State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China.
PLoS Pathog. 2013 Jan;9(1):e1003102. doi: 10.1371/journal.ppat.1003102. Epub 2013 Jan 10.
The stress of living conditions, similar to infections, alters animal immunity. High population density is empirically considered to induce prophylactic immunity to reduce the infection risk, which was challenged by a model of low connectivity between infectious and susceptible individuals in crowded animals. The migratory locust, which exhibits polyphenism through gregarious and solitary phases in response to population density and displays different resistance to fungal biopesticide (Metarhizium anisopliae), was used to observe the prophylactic immunity of crowded animals. We applied an RNA-sequencing assay to investigate differential expression in fat body samples of gregarious and solitary locusts before and after infection. Solitary locusts devoted at least twice the number of genes for combating M. anisopliae infection than gregarious locusts. The transcription of immune molecules such as pattern recognition proteins, protease inhibitors, and anti-oxidation proteins, was increased in prophylactic immunity of gregarious locusts. The differentially expressed transcripts reducing gregarious locust susceptibility to M. anisopliae were confirmed at the transcriptional and translational level. Further investigation revealed that locust GNBP3 was susceptible to proteolysis while GNBP1, induced by M. anisopliae infection, resisted proteolysis. Silencing of gnbp3 by RNAi significantly shortened the life span of gregarious locusts but not solitary locusts. By contrast, gnbp1 silencing did not affect the life span of both gregarious and solitary locusts after M. anisopliae infection. Thus, the GNBP3-dependent immune responses were involved in the phenotypic resistance of gregarious locusts to fungal infection, but were redundant in solitary locusts. Our results indicated that gregarious locusts prophylactically activated upstream modulators of immune cascades rather than downstream effectors, preferring to quarantine rather than eliminate pathogens to conserve energy meanwhile increasing the "distance" of infectious and target individuals. Our study has obvious implications for bio-pesticides management of crowded pests, and for understanding disease epidemics and adaptiveness of pathogens.
生活条件的压力与感染相似，会改变动物的免疫力。高种群密度被经验性地认为会诱导预防性免疫，以降低感染风险，但这一观点受到了拥挤动物中传染性个体与易感染个体之间连通性低的模型的挑战。群居和独居是昆虫对种群密度做出的表型反应，迁飞蝗在群居和独居阶段对真菌生物农药（绿僵菌）表现出不同的抗性，我们利用迁飞蝗来观察拥挤动物的预防性免疫。我们应用 RNA 测序技术，研究了感染前后群居和独居蝗蝻脂肪体样本中的差异表达。与群居蝗蝻相比，独居蝗蝻至少有两倍数量的基因用于对抗绿僵菌感染。免疫分子如模式识别蛋白、蛋白酶抑制剂和抗氧化蛋白的转录在群居蝗蝻的预防性免疫中增加。减少群居蝗蝻对绿僵菌易感性的差异表达转录本在转录和翻译水平上得到了验证。进一步的研究表明，蝗蝻 GNBP3 易受蛋白水解，而 GNBP1 在绿僵菌感染后诱导，能抵抗蛋白水解。通过 RNAi 沉默 gnbp3 显著缩短了群居蝗蝻的寿命，但对独居蝗蝻没有影响。相比之下，gnbp1 沉默后，无论是群居还是独居蝗蝻在感染绿僵菌后，其寿命都没有受到影响。因此，GNBP3 依赖的免疫反应参与了群居蝗蝻对真菌感染的表型抗性，但在独居蝗蝻中是冗余的。我们的研究结果表明，群居蝗蝻预防性地激活了免疫级联的上游调节剂，而不是下游效应器，它们更喜欢隔离而不是消除病原体，以节省能量，同时增加传染性个体和目标个体之间的“距离”。我们的研究结果对拥挤害虫的生物农药管理具有明显的意义，并有助于理解疾病流行和病原体的适应性。
