Lin Gee-Way, Chen Chih-Kuan, Jiang Ting-Xin, Liang Ya-Chen, Tang Pin-Chi, Wu Ping, Widelitz Randall B, Chen Chih-Feng, Chuong Cheng-Ming
Department of Pathology, Keck School of Medicine, University of Southern California, Los Angeles, California, United States of America.
Department of Biochemistry and Molecular Cell Biology, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan.
PLoS Genet. 2025 May 12;21(5):e1011693. doi: 10.1371/journal.pgen.1011693. eCollection 2025 May.
Feathers, the primary skin appendage covering the avian body, undergo dynamic phenotypic changes throughout a bird's life. Males and females of the same species can exhibit sexually dichromatic plumage colors which play a critical role in mating choice, survival, and ecological interactions. In this study, we investigate the molecular mechanisms underlying the changes of color that occur during the transition from juvenile to adult feathers, known as the secondary transition. We focus on sexual dichromatism of craniofacial plumage and use the male cheek domain of the zebra finch (Taeniopygia guttata) as the major model. The transcriptome of the cheek and scalp (crown) domains in males and females of wild-type and genetic color variants were compared. We found that (1) Craniofacial color patterning operates through two regulatory layers. The first layer involves transcription factor (TF) genes that define the cheek domain such as PITX1, PAX1, PAX6. The second layer comprises pigment-related genes responsible for specific colors, including male-biased TFs (SOX10 and DMRT1) and transporters associated with red pigment synthesis. (2) Surprisingly, ASIP, which controls pheomelanin production in other species, was expressed in both male (red) and female (gray) cheeks. Instead, PAX1 in cheek dermal fibroblasts may serve as an upstream regulator, potentially triggering the male-biased color pattern through PAX6 and SOX10. PAX6 and SOX10 in melanocytes potentially enhance the expression of GPR143, SLC45A2, and TMEM163, driving increased pheomelanin production in males. (3) Sexual dichromatism is associated with sex-linked genes on the Z chromosome, notably SLC45A2. In addition, motif analysis comparing the binding strength between regional transcription factors and melanogenesis genes suggests that craniofacial pigmentation may have evolved convergently in passerine birds. These findings provide novel insights into the molecular control of color patterning and lay the groundwork for further studies on avian sexual dichromatism and secondary feather transition.
羽毛是覆盖鸟类身体的主要皮肤附属物，在鸟类的一生中会经历动态的表型变化。同一物种的雄性和雌性可能表现出两性异色的羽毛颜色，这在配偶选择、生存和生态相互作用中起着关键作用。在本研究中，我们调查了从幼羽到成羽转变过程中发生的颜色变化的分子机制，这一过程被称为二次转变。我们专注于颅面部羽毛的两性异色现象，并以斑胸草雀（Taeniopygia guttata）的雄性脸颊区域作为主要模型。比较了野生型和遗传颜色变体的雄性和雌性脸颊和头皮（头顶）区域的转录组。我们发现：（1）颅面部颜色图案通过两个调控层起作用。第一层涉及定义脸颊区域的转录因子（TF）基因，如PITX1、PAX1、PAX6。第二层包括负责特定颜色的色素相关基因，包括雄性偏向的TF（SOX10和DMRT1）以及与红色色素合成相关的转运蛋白。（2）令人惊讶的是，在其他物种中控制褐黑素产生的ASIP在雄性（红色）和雌性（灰色）脸颊中均有表达。相反，脸颊真皮成纤维细胞中的PAX1可能作为上游调节因子，可能通过PAX6和SOX10触发雄性偏向的颜色图案。黑素细胞中的PAX6和SOX10可能增强GPR143、SLC45A2和TMEM163的表达，从而促使雄性中褐黑素生成增加。（3）两性异色与Z染色体上的性连锁基因有关，特别是SLC45A2。此外，比较区域转录因子与黑素生成基因之间结合强度的基序分析表明，颅面部色素沉着可能在雀形目鸟类中趋同进化。这些发现为颜色图案的分子控制提供了新的见解，并为进一步研究鸟类两性异色和二次羽毛转变奠定了基础。
