意大利蜜蜂工蜂幼虫肠道发育过程中lncRNA的表达谱和调控作用

doi:10.16380/j.kcxb.2024.08.002

昆虫学报 ›› 2024, Vol. 67 ›› Issue (8): 1050-1062.doi: 10.16380/j.kcxb.2024.08.002

意大利蜜蜂工蜂幼虫肠道发育过程中lncRNA的表达谱和调控作用

赵浩东^1,#, 臧贺^1,2,3,#, 叶道有¹, 陈颖¹, 王宁¹, 吴鹰⁴, 蒋海宾⁴, 冯睿蓉⁵, 陈大福^1,2,3, 熊翠玲^1,2,3,*, 郭睿^1,2,3,*

(1. 福建农林大学蜂学与生物医药学院, 福州 350002; 2. 天然生物毒素国家地方联合工程实验室, 福州 350002; 3. 福建省蜂疗研究所, 福州 350002; 4. 吉林省养蜂科学研究所, 吉林 132000; 5. 福建农业职业技术学院, 福州 350000)

出版日期:2024-08-20 发布日期:2024-09-23

Expression profiles and regulatory roles of lncRNAs during the developmental process of the larval gut of Apis mellifera ligustica workers

ZHAO Hao-Dong^1,#, ZANG He^1,2,3,#, YE Dao-You¹, CHEN Ying¹, WANG Ning¹, WU Ying⁴, JIANG Hai-Bin⁴, FENG Rui-Rong⁵, CHEN Da-Fu ^1,2,3, XIONG Cui-Ling ^1,2,3,*, GUO Rui ^1,2,3,*

(1. College of Bee Science and Biomedicine, Fujian Agriculture and Forestry University, Fuzhou 350002, China; 2. National & Local United Engineering Laboratory of Natural Biotoxin, Fuzhou 350002, China; 3. Apicultural Research Institute of Fujian Province, Fuzhou 350002, China; 4. Apiculture Science Institute of Jilin Province, Jilin 132000, China; 5. Fujian Vocational College of Agriculture, Fuzhou 350000, China)

Online:2024-08-20 Published:2024-09-23

摘要/Abstract

摘要： 【目的】解析意大利蜜蜂Apis mellifera ligustica工蜂幼虫肠道发育过程中的长链非编码RNA(long non-coding RNA, lncRNA)差异表达谱，并揭示差异表达lncRNA(differentially expressed lncRNA, DElncRNA)在幼虫肠道发育中的调控作用。【方法】基于前期获得的意大利蜜蜂工蜂4, 5和6日龄幼虫肠道转录组数据(分别为Am4, Am5和Am6)，利用相关软件筛选Am4 vs Am5比较组和Am5 vs Am6比较组中的DElncRNA，分析DElncRNA和两个比较组中共同上调和下调lncRNA的顺式调控作用及竞争性内源RNA(competing endogenous RNA, ceRNA)的调控作用。通过RT-qPCR验证转录组数据的可靠性。【结果】在Am4 vs Am5比较组中筛选出214条上调和251条下调lncRNA，在Am5 vs Am6比较组中筛选出141条上调和332条下调lncRNA；两个比较组共有的上调和下调lncRNA分别为7和16条。Am4 vs Am5比较组中的DElncRNA潜在调控250个邻近基因，涉及细胞进程等28个GO条目及Wnt信号通路等58条KEGG通路；Am5 vs Am6比较组中的DElncRNA潜在调控295个邻近基因，涉及细胞部分等35个GO条目及FoxO信号通路等73条KEGG通路；上述两个比较组中共有的7个上调lncRNA潜在调控10个邻近基因，涉及1个GO条目及代谢通路、谷胱甘肽代谢和核质转运等7条KEGG通路。共有的16个下调lncRNA潜在调控27个邻近基因，涉及8个GO条目及精氨酸生物合成、谷胱甘肽代谢和代谢通路等13条KEGG通路。此外， Am4 vs Am5比较组中的49条DElncRNA可靶向16个差异表达miRNA (differentially expressed miRNA, DEmiRNA)进而靶向122条差异表达mRNA (differentially expressed mRNA, DEmRNA)，可注释到代谢进程等24个GO条目和Wnt信号通路等21条KEGG通路。Am5 vs Am6比较组中的38条DElncRNA可靶向8 条DEmiRNA进而靶向67条DEmRNA，可注释到催化活性等21个GO条目和FoxO信号通路等10条KEGG通路；上述两个比较组共有的1条下调lncRNA MSTRG.10589.2可靶向ame-miR-6052和miR-511-y，进而靶向29条DEmRNA。RT-qPCR结果显示随机选取的7条DElncRNA的相对表达量与测序数据一致，证实了所用转录组数据的可靠性。【结论】意大利蜜蜂工蜂幼虫肠道发育过程伴随着lncRNA的动态差异表达，DElncRNA可通过顺式作用和ceRNA网络潜在参与对幼虫肠道发育的调控，在幼虫肠道发育中潜在发挥重要的调控作用。

关键词: 意大利蜜蜂, 工蜂, 幼虫, 长链非编码RNA, 肠道, 发育

Abstract: 【Aim】 To analyze the differential expression profiles of the long non-coding RNAs (lncRNAs) during the developmental process of the larval gut of Apis mellifera ligustica workers and reveal the regulatory roles of differentially expressed lncRNAs (DElncRNAs) in the larval gut development. 【Methods】 Based on the previously obtained transcriptome data from the 4-, 5- and 6-day-old larval gut of A. m. ligustica workers (Am4, Am5 and Am6, respectively), DElncRNAs in the Am4 vs Am5 comparison group and Am5 vs Am6 comparison group were screened using the relevant software, and the cis-acting effect of DElncRNAs and the shared up-regulated and down-regulated lncRNAs and the regulatory roles of competing endogenous RNAs (ceRNAs) were further investigated. The reliability of transcriptome data was verified through RT-qPCR. 【Results】 In the Am4 vs Am5 comparison group, 214 up-regulated and 251 down-regulated lncRNAs were screened, while 141 up-regulated and 332 down-regulated ones were screened in the Am5 vs Am6 comparison group. There were seven up-regulated and 16 down-regulated lncRNAs shared in the two comparison groups. DElncRNAs in the Am4 vs Am5 comparison group potentially regulated 250 neighboring genes, enriched in 28 GO terms such as cellular process as well as 58 KEGG pathways such as Wnt signaling pathway. DElncRNAs in the Am5 vs Am6 comparison group putatively regulated 295 neighboring genes enriched in 35 GO terms such as cell part as well as 73 KEGG pathways such as FoxO signaling pathway. The shared seven up-regulated lncRNAs in the above-mentioned two comparison groups potentially modulated 10 neighboring genes enriched in one GO term and seven KEGG pathways including metabolic pathways, glutathione metabolism and nucleocytoplasmic transport. The shared 16 down-regulated lncRNAs potentially modulated 27 neighboring genes, enriched in eight GO terms and 13 KEGG pathways including arginine biosynthesis, glutathione metabolism and metabolic pathways. Additionally, 49 DElncRNAs in the Am4 vs Am5 comparison group could target 16 differentially expressed miRNAs (DEmiRNAs) and further target 122 differentially expressed mRNAs (DEmRNAs) enriched in 24 GO terms including metabolic process and 21 KEGG pathways including Wnt signaling pathway. In the Am5 vs Am6 comparison group, 38 DElncRNAs could target eight DEmiRNAs and further target 67 DEmRNAs enriched in 21 GO terms including catalytic activity and 10 KEGG pathways including FoxO signaling pathway. The shared down-regulated lncRNA MSTRG.10589.2 in the aforementioned two comparison groups could target ame-miR-6052 and miR-511-y, further targeting 29 DEmRNAs. RT-qPCR results showed that the relative expression levels of the seven randomly selected DElncRNAs were consistent with the sequencing data, confirming the reliability of the transcriptome data. 【Conclusion】 The developmental process of the larval gut of A. m. ligustica workers is accompanied with the dynamic and differential expression of lncRNAs, and DElncRNAs may participate in modulating larval gut development via cis-acting effect and ceRNA network, potentially playing significant regulatory roles in the development of the larval gut.

Key words: Apis mellifera ligustica, workers, larvae, long non-coding RNA, gut, development

赵浩东, 臧贺, 叶道有, 陈颖, 王宁, 吴鹰, 蒋海宾, 冯睿蓉, 陈大福, 熊翠玲, 郭睿. 意大利蜜蜂工蜂幼虫肠道发育过程中lncRNA的表达谱和调控作用[J]. 昆虫学报, 2024, 67(8): 1050-1062.

ZHAO Hao-Dong, ZANG He, YE Dao-You, CHEN Ying, WANG Ning, WU Ying, JIANG Hai-Bin, FENG Rui-Rong, CHEN Da-Fu, XIONG Cui-Ling , GUO Rui . Expression profiles and regulatory roles of lncRNAs during the developmental process of the larval gut of Apis mellifera ligustica workers[J]. Acta Entomologica Sinica, 2024, 67(8): 1050-1062.

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意大利蜜蜂工蜂幼虫肠道发育过程中lncRNA的表达谱和调控作用

Expression profiles and regulatory roles of lncRNAs during the developmental process of the larval gut of Apis mellifera ligustica workers

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