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个人信息

博士生导师
研究员

Email: erjunling@cemps.ac.cn
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研究方向

昆虫和微生物的相互作用

凌尔军

个人简介

1990 年9 月-1997 年7 月，安徽农业大学，农学学士、硕士；
1997 年7 月-1999 年6 月，安徽农业大学，研究人员；
1999 年7 月-2004 年3 月，日本信州大学纤维学部，工学博士。
2003 年4 月-2004 年3 月，日本信州大学纤维学部，博士后；
2004 年4 月-2007 年8 月，美国密苏里大学-堪萨斯城，博士后；
2007 年8 月-2008年7月，美国密苏里大学-哥伦比亚，博士后；
2008年7月26-至今，中国科学院分子植物科学卓越创新中心/植物生理生态研究所，研究员。

研究工作

（1）昆虫致病真菌白僵菌和绿僵菌等是重要的生物农药，由于宿主免疫的抵抗，导致真菌生物农药的作用效率低，因此增强真菌逃避宿主免疫作用能力，或者抑制宿主免疫活性，对提高真菌生物农药的作用效率非常重要。为此以果蝇和家蚕为研究模式，研究白僵菌在穿透宿主表皮的免疫逃避机制，以及宿主表皮的免疫应答作用。
（2）肠道菌可以调控宿主的发育、生殖、神经和免疫等重要的生理活动，但是其中的作用分子机制仍然有待于深入探索。果蝇是研究认识肠道菌和宿主相互作用的重要模式生物之一，其肠道免疫系统可以有效区分共生菌和致病菌，通过活性氧(ROS) 浓度的调控是其肠道免疫反应的重要手段，目前筛选出耐受ROS的菌株，这些细菌在添食后导致果蝇肠道细胞的分裂、分化等作用发生显著差异，研究相关细菌对果蝇肠道的发育、免疫和生殖等的影响，为认识高等动物的肠道菌功能提供参考。

主要成果

通过对昆虫多酚氧化酶（Prophenoloxidase, PPO）功能研究，取得一系列原创性成果：（1）破解食叶昆虫排黑色粪便之谜。研究发现在昆虫后肠存在PPO基因转录、蛋白合成和分泌，参与诱导粪便黑化，清除其中的细菌等微生物（包括可能的病原物）被，从而保证生存环境的清洁，减少致病的机率。因此通过对昆虫排黑色粪便这一自然之谜的研究，发现这背后实际上是与免疫有关系（Journal of Biological Chemistry）。（2）解析眠期昆虫保护机制。昆虫不同于高等动物，在其生命周期中经历数次蜕皮，直至发育成成虫。在眠期，昆虫旧表皮与非常薄的新表皮分离，之间充斥蜕皮液。眠期的昆虫个体被固定，无法移动和逃避潜在的危险，因此这个时期的昆虫如何进行自身保护也是一个未解之谜。通过研究发现处于眠期昆虫的蜕皮液中有PPO在内的多种免疫蛋白，蜕皮液可以直接显著抑制细菌生长，并通过黑化反应阻止白僵菌进一步对新表皮的穿透，因此研究首次揭示蜕皮液的免疫和保护功能（Journal of Biological Chemistry，）。（3）解析刚蜕皮昆虫的保护机制。刚蜕皮昆虫的新表皮并没有发育完全，仍然同眠期一样非常薄，在一定时间内（表皮发育完全前）存在被病原物特别是真菌侵染风险。通过研究发现蜕皮后残留体表蜕皮液中的PPO可以和孢子结合，孢子在发芽时分泌的蛋白酶BPS8被宿主劫持并激活体表PPO和发生黑化反应，从而抑制白僵菌孢子的发芽、侵染。通过这个研究表明，免疫不仅仅发生在昆虫体内，还可以通过残留体表蜕皮液中的PPO进行体外免疫保护（Frontiers in Immunology，2017）。（4）昆虫前肠PPO对食物中的酚类物质进行解毒机制研究。酚类物质是植物重要的次生代谢产物，对人类的健康有益，但是对昆虫是具有毒性作用的。我们在转录和蛋白水平证实昆虫前肠存在PPO，将PPO敲除后，昆虫对食物中的酚类物质解毒功能下降，并进一步致死，表明昆虫PPO不仅是一个重要的免疫蛋白，同时对酚类物质解毒至关重要，成为害虫防治的一个靶基因（Scientific Reports，2015）。

近来实验室研究方向转移到昆虫和微生物的相互作用。通过研究发现，除磷酸化外，果蝇Relish存在类泛素化修饰， H2Av可能是通过介导Relish的类泛素化修饰来调控抗菌肽表达，相关研究结果发表在（PLoS Genetics，2021）。白僵菌在入侵至昆虫体内前必须突破宿主皮肤屏障的保护，因此皮肤的保护作用是决定感染成功与否的关键。为了克服传统感染方法的缺陷，针对家蚕幼虫特定环节表皮涂抹定量孢子溶液进行定点感染，新方法在一定剂量内同样可以感染家蚕，感染后通过切片染色、扫描电镜、透射电镜观察和感染部位转录组检测比较，发现了白僵菌在尚未侵入角质层之前就引起表皮层的黑化，同时感染部位细胞开始分裂和DNA复制，因此家蚕真皮细胞在和白僵菌物理接触之前就发生了防御反应，而且方式更加丰富，相关研究结果发表在（Frontiers in Immunology，2021）。

    1. Yingyu Tang, Ying Zhang, Qiaoli Zhang, Rongbing Chen, Liyuan Gong, Xuefei Wei, Jingfeng Yang, Kai Wu, Wuren Huang, Shirong Li, Shahzad Toufeeq, Qiuning Liu*, Erjun Ling* (2022) Prophenoloxidase-positive tubes derived from the hindguts may be the doorkeeper to detoxify the waste metabolites collected by Malpighian tubules in Lepidoptera insects. Developmental & Comparative Immunology 131:104361

    2. Xiaoyun Wu, Jia Xu, Qiuxiang Ma, Sulaiman Ahmed, Xinlu Lu, Erjun Ling*, Peng Zhang* (2022) Lysozyme inhibits postharvest physiological deterioration of cassava. Journal of Integrative Plant Biology (Accept)

    3. Wuren Huang#, Ruijuan Tang#, Shirong Li, Ying Zhang, Rongbing Chen, Liyuan Gong, Xuefei Wei, Yingyu Tang, Qiuning Liu, Lei Geng, Guoqing Pan, Brenda T. Beerntsen*, Erjun Ling* (2021) Involvement of epidermis cell proliferation in defense against Beauveria bassiana infection. Frontiers in Immunology doi: 10.3389/fimmu.2021.741797

    4. Ruijuan Tang#, Wuren Huang#, Jingmin Guan, Qiuning Liu, Brenda T Beerntsen, Erjun Ling* (2021) Drosophila H2Av negatively regulates the activity of the IMD pathway via facilitating Relish SUMOylation. PLoS Genetics 17(8):e1009718

    5. Kai Wu, Jing Wang, Lei Geng, Kai Chen, Wuren Huang, Qiuning Liu, Brenda T Beerntsen, Erjun Ling* (2020) Loss of control of the culturable bacteria in the hindgut of Bombyx mori after Cry1Ab ingestion. Developmental & Comparative Immunology 111:103754.

    6. Kai Wu, Shirong Li, Jing Wang, Yuyang Ni, Wuren Huang, Qiuning Liu*, Erjun Ling* (2020) Peptide Hormones in the Insect Midgut. Frontiers in Physiology. 11:191.

    7. Antian Huang, Mengting Lu, Erjun Ling, Ping Li, Chengshu Wang (2020)A M35 family metalloprotease is required for fungal virulence against insects by inactivating host prophenoloxidases and beyond. Virulence 11(1):222-237

    8. Yi Yuan, Wuren Huang, Keping Chen, Erjun Ling* (2020) Beauveria bassiana ribotoxin inhibits insect immunity responses to facilitate infection via host translational blockage. Developmental & Comparative Immunology 106:103605

    9. Erjun Ling*, Zhen Zou* (2018) Editorial introduction to the special issue: Insect innate immunity in China. Developmental & Comparative Immunology 83, 1-2

    10. Jingmin Guan, Jie Zhang, Shenglei Yuan, Bing Yang, Kevin D. Clark, Erjun Ling, Wuren Huang* (2018) Analysis of the functions of the signal peptidase complex in the midgut of Tribolium castaneum. Archives of Insect Biochemistry and Physiology 97(3):e21441

    11. Kai Wu, Fang Han, Yi Yuan, Yining Liu, Erjun Ling, Qian Wang*, Wuren Huang* (2018) Effect of the insect phenoloxidase on the metabolism of L-DOPA. Archives of Insect Biochemistry and Physiology 98(4):e21457

    12. Longhai Liu, Xiaoran Qian, Mengling Chao, Yijiao Zhao, Junyi Huang, Taichu Wang, Fan Sun, Erjun Ling, Hongsheng Song* (2018) Aluminum toxicity related to SOD and expression of presenilin and CREB in Bombyx mori. Archives of Insect Biochemistry and Physiology 99(2):e21480

    13. Jie Zhang, Wuren Huang, Chuanfei Yuan, Yuzhen Lu, Bing Yang, Cheng-Yuan Wang, Peng Zhang, Leonard Dobens, Zhen Zou, Chengshu Wang*, Erjun Ling* (2017) Prophenoloxidase-mediated ex vivo immunity to delay fungal infection after insect ecdysis. Frontiers in Immunology 8, 1445, doi:10.3389/fimmu.2017.01445.

    14. Shenglei Yuan, Wuren Huang, Lei Geng, Brenda T. Beerntsen, Hongsheng Song, Erjun Ling* (2017) Differentiation of lepidoptera scale cells from epidermal stem cells followed by ecdysone-regulated DNA duplication and scale secreting. Cell Cycle 16(21):2156-2167. doi: 10.1080/15384101.2017.1376148.

    15. Fei Liu, Wuren Huang, Kai Wu, Zhongying Qiu, Yuan Huang, Erjun Ling* (2017) Exploiting innate immunity for biological pest control. Advances in Insect Physiology 52: 199–230.

    16. Fang Han#, Anrui Lu#, Yi Yuan, Wuren Huang, Brenda T. Beerntsen, Junyi Huang*, Erjun Ling* (2017) Characterization of an entomopathogenic fungi target integument protein, Bombyx mori single domain von Willebrand factor type C, in the silkworm, Bombyx mori. Insect Molecular Biology 26(3), 308–316.

    17. Bing Yang, Wuren Huang, Jie Zhang, Qiuyun Xu, Shoulin Zhu, Qiaoli Zhang, Brenda T. Beerntsen, Hongsheng Song*, Erjun Ling* (2016) Analysis of gene expression in the midgut of Bombyx mori during the larval molting stage. BMC Genomics 17(1):866.

    18. Kai Wu, Bing Yang, Wuren Huang, Leonard Dobens, Hongsheng Song*, Erjun Ling* (2016) Gut immunity in Lepidopteran insects. Developmental and Comparative Immunology 64:65-74 .

    19. Wuren Huang, Jie Zhang, Bing Yang, Brenda T. Beerntsen, Hongsheng Song*, Erjun Ling*. (2016) DNA duplication is essential for the repair of gastrointestinal perforation in the insect midgut. Scientific Reports. 6, 19142.

    20. Kai Wu, Jie Zhang, Qiaoli Zhang, Shoulin Zhu, Qimiao Shao, Kevin D. Clark, Yining Liu*, Erjun Ling* (2015). Plant phenolics are detoxified by prophenoloxidase in the insect gut. Scientific Reports. 5, 16823.

    21. Anrui Lu, Qiaoli Zhang, Jie Zhang, Bing Yang, Kai Wu, Wei Xie, Yun-Xia Luan, Erjun Ling* (2014) Insect prophenoloxidase: the view beyond immunity. Frontiers in Physiology. 5: 252 doi: 10.3389/fphys.2014.00252 (Invited review)

    22. Lulu Kong, Anrui Lu, Jingmin Guan, Bing Yang, Muwang Li, Julián F. Hillyer, Nalini Ramarao, Kenneth S?derh?ll, Chaoliang Liu*, Erjun Ling* （2015）Thermolysin damages animal life through degradation of plasma proteins enhanced by rapid cleavage of serpins and activation of proteases. Archives of Insect Biochemistry and Physiology. 88(1):64-84.

    23. Yujia Hu, Yi Han, Yingyao Shao, Xingjun Wang, Yeqing Ma, Erjun Ling, Lei Xue (2015) Gr33a modulates Drosophila male courtship preference. Scientific Reports. doi: 10.1038/srep07777.

    24. Jie Zhang, Anrui Lu, Lulu Kong, Qiaoli Zhang, Erjun Ling* (2014) Functional analysis of insect molting fluid proteins on the protection and regulation of ecdysis. The Journal of Biological Chemistry. 289: 35891–35906.

    25. Anrui Lu, Xuquan Li, Julián F. Hillyer, Brenda T. Beerntsen, Kenneth S?derh?ll, Erjun Ling* (2014) Recombinant Drosophila prophenoloxidase 1 is sequentially cleaved by α-chymotrypsin during in vitro activation. Biochimie. 102:154-165.

    26. Anrui Lu, Qin Peng, Erjun Ling* (2014) Formation of disulfide bonds in insect prophenoloxidase enhances immunity through improving enzyme activity and stability. Developmental and Comparative Immunology 44(2):351-358.

    27. Fei Liu, Qiuyun Xu, Qiaoli Zhang, Brenda T. Beerntsene, Erjun Ling* (2013) Hemocytes and hematopoiesis in the silkworm, Bombyx mori. Invertebrate Survival Journal 10: 102-109 (Invited review).

    28. Bing Yang, Aanrui Lu, Qin Peng, Qing-Zhi Ling, Erjun Ling* (2013) Activity of fusion prophenoloxidase-GFP and its potential applications for innate immunity study. PLoS ONE 8(5):e64106.

    29. Xiaoguang Duan, Jia Xu, Erjun Ling, Peng Zhang (2013) Expression of Cry1Aa in cassava improves its insect resistance against Helicoverpa armigera. Plant Molecular Biology 83:131–141.

    30. Qiuyun Xu#, Anrui Lu#, Guohua Xiao, Bing Yang, Jie Zhang, Xuquan Li, Jingmin Guan, Qimiao Shao, Brenda T. Beerntsen, Peng Zhang, Chengshu Wang, Erjun Ling* (2012) Transcriptional profiling of midgut immunity response and degeneration in the wandering silkworm, Bombyx mori. PLoS ONE 7(8): e43769.

    31. Yupu Diao, Anrui Lu, Bing Yang, Wenli Hu, Qing Peng, Qing-Zhi Ling, Brenda T. Beerntsen, Kenneth S?derh?ll, Erjun Ling* (2012) Existence of Prophenoloxidase in wing discs: A source of plasma prophenoloxidase in the silkworm, Bombyx mori. PLoS ONE 7(7): e41416.

    32. Chen Yang, Liu Fei, Yang Bing, Lu Aanrui, Shiwei Wang, Jingfang Wang, Qing-Zhi Ling, Xuan Li, Brenda T. Beerntsene, Erjun Ling* (2012) Specific amino acids affecting Drosophila melanogaster prophenoloxidase activity in vitro. Developmental and Comparative Immunology 38(1): 88-97.

    33. Qimiao Shao, Bing Yang, Qiuyun Xu, Xuquan Li, Zhiqiang Lu, Chengshu Wang, Yongping Huang, Kenneth S?derh?ll*, Erjun Ling* (2012) Hindgut innate immunity and regulation of fecal microbiota through melanization in insects. Journal of Biological Chemistry 287: 14270-14279.

    34. Xuquan Li, Miaolian Ma, Fei Liu, Yang Chen, Anrui Lu, Qing-Zhi Ling, Jianyong Li, Brenda T. Beerntsen, Xiao-Qiang Yu, Chaoliang Liu*, Erjun Ling* (2012) Properties of Drosophila melanogaster prophenoloxidases expressed in Escherichia coli. Developmental and Comparative Immunology 36(4): 648-656.

    35. Fei Liu, Yang Chen, Bing Yang, Jingfang Wang, Qin Peng, Qimiao Shao, Xuan Li, Brenda T. Beerntsen, Yechun Xu, Jianyong Li, Xiao-Qiang Yu, Erjun Ling* (2012) Drosophila melanogaster prophenoloxidases respond inconsistently to Cu2+ and have different activity in vitro. Developmental and Comparative Immunology 36(3): 619-628.

    36. Yupu Diao, Yumin Qi, Yajun Ma, Ai Xia, Igor Sharakhov, Xiaoguang Chen, Jim Biedler, Erjun Ling, Zhijian Jake Tu (2011) Next-generation sequencing reveals recent horizontal transfer of a DNA transposon between divergent mosquitoes. PLoS ONE 6 (2): e16743

    37. Zhixiang Wang, Anrui Lu, Xuquan Li, Qimiao Shao, Brenda T. Beerntsen, Chaoliang Liu, Yajun Ma, Yamin Huang, Huaimin Zhu*, Erjun Ling* (2011) A systematic study on hemocyte identification and plasma prophenoloxidase from Culex pipiens quinquefasciatus at different developmental stages. Experimental Parasitology 127:135–141.

    38. Shan Wu, Xiaofeng Zhang, Yongqiang He, Jiangbing Shuai, Xiaomei Chen, Erjun Ling* (2010) Expression of antimicrobial peptide genes in Bombyx mori gut modulated by oral bacterial infection and development. Developmental and Comparative Immunology 34(11):1191-1198.

    39. Shan Wu, Xiaofeng Zhang, Xiaomei Chen, Pingsheng Cao, Erjun Ling* (2010) BmToll9, an Arthropods conservative Toll, is probably involved in the local gut immune response in the silkworm, Bombyx mori. Developmental and Comparative Immunology 34(2):93-96.

    40. Chenglong Wang, Zhixiang Wang, Qing-zhi Ling, Michael M. Kariuki, Kenji Kiguchi, Erjun Ling* (2010) Physiological functions of hemocytes newly emerged from the cultured hematopoietic organs in the silkworm, Bombyx mori. Insect Science 17:7-20.

    41. Xiang-Jun Rao#, Erjun Ling# and Xiao-Qiang Yu (2010) The role of lysozyme in the prophenoloxidase activation system of Manduca sexta: An in vitro approach. Developmental and Comparative Immunology 34(3):264-271 (# Equal contribution).

    42. Ling Tian, Enen Guo, Yupu Diao, Shun Zhou, Qin Peng, Yang Cao, Erjun Ling, Sheng Li (2010) Genome-wide regulation of innate immunity by juvenile hormone and 20-hydroxyecdysone in the Bombyx fat body. BMC Genomics 11:549.

    43. Ling Tian, Enen Guo, Sheng Wang, Shumin Liu, Rong-Jing Jiang, Yang Cao, Erjun Ling and Sheng Li (2010) Developmental regulation of glycolysis by 20-hydroxyecdysone and juvenile hormone in fat body tissues of the silkworm, Bombyx mori. Journal of Molecular Cell Biology 2(5):255-263.

    44. Fei Liu, Erjun Ling, Shan Wu (2009) Gene expression profiling during early response to injury and microbial challenges in the silkworm, Bombyx mori. Archives of Insect Biochemistry and Physiology 72(1):16-33.

    45. Yang Chen, Erjun Ling, Zhihui Weng (2009) Functional characterization of PGRP-LC1 of Anopheles gambiae through deletion and RNA interference. Insect Science 16:443-453.

    46. Qing-zhi Ling, Chenglong Wang, Michael M. Kariuki, Kenji Kiguchi and Erjun Ling （2009）Reexamination of the role of hematopoietic organs on the hematopoiesis in the silkworm, Bombyx mori. African Journal of Biotechnology 8 (15):3658-3665.

    47. Erjun Ling, Xiang-jun Rao, Jing-qun Ao and Xiao-Qiang Yu (2009) Purification and characterization of a small cationic peptide from the tobacco hornworm Manduca sexta. Insect Biochemistry and Molecular Biology 39(4):263-271.

    48. Erjun Ling, Jing-qun Ao and Xiao-Qiang Yu (2008) Nuclear translocation of Immulectin-3 dtimulates hemocyte proliferation. Molecular Immunology 45: 2598-2606.

    49. Jing-qun Ao, Erjun Ling and Xiao-Qiang Yu (2008) A Toll receptor from Manduca sexta is in response to Escherichia coli infection molecular immunology. Molecular Immunology 45: 543-552.

    50. Jing-qun Ao, Erjun Ling, Xiang-jun Rao and Xiao-Qiang Yu (2008) A novel ML protein from Manduca sexta may function as a key accessory protein for lipopolysaccharide signaling. Molecular Immunology 45: 2772-2781.

    51. Jing-qun Ao, Erjun Ling and Xiao-Qiang Yu (2007) Drosophila C-type lectins enhance cellular encapsulation. Molecular Immunology 44: 2541-2548.

    52. Erjun Ling and Xiao-Qiang Yu (2006) Cellular encapsulation and melanization are enhanced by immulectins, pattern recognition receptors from the tobacco hornworm Manduca sexta. Developmental and Comparative Immunology 30: 289-299.

    53. Erjun Ling and Xiao-Qiang Yu (2006) Hemocytes from the tobacco hornworm Manduca sexta have distinct functions in phagocytosis of foreign particles and self dead cells. Developmental and Comparative Immunology 30: 301-309.

    54. Erjun Ling*, Koji Shirai, Rensuke Kanekatsu, Kenji Kiguchi, Yasuhiko Kobayashi, Tomoo Funayama and Hiroshi Watanabe (2006) Contribution of circulating hemocytes to the regeneration of heavy ion beams (12C5+) irradiated hematopoietic organs in the silkworm, Bombyx mori, through the way of phagocytosis of injured cells after invasion. Developmental and Comparative Immunology 30: 531-543.

    55. Xiao-Qiang Yu, Erjun Ling, Miles E. Tracy and Yifei Zhu (2006) Immulectin-4 from the tobacco hornworm Manduca sexta binds to lipopolysaccharide and lipoteichoic acid. Insect Molecular Biology 15: 119-128.

    56. Erjun Ling*, Koji Shirai, Rensuke Kanehatsu and Kenji Kiguchi (2005) Reexamination of phenoloxidase in larval circulating hemocytes of the silkworm, Bombyx mori. Tissue and Cell 37: 101-107.

    57. Erjun Ling*, Koji Shirai, Rensuke Kanekatsu and Kenji Kiguchi (2005) Hemocyte differentiation in the hematopoietic organs of the silkworm, Bombyx mori: prohemocytes have the function of phagocytosis. Cell and Tissue Research 320: 535-543.

    58. Erjun Ling and Xiao-Qiang Yu (2005) Prophenoloxidase binds to the surface of hemocytes and is involved in hemocyte melanization in Manduca sexta. Insect Biochemistry and Molecular Biology 35: 1356-1366.

    59. Xiao-Qiang Yu, Miles E. Tracy, Erjun Ling, Scholz FR and Trenczek T (2005) A novel C-type immulectin-3 from Manduca sexta is translocated from hemolymph into the cytoplasm of hemocytes. Insect Biochemistry and Molecular Biology 35: 285-295.

    60. Erjun Ling, Kana Fukamoto, Shiqing Xu, Koji Shirai, Rensuke Kanekatsu, Yasuhiko Kobayashi, Zhen-Li Tu, Tomoo Funayama, Hiroshi Watanabe and Kenji Kiguchi (2003) Regeneration of hemopoietic organs in the silkworm, Bombyx mori, after locally targeted irradiation with heavy ion beams. Journal of Insect Biotechnology and Sericology 72: 95-100.

    61. Erjun Ling, Koji Shirai, Rensuke Kanekatsu, Yasuhiko Kobayashi, Zhen-Li Tu, Tomoo Funayama, Hiroshi Watanabe and Kenji Kiguchi (2003) Why dose hemocyte density rise at the wandering stage in the silkworm, Bombyx mori? Journal of Insect Biotechnology and Sericology 72: 101-109.

    62. Erjun Ling*, Koji Shirai, Rensuke Kanekatsu and Kenji Kiguchi (2003) Classification of larval circulating hemocytes of the silkworm, Bombyx mori, by acridine orange and propidium iodide staining. Histochemistry and Cell Biology 120: 505-511.