Department of Biology, Syracuse University, Syracuse, NY, United States of America.
Center for Reproductive Evolution, Department of Biology, Syracuse University, Syracuse, NY, United States of America.
PLoS Genet. 2018 Feb 15;14(2):e1007219. doi: 10.1371/journal.pgen.1007219. eCollection 2018 Feb.
Environmental stress during early development in animals can have profound effects on adult phenotypes via programmed changes in gene expression. Using the nematode C. elegans, we demonstrated previously that adults retain a cellular memory of their developmental experience that is manifested by differences in gene expression and life history traits; however, the sophistication of this system in response to different environmental stresses, and how it dictates phenotypic plasticity in adults that contribute to increased fitness in response to distinct environmental challenges, was unknown. Using transcriptional profiling, we show here that C. elegans adults indeed retain distinct cellular memories of different environmental conditions. We identified approximately 500 genes in adults that entered dauer due to starvation that exhibit significant opposite ("seesaw") transcriptional phenotypes compared to adults that entered dauer due to crowding, and are distinct from animals that bypassed dauer. Moreover, we show that two-thirds of the genes in the genome experience a 2-fold or greater seesaw trend in gene expression, and based upon the direction of change, are enriched in large, tightly linked regions on different chromosomes. Importantly, these transcriptional programs correspond to significant changes in brood size depending on the experienced stress. In addition, we demonstrate that while the observed seesaw gene expression changes occur in both somatic and germline tissue, only starvation-induced changes require a functional GLP-4 protein necessary for germline development, and both programs require the Argonaute CSR-1. Thus, our results suggest that signaling between the soma and the germ line can generate phenotypic plasticity as a result of early environmental experience, and likely contribute to increased fitness in adverse conditions and the evolution of the C. elegans genome.
动物早期发育过程中的环境压力可以通过基因表达的程序性改变对成年表型产生深远影响。我们之前使用线虫 C. elegans 证明，成年动物保留了其发育经历的细胞记忆，表现为基因表达和生活史特征的差异；然而，这个系统对不同环境压力的复杂反应，以及它如何决定成年动物的表型可塑性，从而增加对不同环境挑战的适应性，这些都还不清楚。我们通过转录谱分析表明，C. elegans 成年动物确实保留了对不同环境条件的不同细胞记忆。我们发现大约 500 个在饥饿条件下进入 dauer 状态的成年动物的基因表现出与因拥挤而进入 dauer 状态的成年动物显著相反的（“跷跷板”）转录表型，并且与绕过 dauer 状态的动物不同。此外，我们表明，基因组中三分之二的基因经历了两倍或更大的跷跷板趋势的基因表达变化，并且根据变化的方向，在不同染色体上的大的、紧密连锁的区域中富集。重要的是，这些转录程序对应于根据所经历的压力而发生的明显的繁殖力变化。此外，我们证明，虽然观察到的跷跷板基因表达变化发生在体细胞和生殖细胞组织中，但只有饥饿诱导的变化需要功能性 GLP-4 蛋白，该蛋白对于生殖细胞发育是必需的，并且这两个程序都需要 Argonaute CSR-1。因此，我们的结果表明，体细胞和生殖系之间的信号传递可以产生表型可塑性，作为早期环境经验的结果，并且可能有助于在不利条件下增加适应性和 C. elegans 基因组的进化。
