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The Hox gene Antennapedia regulates wing development through 20-hydroxyecdysone in insect

Chunyan Fang, Yaqun Xin, Tao Sun, Antónia Monteiro, Zhanfeng Ye, Fangyin Dai, Cheng Lu, Xiaoling Tong

Preprint posted on May 27, 2021 https://www.biorxiv.org/content/10.1101/2021.05.26.445904v1

A study in the silkworm Bombyx mori reveals that the Hox gene Antennapedia has a function in wing development.

Selected by Lisa Hanna

Background:

Hox genes are transcription factors important for segment identity in bilaterian animals (Mallo and Alonso 2013). In insects, the Hox gene Antennapedia (Antp) is expressed in the thoracic regions where wings develop. However, several previous studies in the fruit fly Drosophila and the beetle Tribolium have shown that the absence of Antp does not affect wing development, suggesting that wings develop without Antp input (Carroll et al. 1995; Tomoyasu et al. 2005). Furthermore, the hindwings of insects are regulated by another Hox gene, Ultrabithorax (Ubx) (Deutsch 2005; Weatherbee et al. (1999). It has therefore long been thought that the forewings alone develop independently from any Hox gene input.

In this study, Fang et al. (2021) observed two loss of functions mutations in Antp (Nc and Wes) that lead to abnormal wing development in the silkworm Bombyx mori. The authors used wildtype and heterozygotes of the Wes mutant strain to investigate how Antp regulates wing development in B. mori.

Main findings:

  • The authors first investigated the expression levels of Antp in wildtype individuals during late development, and how it compares with the Wes mutant strain that exhibits abnormal wings. They found that Antp expression in mori was maintained at low levels during the larval stage, but increased during the pupal stage, and by comparison, these levels were overall lower in the Wes mutant strain. Next the authors dissected the wing discs during late larval development to examine when differences in morphology occur between the wildtype and mutant silkworms. They found that morphological differences appeared during the wandering stage of pupal development where the mutant strain had curlier and smaller wings than those in wildtype individuals. The authors further confirmed that Antp is responsible for the abnormal wing development via both RNAi and Crisper-Cas9 injections.
  • The authors examined whether Antp regulates wing development in mori via the regulation of the molting hormone ecdysone. Ecdysone is important for metamorphosis during pupal development and has been previously found to regulate wing growth and development in insects. They found that the gene Shade, which catalyzes ecdysone into its active form, 20-hydroxyecdysone (20E), was expressed in the wing discs, and moreover, was expressed at lower levels in the mutant strain than wildtype. This pattern was similar for titers of 20E as well. The authors also found other genes responsible for ecdysone signaling and cuticle formation, such as Ecdysone Receptor (EcR) and ultraspiracle (usp), to have lower expression levels in Antp mutants compared with wildtype, suggesting that Antp is upregulating the synthesis of 20E in the wings. Interestingly, this study also found that 20E up-regulates Antp showing a bi-directional regulation between 20E and Antp.
  • Finally, the authors investigated if Antp has a conserved function in wing development in other insects. They tested wing morphology of Drosophila and Tribolium after Antp down-regulation specifically at the pupal stage (a stage that was not examined by previous studies) and found similar effect on the wings – i.e., curlier and smaller wings than wildtype.

Overall, these results show that Antp does indeed regulate wing development in insects, contrary to findings of several previous studies. Specifically, Antp regulates wing development by up-regulating ecdysone synthesis genes and cuticle protein genes. The discovery of Antp function in wing development was possible by investigating its role during a developmental stage that was not examined previously.

 Why I chose this paper:

I chose this paper because it progresses our understanding of Hox gene functions and, more importantly, provides new evidence against a long-held understanding that Antp does not regulate wing development. This was possible because the authors investigated the role of Antp in a developmental stage that was not examined in prior studies, illustrating the importance of a comprehensive examination of development to understand the morphogenesis of a trait. Finally, this paper also illustrates that insect wing development is more intricate and involves more regulatory interactions than previously thought.

I also love the idea that re-doing old experiments using new technology can reveal new findings and change our previous understanding of gene functions.  

Questions to the Authors:

  • Why did you choose the Wes strain and not the Nc strain to test Antp function? Could the Nc strain have a mutation in a different region of Antp than the Wes strain, and possibly reveal new/different regulatory interactions?
  • Your Antp knockdown results show that Antp also controls the normal development of the hindwings. The general understanding is that Antp is suppressed by Ubx in the hindwings. If so, then how do you explain the function of Antp in the hindwings? Does Ubx function differently in the silkworm compared to other studied insects?
  • Can you elaborate more on the effect of Antp knockdown on hindwing development in Tribolium and Drosophila? Especially its role on cuticle development since in Tribolium the hindwing is membranous and has thinner cuticle than the forewings and in Drosophila the hindwing is a haltere structure.

References:

Carroll SB, Weatherb Ee SD, Langeland JA. Homeotic genes and the regulation and evolution of insect wing number. Nature. 1995;375(6526):58-61

Deutsch J. Hox and wings. Bioessays. 2005;27(7):673–5.

Mallo M, Alonso CR. The regulation of Hox gene expression during animal development. Development. 2013;140(19):3951- 63.

Tomoyasu Y, Wheeler SR, Denell RE. Ultrabithorax is required for membranous wing identity in the beetle Tribolium castaneum. Nature. 2005;433(7026):643-7.

Weatherbee SD, Halder G, Kim, J, Hudson A, Carroll S. Ultrabithorax regulates genes at several   levels of the wing-patterning hierarchy to shape the development of the Drosophila   haltere. Genes Dev. 1998;12(10):1474-82

 

 

Posted on: 20th March 2022 , updated on: 21st March 2022

doi: https://doi.org/10.1242/prelights.31681

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