Pers Daniel, Hansen Allison K
Department of Entomology, University of California, Riverside, CA 92521, USA.
Department of Biochemistry, Vanderbilt University School of Medicine, Nashville, TN 37232, USA.
G3 (Bethesda). 2021 Sep 6;11(9). doi: 10.1093/g3journal/jkab115.
Within long-term symbioses, animals integrate their physiology and development with their symbiont. In a model nutritional mutualism, aphids harbor the endosymbiont, Buchnera, within specialized bacteriocyte cells. Buchnera synthesizes essential amino acids (EAAs) and vitamins for their host, which are lacking from the aphid's plant sap diet. It is unclear if the aphid host differentially expresses aphid EAA metabolism pathways and genes that collaborate with Buchnera for the production of EAA and vitamins throughout nymphal development when feeding on plants. It is also unclear if aphid bacteriocytes are differentially methylated throughout aphid development as DNA methylation may play a role in gene regulation. By analyzing aphid gene expression, we determined that the bacteriocyte is metabolically more active in metabolizing Buchnera's EAAs and vitamins early in nymphal development compared to intermediate or later immature and adult lifestages. The largest changes in aphid bacteriocyte gene expression, especially for aphid genes that collaborate with Buchnera, occurred during the 3rd to 4th instar transition. During this transition, there is a huge shift in the bacteriocyte from a high energy "nutrient-consuming state" to a "recovery and growth state" where patterning and signaling genes and pathways are upregulated and differentially methylated, and de novo methylation is reduced as evidenced by homogenous DNA methylation profiles after the 2nd instar. Moreover, bacteriocyte number increased and Buchnera's titer decreased throughout aphid nymphal development. These data suggest in combination that bacteriocytes of older nymphal and adult lifestages depend less on the nutritional symbiosis compared to early nymphal lifestages.
在长期共生关系中，动物会将自身的生理机能和发育过程与共生体整合在一起。在一种典型的营养互利共生关系中，蚜虫在特殊的含菌细胞内携带着内共生菌布赫纳氏菌。布赫纳氏菌为其宿主合成必需氨基酸（EAA）和维生素，而这些在蚜虫的植物汁液食物中是缺乏的。目前尚不清楚，在以植物为食的若虫发育过程中，蚜虫宿主是否会差异表达蚜虫EAA代谢途径以及与布赫纳氏菌协作产生EAA和维生素的基因。同样不清楚的是，在蚜虫的整个发育过程中，含菌细胞的DNA甲基化是否存在差异，因为DNA甲基化可能在基因调控中发挥作用。通过分析蚜虫的基因表达，我们确定，与若虫发育中期、后期以及成虫阶段相比，含菌细胞在若虫发育早期代谢布赫纳氏菌的EAA和维生素时，代谢活性更高。蚜虫含菌细胞基因表达的最大变化，尤其是与布赫纳氏菌协作的蚜虫基因，发生在3龄到4龄的转变过程中。在这个转变过程中，含菌细胞发生了巨大的变化，从高能量的“营养消耗状态”转变为“恢复和生长状态”，此时模式形成和信号传导基因及途径被上调且发生差异甲基化，从头甲基化减少，这在2龄若虫后均匀的DNA甲基化图谱中得到了证明。此外，在蚜虫若虫发育过程中，含菌细胞数量增加，而布赫纳氏菌的滴度下降。这些数据综合表明，与若虫早期阶段相比，大龄若虫和成虫阶段的含菌细胞对营养共生的依赖程度较低。
