Gene Duplication, Lineage-Specific Expansion, and Subfunctionalization in the MADF-BESS Family Patterns theDrosophilaWing Hinge

Abstract

Gene duplication, expansion, and subsequent diversification are features of the evolutionary process. Duplicated genes can be lost, modified, or altered to generate novel functions over evolutionary timescales. These features make gene duplication a powerful engine of evolutionary change. In this study, we explore these features in the MADF-BESS family of transcriptional regulators. In Drosophila melanogaster, the family contains 16 similar members, each containing an N-terminal, DNA-binding MADF domain and a C-terminal, protein-interacting, BESS domain. Phylogenetic analysis shows that members of the MADF-BESS family are expanded in the Drosophila lineage. Three members, which we name hinge1, hinge2, and hinge3 are required for wing development, with a critical role in the wing hinge. hinge1 is a negative regulator of Winglesss expression and interacts with core wing-hinge patterning genes such as teashirt, homothorax, and jing. Double knockdowns along with heterologous rescue experiments are used to demonstrate that members of the MADF-BESS family retain function in the wing hinge, in spite of expansion and diversification for over 40 million years. The wing hinge connects the blade to the thorax and has critical roles in fluttering during flight. MADF-BESS family genes appear to retain redundant functions to shape and form elements of the wing hinge in a robust and fail-safe manner.

Comparative Evidence of an Exceptional Impact of Gene Duplication on the Developmental Evolution of Drosophila and the Higher Diptera

“…Recent gene-specific and genome-wide studies, however, produced evidence for a role of genetic redundancy in securing developmental, genetic, and environmental robustness over hundreds of millions of years in part through conservation of genetically redundant gene paralogs (Celniker et al, 2002;Maslov et al, 2004;Pasek et al, 2006;Dean et al, 2008;Vavouri et al, 2008;Yang et al, 2009;Bao et al, 2012;Buscà et al, 2015). As an example, the recent discovery of partially, yet longterm conserved redundant roles of paralogs of the Drosophila lineage expanded MADF-BESS transcription factor family in the development of the wing hinge has been proposed to be explained by the benefit of developmental robustness (Shukla et al, 2014).…”

Evolution of theD. melanogasterchromatin landscape and its associated proteins

“…Among all known proteins (not just the ones in our data set) with an inferred BESS domain (InterPro identifier IPR004210), more than 80% are restricted to insects and more than 50% are restricted to diptera. A comparison among drosophilids has shown that the BESS domain family expanded through duplications in a lineage-specific way approximately 40 million years ago (Shukla et al 2014). In our dataset, five of 107 proteins have a BESS domain (SU(VAR)3-7, LHR, BEAF-32, CC20, and CC25).…”

Drosophila domino Exhibits Genetic Interactions with a Wide Spectrum of Chromatin Protein-Encoding Loci

“…The MADF domain is similar to the SANT domain (a domain found in Dom, as well as ISWI and BRM), and was first identified in the transcriptional activator, Adh transcription factor 1 (Adf-1). Proteins with the MADF domain have been found to act as both activators and repressors [ 35 ]. It may be relevant that 4 of the 5 proteins in our study that contain a MADF domain behaved similarly in the assay for dom modification ( Table 1 ).…”