hungarian ‘R7’ and French ‘F’ also has been down in order to select the 76 resistant fish, and then found that MH class II B genes of carp can have an effect on 77 immunity against CyHV-3 infection (6).Additionally, carp strains of Asian origin, 78 particularly Amur wild carp, were shown to be more resistant to CyHV-3 than strains 79 originating from Europe, such as the Prerov scale carp or koi carp from a breed in the 80 Czech Republic (7). 81 82 The immune response of carp to CyHV-3 involves both innate and adaptive aspects 83 with the outcome of the disease largely depending on whether the balance is tipped in 84 favor of the host’s immune response or virus’s evasion strategy (2). In general, 85 transcriptomic analysis has revealed that three immune-related pathways, namely the 86 mitogen-activated protein kinase (MAPK) signaling pathway, the innate immune 87 response, and the cytokine-mediated signaling pathway, were highly involved in the 88 infection with CyHV-3 (8). In red common carp × koi, the expression of interleukin 89 12 (IL12) p35, interferon (IFN) ɑβ, and toll-like receptor 9 (TLR9) may provide 90 potential genes related to resistance against KHV (another term for CyHV-3) (9). 91 However, the magnitude of type I IFN response did not correlate with a higher 92 resistance in CyHV-3-infected carp, during the challenge test among different strains, 93 although CyHV-3 infection can induce type I IFNs (7, 10). Regarding the innate 94 resistance in carp, the mapped CyHV-3 survival quantitative trait loci have been 95 reported mainly in IL10 and MHC II (11). Recently, by quantitative trait locus 96 mapping and genome-wide association study, tumor necrosis factor-alpha (TNFA), 97 hypoxia inducible factor 1 subunit alpha (HIF1A), galectin-8 (LGALS8), rootletin, 98 and paladin, have also been related to resistance against CyHV-3 (12). Adaptive 99 immunity through both cytotoxicity and immunoglobulin (Ig) secretion may be 100 involved in resistance. Matthew et al. revealed that, in the anterior kidney, Ig secretion 101 plays an important role in the resistance during the persistent infection or reactivation 102 phases of CyHV-3 (1). In addition, CyHV-3 profoundly influences the expression of 103 host miRNA, although the regulation of immune processes by miRNA in the clinical 104 and latent phases differs (4). This suggests an important role of non-coding RNAs in 105 anti-CyHV-3 immunity. 106 107 The first transcriptional analysis of carp anterior kidney mainly pointed out the 108 important role of humoral immune responses, especially those related to 109 immunoglobulin (1). Spleen transcriptomic analyses comparing the susceptible and 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.11.10.375915; this version posted March 28, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. CyHV-3 Resistant Immune Mechanism 110 resistant common carp revealed that the susceptible fish elicited a typical anti-viral 111 interferon response, while the upregulated IL-8 attracted innate immune cells and 112 related response may play an essential role in resistant fish (13). 113 114 German mirror carp selection G4 is a strain of common carp cultivated widely in 115 China, yet with a high mortality caused by CyHV-3 virus. Based on our previous 116 study, a strain of common carp from German mirror carp selection G4 has already 117 shown a higher survival rate after breeding for three generations. Among fish from the 118 G3 generation, 1000 individuals were genotyped by four SNP loci, including 119 carp065309, carp070076, carp183811 and carp160380, and then four main groups, 120 with genotypes of GG/GT/GG/AA, GG/TT/TT/AA, AG/TT/AG/AT and 121 GG/GG/GG/AA, whose survival rates were 89.9%, 94.7%, 88.0% and 92.7% 122 respectively, were propagated (14). While the unselected mirror carp were 62.6%.
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