The single fgf receptor gene in the beetle Tribolium castaneum codes for two isoforms that integrate FGF8- and Branchless-dependent signals

• Published in: Developmental biology Vol. 402; no. 2; pp. 264 - 275
• Main Authors: Sharma, Rahul, Beer, Katharina, Iwanov, Katharina, Schmöhl, Felix, Beckmann, Paula Indigo, Schröder, Reinhard
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 15.06.2015
• Subjects: Animals; Base Sequence; DNA Primers - genetics; Embryo, Nonmammalian - metabolism; Embryo, Nonmammalian - ultrastructure; Evolution; Evolution, Molecular; Exon-specific RNAi; FGFR; Fibroblast Growth Factor 8 - metabolism; Insect Proteins - genetics; Insect Proteins - metabolism; Larva - metabolism; Larva - ultrastructure; Molecular Sequence Data; Protein Isoforms - genetics; Protein Isoforms - physiology; Receptors, Fibroblast Growth Factor - genetics; RNA Interference; Sequence Analysis, DNA; Sialoglycoproteins - genetics; Signal Transduction - genetics; Signal Transduction - physiology; Signalling; Tribolium; Tribolium - genetics; Evolution; Signalling; Exon-specific RNAi; FGFR; Tribolium
• ISSN: 0012-1606; 1095-564X
• DOI: 10.1016/j.ydbio.2015.04.001

The precise regulation of cell–cell communication by numerous signal-transduction pathways is fundamental for many different processes during embryonic development. One important signalling pathway is the evolutionary conserved fibroblast-growth-factor (FGF)-pathway that controls processes like cell migration, axis specification and mesoderm formation in vertebrate and invertebrate animals. In the model insect Drosophila, the FGF ligand / receptor combinations of FGF8 (Pyramus and Thisbe) / Heartless (Htl) and Branchless (Bnl) / Breathless (Btl) are required for the migration of mesodermal cells and for the formation of the tracheal network respectively with both the receptors functioning independently of each other. However, only a single fgf-receptor gene (Tc-fgfr) has been identified in the genome of the beetle Tribolium. We therefore asked whether both the ligands Fgf8 and Bnl could transduce their signal through a common FGF-receptor in Tribolium. Indeed, we found that the function of the single Tc-fgfr gene is essential for mesoderm differentiation as well as for the formation of the tracheal network during early development. Ligand specific RNAi for Tc-fgf8 and Tc-bnl resulted in two distinct non-overlapping phenotypes of impaired mesoderm differentiation and abnormal formation of the tracheal network in Tc-fgf8- and Tc-bnlRNAi embryos respectively. We further show that the single Tc-fgfr gene encodes at least two different receptor isoforms that are generated through alternative splicing. We in addition demonstrate through exon-specific RNAi their distinct tissue-specific functions. Finally, we discuss the structure of the fgf-receptor gene from an evolutionary perspective. •First functional study of the FGF ligands Fgf8 and Branchless and FGFR in Tribolium.•Strong reduction of mesoderm in fgf8- and fgfr-RNAi embryos.•Tracheal development is impaired in branchless and fgfr-RNAi embryos.•Multifunctionality of the sole Fgf-receptor gene in Tribolium made possible through differential splicing.•Similar as in vertebrate FGFR but different to Drosophila, exon swapping creates alternative IG-domains.