A novel gene REPTOR2 activates the autophagic degradation of wing disc in pea aphid.

A novel gene REPTOR2 activates the autophagic degradation of wing disc in pea aphid.
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DOI:
10.7554/elife.83023
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发表时间:
2023-03-21
期刊:
影响因子:
7.7
通讯作者:
Sun Y
Sun Y
中科院分区:
生物学1区
文献类型:
--
作者:
Yuan E;Guo H;Chen W;Du B;Mi Y;Qi Z;Yuan Y;Zhu-Salzman K;Ge F;Sun Y

文献摘要

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翅型是昆虫在进化过程中的一种适应性特征,通过翅型适应性来最大化昆虫在不同环境中的适应性,从而使种群在扩散和繁殖之间达到平衡。大多数研究都关注蚜虫翅膀形态刺激的调节机制,但相对较少的研究涉及翅膀丧失的分子基础。在这里,我们发现,而正常发展的翼注定豌豆蚜虫,翼盘在无翼注定蚜虫出生后30小时退化,这种退化是由于自噬,而不是细胞凋亡。一龄蚜虫自噬的激活降低了有翅蚜虫的比例,而抑制自噬则增加了有翅蚜虫的比例。REPTOR 2与TOR信号通路相关,通过RNA-seq鉴定为两种变体之间的差异表达基因,其在无翅蚜虫胸部中表达较高。进一步的遗传分析表明,REPTOR 2可能是一个新的基因,来自一个基因复制事件,只发生在豌豆蚜虫的常染色体A1,但易位到性染色体上。REPTOR 2的敲除减少了翅盘中的自噬,并增加了有翅蚜虫的比例。与REPTOR的典型的TOR对自噬的负调控作用一致,有翅膀的蚜虫在翅盘中有更高的TOR表达。抑制TOR激活翅盘的自噬,减少有翅蚜虫的比例,反之亦然。TOR和REPTOR 2的共抑制表明,dsREPTOR 2可以掩盖dsTOR对自噬的积极作用,表明REPTOR 2在信号通路中作为TOR下游的关键调节剂。这些结果表明,TOR信号通路通过负调控REPTOR 2的表达来抑制豌豆蚜虫翅盘的自噬降解。
Wing dimorphism in insects is an evolutionarily adaptive trait to maximize insect fitness under various environments, by which the population could be balanced between dispersing and reproduction. Most studies concern the regulatory mechanisms underlying the stimulation of wing morph in aphids, but relatively little research addresses the molecular basis of wing loss. Here, we found that, while developing normally in winged-destined pea aphids, the wing disc in wingless-destined aphids degenerated 30-hr postbirth and that this degeneration was due to autophagy rather than apoptosis. Activation of autophagy in first instar nymphs reduced the proportion of winged aphids, and suppression of autophagy increased the proportion. REPTOR2, associated with TOR signaling pathway, was identified by RNA-seq as a differentially expressed gene between the two morphs with higher expression in the thorax of wingless-destined aphids. Further genetic analysis indicated that REPTOR2 could be a novel gene derived from a gene duplication event that occurred exclusively in pea aphids on autosome A1 but translocated to the sex chromosome. Knockdown of REPTOR2 reduced autophagy in the wing disc and increased the proportion of winged aphids. In agreement with REPTOR’s canonical negative regulatory role of TOR on autophagy, winged-destined aphids had higher TOR expression in the wing disc. Suppression of TOR activated autophagy of the wing disc and decreased the proportion of winged aphids, and vice versa. Co-suppression of TOR and REPTOR2 showed that dsREPTOR2 could mask the positive effect of dsTOR on autophagy, suggesting that REPTOR2 acted as a key regulator downstream of TOR in the signaling pathway. These results revealed that the TOR signaling pathway suppressed autophagic degradation of the wing disc in pea aphids by negatively regulating the expression of REPTOR2.