Hagadorn Mallory A, Hunter Frances K, DeLory Tim, Johnson Makenna M, Pitts-Singer Theresa L, Kapheim Karen M
Department of Biology, Department of Biology, Utah State University, Logan, UT, United States.
United States Department of Agriculture, Agricultural Research Service, Pollinating Insects Research Unit, Logan, UT, United States.
Front Genet. 2023 Jan 4;13:1064332. doi: 10.3389/fgene.2022.1064332. eCollection 2022.
Maternal effects are an important source of phenotypic variance, whereby females influence offspring developmental trajectory beyond direct genetic contributions, often in response to changing environmental conditions. However, relatively little is known about the mechanisms by which maternal experience is translated into molecular signals that shape offspring development. One such signal may be maternal RNA transcripts (mRNAs and miRNAs) deposited into maturing oocytes. These regulate the earliest stages of development of all animals, but are understudied in most insects. Here we investigated the effects of female internal (body condition) and external (time of season) environmental conditions on maternal RNA in the maturing oocytes and 24-h-old eggs (24-h eggs) of alfalfa leafcutting bees. Using gene expression and WGCNA analysis, we found that females adjust the quantity of mRNAs related to protein phosphorylation, transcriptional regulation, and nuclease activity deposited into maturing oocytes in response to both poor body condition and shorter day lengths that accompany the late season. However, the magnitude of these changes was higher for time of season. Females also adjusted miRNA deposition in response to seasonal changes, but not body condition. We did not observe significant changes in maternal RNAs in response to either body condition or time of season in 24-h eggs, which were past the maternal-to-zygotic transition. Our results suggest that females adjust the RNA transcripts they provide for offspring to regulate development in response to both internal and external environmental cues. Variation in maternal RNAs may, therefore, be important for regulating offspring phenotype in response to environmental change.
母体效应是表型变异的一个重要来源,即雌性会影响后代的发育轨迹,这种影响超出了直接的基因贡献,通常是对不断变化的环境条件做出的反应。然而,对于母体经历如何转化为塑造后代发育的分子信号的机制,我们了解得相对较少。一种这样的信号可能是沉积到成熟卵母细胞中的母体RNA转录本(mRNA和miRNA)。这些转录本调节所有动物发育的最早阶段,但在大多数昆虫中却未得到充分研究。在这里,我们研究了雌性内部(身体状况)和外部(季节时间)环境条件对苜蓿切叶蜂成熟卵母细胞和24小时龄卵(24小时卵)中母体RNA的影响。通过基因表达和加权基因共表达网络分析(WGCNA),我们发现雌性会根据身体状况不佳以及季节后期伴随的较短日照长度,调整沉积到成熟卵母细胞中的与蛋白质磷酸化、转录调控和核酸酶活性相关的mRNA数量。然而,这些变化的幅度在季节时间方面更高。雌性也会根据季节变化调整miRNA的沉积,但不会根据身体状况进行调整。在已经度过母型向合子型转变的24小时卵中,我们没有观察到母体RNA因身体状况或季节时间而发生显著变化。我们的结果表明,雌性会调整为后代提供的RNA转录本,以根据内部和外部环境线索调节发育。因此,母体RNA的变异对于响应环境变化调节后代表型可能很重要。