Hu Yonggang, Crabtree Jordan R, Macagno Anna L M, Moczek Armin P
Department of Biology, Indiana University, 915 East 3rd Street, Bloomington, IN, 47405, USA.
State Key Laboratory of Resource Insects, Institute of Sericulture and Systems Biology, Southwest University, No.2 Tiansheng Road, Beibei District, Chongqing, 400715, China.
Evodevo. 2024 Apr 5;15(1):4. doi: 10.1186/s13227-024-00223-5.
Nutrient availability is among the most widespread means by which environmental variability affects developmental outcomes. Because almost all cells within an individual organism share the same genome, structure-specific growth responses must result from changes in gene regulation. Earlier work suggested that histone deacetylases (HDACs) may serve as epigenetic regulators linking nutritional conditions to trait-specific development. Here we expand on this work by assessing the function of diverse HDACs in the structure-specific growth of both sex-shared and sex-specific traits including evolutionarily novel structures in the horned dung beetle Onthophagus taurus.
We identified five HDAC members whose downregulation yielded highly variable mortality depending on which HDAC member was targeted. We then show that HDAC1, 3, and 4 operate in both a gene- and trait-specific manner in the regulation of nutrition-responsiveness of appendage size and shape. Specifically, HDAC 1, 3, or 4 knockdown diminished wing size similarly while leg development was differentially affected by RNAi targeting HDAC3 and HDAC4. In addition, depletion of HDAC3 transcript resulted in a more rounded shape of genitalia at the pupal stage and decreased the length of adult aedeagus across all body sizes. Most importantly, we find that HDAC3 and HDAC4 pattern the morphology and regulate the scaling of evolutionarily novel head and thoracic horns as a function of nutritional variation.
Collectively, our results suggest that both functional overlap and division of labor among HDAC members contribute to morphological diversification of both conventional and recently evolved appendages. More generally, our work raises the possibility that HDAC-mediated scaling relationships and their evolution may underpin morphological diversification within and across insect species broadly.
营养物质的可利用性是环境变化影响发育结果最普遍的方式之一。由于个体生物体内几乎所有细胞都共享相同的基因组，特定结构的生长反应必定源于基因调控的变化。早期研究表明，组蛋白去乙酰化酶（HDACs）可能作为表观遗传调节因子，将营养状况与特定性状的发育联系起来。在此，我们通过评估多种HDACs在雌雄共享和性别特异性性状（包括有角蜣螂Onthophagus taurus中进化上新颖的结构）的特定结构生长中的功能，对这项研究进行拓展。
我们鉴定出五个HDAC成员，其下调会导致高度可变的死亡率，具体取决于靶向的是哪个HDAC成员。然后我们表明，HDAC1、3和4在附属肢体大小和形状的营养反应调节中以基因和性状特异性方式发挥作用。具体而言，HDAC 1、3或4的敲低同样会减小翅膀大小，而腿部发育受到靶向HDAC3和HDAC4的RNA干扰差异影响。此外，HDAC3转录本的缺失导致蛹期生殖器形状更圆润，并在所有体型中缩短了成虫阳茎的长度。最重要的是，我们发现HDAC3和HDAC4根据营养变化塑造了进化上新颖的头部和胸角的形态并调节其比例。
总体而言，我们的结果表明，HDAC成员之间的功能重叠和分工共同促成了传统和最近进化的附属肢体的形态多样化。更普遍地说，我们的工作提出了一种可能性，即HDAC介导的比例关系及其进化可能广泛地支撑昆虫物种内部和之间的形态多样化。
