A hemipteran insect reveals new genetic mechanisms and evolutionary insights into tracheal system development

Abstract

The diversity in the organization of the tracheal system is one of the drivers of insect evolutionary success; however, the genetic mechanisms responsible are yet to be elucidated. Here, we highlight the advantages of utilizing hemimetabolous insects, such as the milkweed bug Oncopeltus fasciatus, in which the final adult tracheal patterning can be directly inferred by examining its blueprint in embryos. By reporting the expression patterns, functions, and Hox gene regulation of trachealess (trh), ventral veinless (vvl), and cut (ct), key genes involved in tracheal development, this study provides important insights. First, Hox genes function as activators, modifiers, and suppressors of trh expression, which in turn results in a difference between the thoracic and abdominal tracheal organization. Second, spiracle morphogenesis requires the input of both trh and ct, where ct is positively regulated by trh. As Hox genes regulate trh, we can now mechanistically explain the previous observations of their effects on spiracle formation. Third, the default state of vvl expression in the thorax, in the absence of Hox gene expression, features three lateral cell clusters connected to ducts. Fourth, the exocrine scent glands express vvl and are regulated by Hox genes. These results extend previous findings [Sánchez-Higueras et al., 2014], suggesting that the exocrine glands, similar to the endocrine, develop from the same primordia that give rise to the trachea. The presence of such versatile primordia in the miracrustacean ancestor could account for the similar gene networks found in the glandular and respiratory organs of both insects and crustaceans.

Functional analysis of sense organ specification in the Tribolium castaneum larva reveals divergent mechanisms in insects

“…6 i, j; black asterisks indicating missing tracheal pits) and is in line with a previous Tc ct RNAi study [ 52 ]. Ct function in tracheal development seems to be conserved in insects [ 53 , 54 ]. Taken together, Tc ct is required to various degrees for the development of all ESO subtypes.…”

The entry of pinewood nematode is linked to programmed tracheal development of vector beetles

“…More specifically, we found that Trh, Vvl and Bnl-Btl signaling were activated during the first day post eclosion. Both Trh and Vvl are known to be the earliest upstream regulatory transcription factors activating numerous tracheal genes in insects (Hanna and Popadic, 2020; Hayashi and Kondo, 2018), whereas Bnl-Btl signaling is known to be important for guiding tracheal branch migration, as well as being involved in the establishment of tracheal pattern at multiple developmental stages (Hayashi and Kondo, 2018). In addition, transcriptional factors involved in shaping the tracheal tubes, such as knirl and salm , were also up-regulated soon after eclosion, collectively indicating that vigorous formation of primary branches occurred during the first day after the adult beetle eclosed.…”

Anterior Hox Genes and the Process of Cephalization

“…In Drosophila , Dfd and Scr are expressed transiently in the endocrine primordia where, together with STAT, mediate expression of the snail transcription factor to induce an EMT of these cells necessary for CA and PG development ( Sanchez-Higueras et al, 2014 ). In the hemipteran insect bug Oncopeltus fasciatus , RNAi against Scr disrupts prothoracic gland fate, indicating that this gene network is conserved across insects ( Hanna and Popadic, 2020 ). A recent study points out that Scr is activated in Bombyx mori larval prothoracic glands, where it negatively regulates the levels of Ecdysone to control the number of molts ( Daimon et al, 2021 ).…”