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Spalt mediates an evolutionarily conserved switch to fibrillar muscle fate in insects

Abstract

Flying insects oscillate their wings at high frequencies of up to 1,000 Hz1,2 and produce large mechanical forces of 80 W per kilogram of muscle3. They utilize a pair of perpendicularly oriented indirect flight muscles that contain fibrillar, stretch-activated myofibres. In contrast, all other, more slowly contracting, insect body muscles have a tubular muscle morphology4. Here we identify the transcription factor Spalt major (Salm) as a master regulator of fibrillar flight muscle fate in Drosophila. salm is necessary and sufficient to induce fibrillar muscle fate. salm switches the entire transcriptional program from tubular to fibrillar fate by regulating the expression and splicing of key sarcomeric components specific to each muscle type. Spalt function is conserved in insects evolutionarily separated by 280 million years. We propose that Spalt proteins switch myofibres from tubular to fibrillar fate during development, a function potentially conserved in the vertebrate heart—a stretch-activated muscle sharing features with insect flight muscle.

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Figure 1: salm specifies fibrillar flight muscle.
Figure 2: Salm expression is sufficient to induce fibrillar muscle fate.
Figure 3: vg functions upstream of salm.
Figure 4: Fibrillar insect flight muscle requires spalt function.

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Acknowledgements

We thank M. Affolter, D. Bäumer, M. Beckerle, B. Bullard, E. Chen, K. Clark, C. Desplan, K. Jagla, A. Lalouette, J. Posakony, D. Reiff, J. Saide, S. Sprecher, R. Schuh, G. Tanentzapf, J. Vigoreaux, K. VijayRaghavan, the Bloomington and the VDRC stock centres for fly stocks, antibodies and insect species. We are grateful to B. Dickson, I. Hein, M. Klingler and M. Sixt for discussions, and to R. Fässler for support and discussions. We thank A. Kaya-Copur, H. Knaut, M. Spletter and N. Vogt for critical comments on the manuscript. This work was supported by the Max-Planck-Society, a Career Development Award by the Human Frontier Science Programme to F.S., a Doc-fForte predoctoral fellowship from the Austrian Academy of Sciences to C.S., and DFG grants to M.F.

Author information

Authors and Affiliations

Authors

Contributions

C.S. performed most of the experiments, analysed the data and created most of the figures. F.S. acquired the time-lapse movies and performed western blots. J.D. and M.F conducted the Tribolium RNAi experiments, M.R. performed the microarray analysis, and N.J. and H.-U.D. were involved in the initial characterisation of the salm mutant phenotype. F.S. conceived and supervised the project and wrote the manuscript with input from C.S. and M.F.

Corresponding author

Correspondence to Frank Schnorrer.

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Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

The file contains Supplementary Figures 1-8 with legends, Supplementary Table 1, legends for Supplementary Table 2 and Supplementary Movies 1-3 and Supplementary Data for the Tc’sal fragment for RNAi injections 3320bp. (PDF 9022 kb)

Supplementary Table 2

The table shows top 500 salm targets and IFM specific genes of microarray analysis (see Supplementary Information for full legend). (XLS 493 kb)

Supplementary Movie 1

The movie shows early IFM development in a wild-type pupa (see Supplementary Information for full legend). (MOV 4343 kb)

Supplementary Movie 2

The movie shows early IFM development in a UAS-salm-IR pupa (see Supplementary Information for full legend). (MOV 4592 kb)

Supplementary Movie 3

The movie shows salm expression in developing IFMs (see Supplementary Information for full legend). (MOV 7703 kb)

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Schönbauer, C., Distler, J., Jährling, N. et al. Spalt mediates an evolutionarily conserved switch to fibrillar muscle fate in insects. Nature 479, 406–409 (2011). https://doi.org/10.1038/nature10559

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