O'Hanlon Kenley N, Dam Rachel A, Archambeault Sophie L, Berg Celeste A
Department of Genome Sciences, University of Washington, 3720 15th AVE NE, Seattle, WA, 98195-5065, USA.
Molecular and Cellular Biology Program, University of Washington, 1959 NE Pacific Street, Seattle, WA, 98195-7275, USA.
Dev Genes Evol. 2018 Jan;228(1):31-48. doi: 10.1007/s00427-017-0601-8. Epub 2017 Dec 20.
Deciphering the evolution of morphological structures is a remaining challenge in the field of developmental biology. The respiratory structures of insect eggshells, called the dorsal appendages, provide an outstanding system for exploring these processes since considerable information is known about their patterning and morphogenesis in Drosophila melanogaster and dorsal appendage number and morphology vary widely across Drosophilid species. We investigated the patterning differences that might facilitate morphogenetic differences between D. melanogaster, which produces two oar-like structures first by wrapping and then elongating the tubes via cell intercalation and cell crawling, and Scaptodrosophila lebanonensis, which produces a variable number of appendages simply by cell intercalation and crawling. Analyses of BMP pathway components thickveins and P-Mad demonstrate that anterior patterning is conserved between these species. In contrast, EGF signaling exhibits significant differences. Transcripts for the ligand encoded by gurken localize similarly in the two species, but this morphogen creates a single dorsolateral primordium in S. lebanonensis as defined by activated MAP kinase and the downstream marker broad. Expression patterns of pointed, argos, and Capicua, early steps in the EGF pathway, exhibit a heterochronic shift in S. lebanonensis relative to those seen in D. melanogaster. We demonstrate that the S. lebanonensis Gurken homolog is active in D. melanogaster but is insufficient to alter downstream patterning responses, indicating that Gurken-EGF receptor interactions do not distinguish the two species' patterning. Altogether, these results differentiate EGF signaling patterns between species and shed light on how changes to the regulation of patterning genes may contribute to different tube-forming mechanisms.
解读形态结构的演化是发育生物学领域尚存的一项挑战。昆虫卵壳的呼吸结构，即背附器，为探索这些过程提供了一个绝佳的系统，因为关于其在黑腹果蝇中的模式形成和形态发生已有相当多的信息，而且背附器的数量和形态在果蝇科物种中差异很大。我们研究了可能促成黑腹果蝇与黎巴嫩果蝇形态发生差异的模式形成差异，黑腹果蝇首先通过包裹，然后通过细胞插入和细胞爬行使管子伸长，产生两个桨状结构，而黎巴嫩果蝇仅通过细胞插入和爬行产生数量可变的附器。对骨形态发生蛋白（BMP）信号通路成分粗脉和磷酸化母分化因子（P-Mad）的分析表明，这些物种之间的前部模式形成是保守的。相比之下，表皮生长因子（EGF）信号传导则表现出显著差异。由gurken编码的配体的转录本在这两个物种中的定位相似，但这种形态发生素在黎巴嫩果蝇中形成了一个单一的背外侧原基，这是由活化的丝裂原活化蛋白激酶（MAP激酶）和下游标记broad所定义的。在EGF信号通路早期阶段的pointed、argos和Capicua的表达模式，相对于在黑腹果蝇中观察到的模式，在黎巴嫩果蝇中表现出异时性转变。我们证明，黎巴嫩果蝇的Gurken同源物在黑腹果蝇中是有活性的，但不足以改变下游的模式形成反应，这表明Gurken-EGF受体相互作用并不能区分这两个物种的模式形成。总之，这些结果区分了不同物种之间的EGF信号模式，并揭示了模式形成基因调控的变化可能如何导致不同的管状结构形成机制。
