Department of Entomology, Texas A&M University, TAMU 2475, College Station, TX, 77843, USA; Department of Entomology, University of Minnesota, 219 Hodson Hall, St. Paul, MN, 55108, USA.
Department of Entomology, Texas A&M University, TAMU 2475, College Station, TX, 77843, USA.
Insect Biochem Mol Biol. 2022 Jun;145:103773. doi: 10.1016/j.ibmb.2022.103773. Epub 2022 Apr 9.
Dietary protein and digestible carbohydrates are two key macronutrients for insect herbivores, but the amounts and ratios of these two macronutrients in plant vegetative tissues can be highly variable. Typically, insect herbivores regulate their protein-carbohydrate intake by feeding selectively on nutritionally complementary plant tissues, but this may not always be possible. Interestingly, lab experiments consistently demonstrate that performance - especially growth and survival - does not vary greatly when caterpillars and nymphal grasshoppers are reared on diets that differ in their protein-carbohydrate content. This suggests insect herbivores employ post-ingestive physiological mechanisms to compensate for variation in diet protein-carbohydrate profile. However, the molecular mechanisms that underlie this compensation are not well understood. Here we explore, for the first time in an insect herbivore, the transcriptional effects of two dietary factors: protein-to-carbohydrate ratio (p:c) and total macronutrient (p + c) content. Specifically, we reared Helicoverpa zea caterpillars on three diets that varied in diet p:c ratio and one diet that varied in total p + c concentration, all within an ecologically-relevant range. We observed two key findings. Caterpillars reared on diets with elevated total p + c content showed large differences in gene expression. In contrast, only small differences in gene expression were observed when caterpillars were reared on diets with different p:c ratios (spanning from protein-biased to carbohydrate-biased). The invariable expression of many metabolic genes across these variable diets suggests that H. zea caterpillars employ a strategy of constitutive expression to deal with protein-carbohydrate imbalances rather than diet-specific changes. This is further supported by two findings. First, few genes were uniquely associated with feeding on a protein- and carbohydrate-biased diet. Second, many differentially-expressed genes were shared across protein-biased, carbohydrate-biased, and concentrated diet treatments. Our study provides insights into the post-ingestive physiological mechanisms insect herbivores employ to regulate protein-carbohydrate intake. Most notably, it suggests that H. zea, and perhaps other generalist species, use similar post-ingestive mechanisms to deal with protein-carbohydrate imbalances - regardless of the direction of the imbalance.
饮食中的蛋白质和可消化碳水化合物是昆虫食草动物的两种主要宏量营养素，但植物营养组织中这两种宏量营养素的含量和比例可能变化很大。通常，昆虫食草动物通过选择性地食用营养互补的植物组织来调节其蛋白质-碳水化合物的摄入量，但这并不总是可行的。有趣的是，实验室实验一致表明，当毛毛虫和若虫蝗虫被饲养在蛋白质-碳水化合物含量不同的饮食中时，它们的表现（尤其是生长和存活）并没有很大差异。这表明昆虫食草动物采用了摄食后生理机制来补偿饮食蛋白质-碳水化合物图谱的变化。然而，这种补偿的分子机制尚不清楚。在这里，我们首次在昆虫食草动物中探索了两种饮食因素的转录效应：蛋白质与碳水化合物的比例（p：c）和总宏量营养素（p + c）含量。具体来说，我们用三种不同的饮食来饲养玉米螟幼虫，这三种饮食的 p：c 比值不同，还有一种饮食的总 p + c 浓度不同，所有饮食都在生态相关的范围内。我们观察到两个关键发现。饲养在高总 p + c 含量饮食中的幼虫表现出显著的基因表达差异。相比之下，当幼虫饲养在不同 p：c 比值的饮食中时（从蛋白质偏置到碳水化合物偏置），只有很小的基因表达差异。在这些可变饮食中，许多代谢基因的不变表达表明，H. zea 幼虫采用了组成型表达策略来应对蛋白质-碳水化合物失衡，而不是特定于饮食的变化。这进一步得到了两个发现的支持。首先，很少有基因与进食蛋白质和碳水化合物偏置饮食有关。其次，许多差异表达基因在蛋白质偏置、碳水化合物偏置和浓缩饮食处理中共享。我们的研究提供了昆虫食草动物用于调节蛋白质-碳水化合物摄入的摄食后生理机制的见解。最值得注意的是，它表明 H. zea，也许还有其他的广食性物种，使用类似的摄食后机制来应对蛋白质-碳水化合物失衡，而不管失衡的方向如何。
