意大利蜜蜂和中华蜜蜂雄蜂与工蜂触角差异蛋白质组分析
摘要
蜜蜂利用复杂的化学信号交流系统来调节其多层次的社会生活,而触角是感受这些化学信号的主要器官。为了进一步探明雄蜂与工蜂触角发挥功能的分子机制,选择从形态学和差异蛋白质组的角度对其进行分析。本研究分别对意大利蜜蜂(Apis mellifera ligustica)和中华蜜蜂(A. cerana cerana)的雄蜂和工蜂触角进行扫描电镜观察以及蛋白质的二维电泳,结合质谱技术和实时荧光定量PCR技术对蛋白质进行鉴定以及验证,并利用生物信息学等方法对结果进行分析。
对意大利蜜蜂(A. mellifera ligustica)和中华蜜蜂(A. cerana cerana)触角形态学分析发现,相比工蜂,雄蜂具有较长的触角和较多的板型感受器(意蜂7.5倍,中蜂3倍),可以推测雄蜂触角中的大量板型感受器能促进雄蜂对蜂王性信息素的识别以及交配过程中对蜂王的定位;相反工蜂触角中的类毛状感受器要比雄蜂多(意蜂2倍,中蜂2倍),这些类毛状感受器可能与昆虫搜寻食物,以及对温湿度、机械力刺激较敏感有关,这有助于工蜂通过调节自身活动来维持蜂群的稳定。意蜂雄蜂触角中板型感受器的数目约是中蜂雄蜂的2.5倍,这表明了中蜂雄蜂的板型感受器可能对识别蜂王信息素更加敏感,而意大利蜜蜂在生物进化过程中需要更多的板型感受器来提高其对蜂王信息素的灵敏性。
对意大利蜜蜂(A. mellifera ligustica)性成熟雄蜂与采集蜂触角的蛋白质组图谱进行比较发现,在雄蜂触角中表达454个蛋白质,在工蜂触角中表达439个蛋白质,其中402个共有蛋白质占总蛋白质数量的82%,这说明虽然雄蜂与工蜂触角在形态学上及功能上存在差异,但它们在分子进化过程中还是相对保守的。在有差异的蛋白质中,61个高丰度蛋白质的功能得到了鉴定,其中有41个(67%)蛋白质在性成熟雄蜂触角中高表达,仅有20个(33%)蛋白质在采集蜂触角中高表达。更多的参与脂肪酸代谢、抗氧化和蛋白质折叠相关的蛋白质在性成熟雄蜂触角中高表达,这些蛋白质可能为促进对性信息素的检测及降解过程提供了保障。在采集蜂触角中高表达蛋白质主要参与碳水化合物代谢和能量产生以及分子转运功能,这表明在工蜂的采集活动和其他的触角功能反中需要大量的能量代谢和分子转运蛋白质参与。对表达量有差异的蛋白质进行功能富集和生化通路分析,其中都发现了参与碳水化合物代谢和能量产生,脂肪酸代谢,细胞骨架,抗氧化,以及分子转运5个功能的蛋白质,这进一步表明了参与这5个功能的蛋白质在蜜蜂触角发挥功能过程中起到重要作用。其中,参与碳水化合物代谢和能量产生以及分子转运功能蛋白质占据了功能富集分析的80%以上,并占构建的触角差异蛋白质生物相互作用网络的45%,表明这两类蛋白质家族对雄蜂和采集蜂触角具有更为重要的影响。对生化通路中的10个蛋白质的基因水平表达进行验证,发现其中9个蛋白质的表达趋势与转录水平是一致的,这些表达一致性的蛋白质可以作为后续基因操作的靶向蛋白质。
对中华蜜蜂(A. cerana cerana)性成熟雄蜂和采集蜂触角进行差异蛋白质组比较发现,在雄蜂触角中表达424个蛋白质,在工蜂触角中表达408个蛋白质,其中包括361个共有蛋白质这也表明了触角在不同性别蜜蜂中的分子进化水平的保守性。其中有46个高丰度差异蛋白质得到鉴定,其中在雄蜂触角中高表达的28个蛋白质(60.9%)主要参与碳水化合物代谢和能量产生、蛋白质折叠、脂肪酸代谢、发育以及分子转运,这些蛋白质为雄蜂触角运动以及对信息素识别和转运过程提供了能量来源和信号转导的分子基础。在工蜂触角中高表达的18个蛋白质(39.1%)中,参与分子转运以及抗氧化作用的蛋白质更多的在工蜂中高表达,这些蛋白质对采集蜂识别蜜粉源、防御敌害以及调节蜂群内的分工具有重要意义。对差异蛋白质进行功能富集和生化通路分析,其中都发现了参与碳水化合物代谢和能量产生、脂肪酸代谢、抗氧化和分子转运功能的蛋白质,这说明参与这些功能的蛋白质对蜜蜂触角功能的发挥提供了分子依据。
虽然意蜂和中蜂为两个不同的蜂种,但是从各自的雄蜂和工蜂触角蛋白质组成比较,发现差异蛋白质的种类和表达水平十分相似,表明不同蜂种间触角功能的发挥具有一定的保守性；另一方面意蜂中参与碳水化合物代谢和能量产生以及抗氧化的蛋白质分别在工蜂和雄蜂中高表达的较多；而在中蜂中更多的碳水化合物代谢和能量产生类蛋白质在雄蜂中高表达,抗氧化类的蛋白质更多的在工蜂中高表达；产生这种现象的原因可能是由于不同种间进化水平的差异造成的。
蜜蜂触角差异蛋白质组分析不仅表明了在性成熟雄蜂和采集蜂触角中性别偏好的蛋白质表达水平,也表明了它们对不同的嗅觉功能相应的反应机制。这对深入了解蜜蜂社会活动和蜜蜂生物学具有重要意义。
Honey bees have evolved an intricate system of chemical communication to regulate their multifaceted social interactions. To gain better understanding how the drone and the worker react to different olfactory responses and undertake their activities, morphology and differential proteomics research were carried out. The antennae of drones and workers from Apis mellifera ligustica and A. cerana cerana were examined using scanning electron microscope (SEM), and the antennae proteins were extracted, then two dimensional electrophoresis (2-DE), mass spectrometry, quantitative real-time PCR (qRT-PCR) and bioinformatics approaches were used.
Morphological assay by SEM showed that the antennae of drone are lager than worker', and the total poreplate sensilla showed significant higher number in the drone than those of the worker (almost 7.5 times in A. mellifera ligustica, almost 3 times in A. cerana cerana), suggested to assist its high antennal olfactory functions, particularly the sex pheromone related responses. In contrast, the number of hair-like sensilla of workers was two-fold higher than drones', This is likely to help the foragers to search nectar resource quickly, to sense temperature, humidity and mechanical force.
With the comparison of the proteins profile of sexual matured drones and foragers' antennae (A. mellifera ligustica), a total of 484 and 439 protein spots were detected in adult drones and workers'antennae, respectively, of which 416 expressed proteins were shared between drone and worker antennae, it means that they evolve conservatively between them.61 proteins differentially expressed proteins were identified, of which 41 proteins (67%) were highly regulated in the sexual mature drones' antennae whereas only 20 proteins (33%) upregulated in forager worker bees'. Proteins associated with fatty acid metabolism, antioxidant activities and protein folding were highly upregulated in the sexual mature drones' antennae indicating their significance to detection and degradation of sex pheromones required in queen mating. The forager worker bees' antennae highly expressed proteins related to carbohydrate and energy metabolism and the molecular transporters signifying high demand for metabolic energy and odorant binding proteins in their foraging activities and other olfactory responses. Some proteins were found in the results of functional enrichment and biological interaction networks (BIN) analysis. The involvement of carbohydrate and energy metabolism, fatty acid metabolism, cytoskeleton, antioxidant and molecular transporters in these groups reveals their important role in the antennal olfasctory function. Over 80% of the functional enrichment analysis and 45% of the BIN of the altered antennal proteins were covered by carbohydrate metabolism and energy production and molecular transporters, respectively confirming that these two protein families play the crucial role in the antennal olfactory function of sexual mature drone and forager worker bees.10 key node proteins in the BIN were validated at the transcript level and 9 proteins displayed comparable expression with the qRT-PCR analysis, and these proteins provide us some target proteins for further genetically manipulation.
By comparison of the proteins profile of sexual matured drones and foragers' antennae (A. cerana cerana),424 and 408 protein spots were detected in drones and workers' antennae, respectively, and 416 shared proteins mean that they evolve conservatively between them.46 differentially expressed proteins were identified, proteins were highly regulated in the sexual mature drones' antennae, which was involving in carbohydrate and energy metabolism, fatty acid metabolism, development and molecular transporters, and they provide energy and molecular transporter in recognizing and processing of pheromone. More proteins expressed highly in workers, which related to carbohydrate and energy metabolism and the molecular transporters, this demonstrates that foraging activities, defense, and other olfactory responses need high metabolic energy and more odorant binding proteins. Although Apis mellifera ligustica and Apis cerana cerana belong to two different species, the kind and expressional level of differentially expressed proteins seem similar between drones and workers'antennae and it indicates molecular mechanism is conservative at a certain extent in different species. For Apis mellifera ligustica, more proteins expressed highly in drone and worker respectively, which related to carbohydrate and energy metabolism and antioxidant. However the results were contrast in Apis cerana cerana, the dispency between two spiecies may contribute to different evolve level.
This differential proteomic analysis reveals sex-biased protein expression in the sexual mature antennae of drone and forager worker bees, and indicates their responding mechanism to different olfactory functions accordingly. Moreover, the results will open the way for future detailed functional analysis in the antennae of the two honeybee casts.
对意大利蜜蜂(A. mellifera ligustica)和中华蜜蜂(A. cerana cerana)触角形态学分析发现,相比工蜂,雄蜂具有较长的触角和较多的板型感受器(意蜂7.5倍,中蜂3倍),可以推测雄蜂触角中的大量板型感受器能促进雄蜂对蜂王性信息素的识别以及交配过程中对蜂王的定位;相反工蜂触角中的类毛状感受器要比雄蜂多(意蜂2倍,中蜂2倍),这些类毛状感受器可能与昆虫搜寻食物,以及对温湿度、机械力刺激较敏感有关,这有助于工蜂通过调节自身活动来维持蜂群的稳定。意蜂雄蜂触角中板型感受器的数目约是中蜂雄蜂的2.5倍,这表明了中蜂雄蜂的板型感受器可能对识别蜂王信息素更加敏感,而意大利蜜蜂在生物进化过程中需要更多的板型感受器来提高其对蜂王信息素的灵敏性。
对意大利蜜蜂(A. mellifera ligustica)性成熟雄蜂与采集蜂触角的蛋白质组图谱进行比较发现,在雄蜂触角中表达454个蛋白质,在工蜂触角中表达439个蛋白质,其中402个共有蛋白质占总蛋白质数量的82%,这说明虽然雄蜂与工蜂触角在形态学上及功能上存在差异,但它们在分子进化过程中还是相对保守的。在有差异的蛋白质中,61个高丰度蛋白质的功能得到了鉴定,其中有41个(67%)蛋白质在性成熟雄蜂触角中高表达,仅有20个(33%)蛋白质在采集蜂触角中高表达。更多的参与脂肪酸代谢、抗氧化和蛋白质折叠相关的蛋白质在性成熟雄蜂触角中高表达,这些蛋白质可能为促进对性信息素的检测及降解过程提供了保障。在采集蜂触角中高表达蛋白质主要参与碳水化合物代谢和能量产生以及分子转运功能,这表明在工蜂的采集活动和其他的触角功能反中需要大量的能量代谢和分子转运蛋白质参与。对表达量有差异的蛋白质进行功能富集和生化通路分析,其中都发现了参与碳水化合物代谢和能量产生,脂肪酸代谢,细胞骨架,抗氧化,以及分子转运5个功能的蛋白质,这进一步表明了参与这5个功能的蛋白质在蜜蜂触角发挥功能过程中起到重要作用。其中,参与碳水化合物代谢和能量产生以及分子转运功能蛋白质占据了功能富集分析的80%以上,并占构建的触角差异蛋白质生物相互作用网络的45%,表明这两类蛋白质家族对雄蜂和采集蜂触角具有更为重要的影响。对生化通路中的10个蛋白质的基因水平表达进行验证,发现其中9个蛋白质的表达趋势与转录水平是一致的,这些表达一致性的蛋白质可以作为后续基因操作的靶向蛋白质。
对中华蜜蜂(A. cerana cerana)性成熟雄蜂和采集蜂触角进行差异蛋白质组比较发现,在雄蜂触角中表达424个蛋白质,在工蜂触角中表达408个蛋白质,其中包括361个共有蛋白质这也表明了触角在不同性别蜜蜂中的分子进化水平的保守性。其中有46个高丰度差异蛋白质得到鉴定,其中在雄蜂触角中高表达的28个蛋白质(60.9%)主要参与碳水化合物代谢和能量产生、蛋白质折叠、脂肪酸代谢、发育以及分子转运,这些蛋白质为雄蜂触角运动以及对信息素识别和转运过程提供了能量来源和信号转导的分子基础。在工蜂触角中高表达的18个蛋白质(39.1%)中,参与分子转运以及抗氧化作用的蛋白质更多的在工蜂中高表达,这些蛋白质对采集蜂识别蜜粉源、防御敌害以及调节蜂群内的分工具有重要意义。对差异蛋白质进行功能富集和生化通路分析,其中都发现了参与碳水化合物代谢和能量产生、脂肪酸代谢、抗氧化和分子转运功能的蛋白质,这说明参与这些功能的蛋白质对蜜蜂触角功能的发挥提供了分子依据。
虽然意蜂和中蜂为两个不同的蜂种,但是从各自的雄蜂和工蜂触角蛋白质组成比较,发现差异蛋白质的种类和表达水平十分相似,表明不同蜂种间触角功能的发挥具有一定的保守性；另一方面意蜂中参与碳水化合物代谢和能量产生以及抗氧化的蛋白质分别在工蜂和雄蜂中高表达的较多；而在中蜂中更多的碳水化合物代谢和能量产生类蛋白质在雄蜂中高表达,抗氧化类的蛋白质更多的在工蜂中高表达；产生这种现象的原因可能是由于不同种间进化水平的差异造成的。
蜜蜂触角差异蛋白质组分析不仅表明了在性成熟雄蜂和采集蜂触角中性别偏好的蛋白质表达水平,也表明了它们对不同的嗅觉功能相应的反应机制。这对深入了解蜜蜂社会活动和蜜蜂生物学具有重要意义。
Honey bees have evolved an intricate system of chemical communication to regulate their multifaceted social interactions. To gain better understanding how the drone and the worker react to different olfactory responses and undertake their activities, morphology and differential proteomics research were carried out. The antennae of drones and workers from Apis mellifera ligustica and A. cerana cerana were examined using scanning electron microscope (SEM), and the antennae proteins were extracted, then two dimensional electrophoresis (2-DE), mass spectrometry, quantitative real-time PCR (qRT-PCR) and bioinformatics approaches were used.
Morphological assay by SEM showed that the antennae of drone are lager than worker', and the total poreplate sensilla showed significant higher number in the drone than those of the worker (almost 7.5 times in A. mellifera ligustica, almost 3 times in A. cerana cerana), suggested to assist its high antennal olfactory functions, particularly the sex pheromone related responses. In contrast, the number of hair-like sensilla of workers was two-fold higher than drones', This is likely to help the foragers to search nectar resource quickly, to sense temperature, humidity and mechanical force.
With the comparison of the proteins profile of sexual matured drones and foragers' antennae (A. mellifera ligustica), a total of 484 and 439 protein spots were detected in adult drones and workers'antennae, respectively, of which 416 expressed proteins were shared between drone and worker antennae, it means that they evolve conservatively between them.61 proteins differentially expressed proteins were identified, of which 41 proteins (67%) were highly regulated in the sexual mature drones' antennae whereas only 20 proteins (33%) upregulated in forager worker bees'. Proteins associated with fatty acid metabolism, antioxidant activities and protein folding were highly upregulated in the sexual mature drones' antennae indicating their significance to detection and degradation of sex pheromones required in queen mating. The forager worker bees' antennae highly expressed proteins related to carbohydrate and energy metabolism and the molecular transporters signifying high demand for metabolic energy and odorant binding proteins in their foraging activities and other olfactory responses. Some proteins were found in the results of functional enrichment and biological interaction networks (BIN) analysis. The involvement of carbohydrate and energy metabolism, fatty acid metabolism, cytoskeleton, antioxidant and molecular transporters in these groups reveals their important role in the antennal olfasctory function. Over 80% of the functional enrichment analysis and 45% of the BIN of the altered antennal proteins were covered by carbohydrate metabolism and energy production and molecular transporters, respectively confirming that these two protein families play the crucial role in the antennal olfactory function of sexual mature drone and forager worker bees.10 key node proteins in the BIN were validated at the transcript level and 9 proteins displayed comparable expression with the qRT-PCR analysis, and these proteins provide us some target proteins for further genetically manipulation.
By comparison of the proteins profile of sexual matured drones and foragers' antennae (A. cerana cerana),424 and 408 protein spots were detected in drones and workers' antennae, respectively, and 416 shared proteins mean that they evolve conservatively between them.46 differentially expressed proteins were identified, proteins were highly regulated in the sexual mature drones' antennae, which was involving in carbohydrate and energy metabolism, fatty acid metabolism, development and molecular transporters, and they provide energy and molecular transporter in recognizing and processing of pheromone. More proteins expressed highly in workers, which related to carbohydrate and energy metabolism and the molecular transporters, this demonstrates that foraging activities, defense, and other olfactory responses need high metabolic energy and more odorant binding proteins. Although Apis mellifera ligustica and Apis cerana cerana belong to two different species, the kind and expressional level of differentially expressed proteins seem similar between drones and workers'antennae and it indicates molecular mechanism is conservative at a certain extent in different species. For Apis mellifera ligustica, more proteins expressed highly in drone and worker respectively, which related to carbohydrate and energy metabolism and antioxidant. However the results were contrast in Apis cerana cerana, the dispency between two spiecies may contribute to different evolve level.
This differential proteomic analysis reveals sex-biased protein expression in the sexual mature antennae of drone and forager worker bees, and indicates their responding mechanism to different olfactory functions accordingly. Moreover, the results will open the way for future detailed functional analysis in the antennae of the two honeybee casts.
引文
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