Role of the Forkhead Transcription Factors Fd4 and Fd5 During Leg Development

Overview

Journal Front Cell Dev Biol

Specialty Cell Biology

Date 2021 Aug 19

PMID 34409041

Citations 1

Authors

Mireya Ruiz-Losada

Cristian Perez-Reyes

Carlos Estella

Affiliations

Soon will be listed here.

Abstract

Appendage development requires the coordinated function of signaling pathways and transcription factors to pattern the leg along the three main axes: the antero-posterior (AP), proximo-distal (PD), and dorso-ventral (DV). The leg DV axis is organized by two morphogens, Decapentaplegic (Dpp), and Wingless (Wg), which direct dorsal and ventral cell fates, respectively. However, how these signals regulate the differential expression of its target genes is mostly unknown. In this work, we found that two members of the forkhead family of transcription factors, Fd4 and Fd5 (also known as and ), are identically expressed in the ventro-lateral domain of the leg imaginal disc in response to Dpp signaling. Here, we analyze the expression regulation and function of these genes during leg development. We have generated specific mutant alleles for each gene and a double mutant chromosome to study their function during development. We highlight the redundant role of the genes during the formation of the sex comb, a male specific structure that appears in the ventro-lateral domain of the prothoracic leg.

Citing Articles

A single-cell atlas of the sexually dimorphic Drosophila foreleg and its sensory organs during development.

Hopkins B, Barmina O, Kopp A PLoS Biol. 2023; 21(6):e3002148.

PMID: 37379332 PMC: 10335707. DOI: 10.1371/journal.pbio.3002148.

References

Kopp A . Drosophila sex combs as a model of evolutionary innovations. Evol Dev. 2012; 13(6):504-22. PMC: 3462374. DOI: 10.1111/j.1525-142X.2011.00507.x. View

Prpic N, Wigand B, Damen W, Klingler M . Expression of dachshund in wild-type and Distal-less mutant Tribolium corroborates serial homologies in insect appendages. Dev Genes Evol. 2001; 211(10):467-77. DOI: 10.1007/s004270100178. View

Ober K, Jockusch E . The roles of wingless and decapentaplegic in axis and appendage development in the red flour beetle, Tribolium castaneum. Dev Biol. 2006; 294(2):391-405. DOI: 10.1016/j.ydbio.2006.02.053. View

Estella C, McKay D, Mann R . Molecular integration of wingless, decapentaplegic, and autoregulatory inputs into Distalless during Drosophila leg development. Dev Cell. 2008; 14(1):86-96. PMC: 2709787. DOI: 10.1016/j.devcel.2007.11.002. View

Arora K, Dai H, Kazuko S, Jamal J, OConnor M, Letsou A . The Drosophila schnurri gene acts in the Dpp/TGF beta signaling pathway and encodes a transcription factor homologous to the human MBP family. Cell. 1995; 81(5):781-90. DOI: 10.1016/0092-8674(95)90539-1. View

Brook W . T-box genes organize the dorsal ventral leg axis in Drosophila melanogaster. Fly (Austin). 2010; 4(2):159-62. DOI: 10.4161/fly.4.2.11251. View

Heingard M, Turetzek N, Prpic N, Janssen R . , a new and highly conserved key factor in arthropod dorsal-ventral (DV) limb patterning. Evodevo. 2019; 10:28. PMC: 6842170. DOI: 10.1186/s13227-019-0141-6. View

Lecuit T, Cohen S . Proximal-distal axis formation in the Drosophila leg. Nature. 1997; 388(6638):139-45. DOI: 10.1038/40563. View

Svendsen P, Ryu J, Brook W . The expression of the T-box selector gene midline in the leg imaginal disc is controlled by both transcriptional regulation and cell lineage. Biol Open. 2015; 4(12):1707-14. PMC: 4736030. DOI: 10.1242/bio.013565. View

10.

Couderc J, Godt D, Zollman S, Chen J, Li M, Tiong S . The bric à brac locus consists of two paralogous genes encoding BTB/POZ domain proteins and acts as a homeotic and morphogenetic regulator of imaginal development in Drosophila. Development. 2002; 129(10):2419-33. DOI: 10.1242/dev.129.10.2419. View

11.

Boy A, Zhai Z, Habring-Muller A, Kussler-Schneider Y, Kaspar P, Lohmann I . Vectors for efficient and high-throughput construction of fluorescent drosophila reporters using the PhiC31 site-specific integration system. Genesis. 2010; 48(7):452-6. DOI: 10.1002/dvg.20637. View

12.

Burtis K, Baker B . Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell. 1989; 56(6):997-1010. DOI: 10.1016/0092-8674(89)90633-8. View

13.

McKay D, Lieb J . A common set of DNA regulatory elements shapes Drosophila appendages. Dev Cell. 2013; 27(3):306-18. PMC: 3866527. DOI: 10.1016/j.devcel.2013.10.009. View

14.

Grossmann D, Scholten J, Prpic N . Separable functions of wingless in distal and ventral patterning of the Tribolium leg. Dev Genes Evol. 2009; 219(9-10):469-79. PMC: 2811246. DOI: 10.1007/s00427-009-0310-z. View

15.

Diaz-Benjumea F, Cohen B, Cohen S . Cell interaction between compartments establishes the proximal-distal axis of Drosophila legs. Nature. 1994; 372(6502):175-9. DOI: 10.1038/372175a0. View

16.

Archbold H, Broussard C, Chang M, Cadigan K . Bipartite recognition of DNA by TCF/Pangolin is remarkably flexible and contributes to transcriptional responsiveness and tissue specificity of wingless signaling. PLoS Genet. 2014; 10(9):e1004591. PMC: 4154663. DOI: 10.1371/journal.pgen.1004591. View

17.

Hacker U, Grossniklaus U, Gehring W, Jackle H . Developmentally regulated Drosophila gene family encoding the fork head domain. Proc Natl Acad Sci U S A. 1992; 89(18):8754-8. PMC: 49999. DOI: 10.1073/pnas.89.18.8754. View

18.

Janssen R, Feitosa N, Damen W, Prpic N . The T-box genes H15 and optomotor-blind in the spiders Cupiennius salei, Tegenaria atrica and Achaearanea tepidariorum and the dorsoventral axis of arthropod appendages. Evol Dev. 2008; 10(2):143-54. DOI: 10.1111/j.1525-142X.2008.00222.x. View

19.

Brook W, Cohen S . Antagonistic interactions between wingless and decapentaplegic responsible for dorsal-ventral pattern in the Drosophila Leg. Science. 1996; 273(5280):1373-7. DOI: 10.1126/science.273.5280.1373. View

20.

Reim I, Lee H, Frasch M . The T-box-encoding Dorsocross genes function in amnioserosa development and the patterning of the dorsolateral germ band downstream of Dpp. Development. 2003; 130(14):3187-204. DOI: 10.1242/dev.00548. View