Sánchez-Serna Gaspar, Badia-Ramentol Jordi, Bujosa Paula, Ferrández-Roldán Alfonso, Torres-Águila Nuria P, Fabregà-Torrus Marc, Wibisana Johannes N, Mansfield Michael J, Plessy Charles, Luscombe Nicholas M, Albalat Ricard, Cañestro Cristian
Departament de Genètica, Microbiologia i Estadística, Facultat de Biologia, Universitat de Barcelona (UB), Barcelona 08028, Spain.
Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona (UB), Barcelona, Spain.
Mol Biol Evol. 2025 Jan 6;42(1). doi: 10.1093/molbev/msae260.
The impact of gene loss on the diversification of taxa and the emergence of evolutionary innovations remains poorly understood. Here, our investigation on the evolution of the Fibroblast Growth Factors (FGFs) in appendicularian tunicates as a case study reveals a scenario of "less, but more" characterized by massive losses of all Fgf gene subfamilies, except for the Fgf9/16/20 and Fgf11/12/13/14, which in turn underwent two bursts of duplications. Through phylogenetic analysis, synteny conservation, and gene and protein structure, we reconstruct the history of appendicularian Fgf genes, highlighting their paracrine and intracellular functions. An exhaustive analysis of developmental Fgf expression in Oikopleura dioica allows us to identify four associated evolutionary patterns characterizing the "less, but more" conceptual framework: conservation of ancestral functions; function shuffling between paralogs linked to gene losses; innovation of new functions after the duplication bursts; and function extinctions linked to gene losses. Our findings allow us to formulate novel hypotheses about the impact of Fgf losses and duplications on the transition from an ancestral ascidian-like biphasic lifestyle to the fully free-living appendicularians. These hypotheses include massive co-options of Fgfs for the development of the oikoblast and the tail fin; recruitment of Fgf11/12/13/14s into the evolution of a new mouth, and their role modulating neuronal excitability; the evolutionary innovation of an anterior tail FGF signaling source upon the loss of retinoic acid signaling; and the potential link between the loss of Fgf7/10/22 and Fgf8/17/18 and the loss of drastic metamorphosis and tail absorption in appendicularians, in contrast to ascidians.
基因缺失对分类群多样化和进化创新出现的影响仍知之甚少。在此,我们以尾海鞘纲被囊动物中纤维母细胞生长因子(FGFs)的进化为例进行研究,结果揭示了一种“少而精”的情况,其特征是除Fgf9/16/20和Fgf11/12/13/14外,所有Fgf基因亚家族均大量缺失,而后这两个亚家族经历了两次复制爆发。通过系统发育分析、共线性保守性以及基因和蛋白质结构分析,我们重建了尾海鞘纲Fgf基因的历史,突出了它们的旁分泌和细胞内功能。对异体住囊虫发育过程中Fgf表达的详尽分析使我们能够确定四种相关的进化模式,这些模式表征了“少而精”的概念框架:祖先功能的保守性;与基因缺失相关的旁系同源物之间的功能洗牌;复制爆发后新功能的创新;以及与基因缺失相关的功能灭绝。我们的研究结果使我们能够就Fgf缺失和复制对从祖先海鞘类双相生活方式向完全自由生活的尾海鞘纲转变的影响提出新的假设。这些假设包括Fgfs在卵母细胞和成尾鳍发育中的大量共同选择;Fgf11/12/13/14在新口进化中的招募及其调节神经元兴奋性的作用;视黄酸信号缺失后前尾FGF信号源的进化创新;以及与海鞘类相比,Fgf7/10/22和Fgf8/17/18的缺失与尾海鞘纲中剧烈变态和尾吸收缺失之间的潜在联系。
BMC Evol Biol. 2013-6-4
Genome Res. 2024-4-25
Nucleic Acids Res. 2024-7-5
Nat Commun. 2023-7-6
Genes Dev. 2023-2-1
WIREs Mech Dis. 2022-7
Nat Biotechnol. 2022-7