Broad complex and wing development in cockroaches

Fernández-Nicolas, Ana; Ventós-Alfonso, Alba; Kamsoi, Orathai; Clark-Hachtel, Courtney M.; Tomoyasu, Yoshinori; Bellés, Xavier

doi:10.1016/j.ibmb.2022.103798

Cited by 8 publications

(7 citation statements)

References 38 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…5 A ) is strikingly similar to that of E93 both during embryogenesis and in postembryonic development. In B. germanica , maternal RNAi experiments ( 8 , 27 ) revealed that Br-C has functions in the formation of the germinal band, as well as in other stages of embryo development. Br-C has also been shown to be important in the embryogenesis of another hemimetabolan species, namely the bug Oncopeltus fasciatus ( 7 ).…”

Section: Resultsmentioning

confidence: 99%

Reduction of embryonic E93 expression as a hypothetical driver of the evolution of insect metamorphosis

Fernández-Nicolas

Machaj

Ventós-Alfonso

et al. 2023

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

View full text Add to dashboard Cite

The early embryo of the cockroach Blattella germanica exhibits high E93 expression. In general, E93 triggers adult morphogenesis during postembryonic development. Here we show that E93 is also crucial in early embryogenesis in the cockroach, as a significant number of E93-depleted embryos are unable to develop the germ band under maternal RNAi treatment targeting E93 . Moreover, transcriptomic analysis indicates that E93 depletion results in important gene expression changes in the early embryo, and many of the differentially expressed genes are involved in development. Then, using public databases, we gathered E93 expression data in embryo and preadult stages, finding that embryonic expression of E93 is high in hemimetabolan species (whose juveniles, or nymphs, are similar to the adult) and low in holometabolans (whose juveniles, or larvae, are different from the adult). E93 expression is also low in Thysanoptera and in Hemiptera Sternorrhyncha, hemimetabolans with postembryonic quiescent stages, as well as in Odonata, the nymph of which is very different from the adult. In ametabolans, such as the Zygentoma Thermobia domestica , E93 transcript levels are very high in the early embryo, whereas during postembryonic development they are medium and relatively constant. We propose the hypothesis that during evolution, a reduction of E93 expression in the embryo of hemimetabolans facilitated the larval development and the emergence of holometaboly. Independent decreases of E93 transcripts in the embryo of Odonata, Thysanoptera, and different groups of Hemiptera Sternorrhyncha would have allowed the development of modified juvenile stages adapted to specific ecophysiological conditions.

show abstract

Section: Resultsmentioning

confidence: 99%

Reduction of embryonic E93 expression as a hypothetical driver of the evolution of insect metamorphosis

Fernández-Nicolas

Machaj

Ventós-Alfonso

et al. 2023

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

View full text Add to dashboard Cite

show abstract

“…Wing development occurs within wing buds, which appear as morphologically distinct structures in i3 and subsequently undergo incremental changes in shape and size in each successive molt (Figure 1D). However, it is likely that the wing identity of the wing bud progenitor tissue is specified already during embryogenesis as in other Hemimetabolous insects (Fernandez-Nicolas et al ., 2022; Ohde, Mito and Niimi, 2022). Post-embryonic wing development in water striders is variable, with some species developing distinctly different wing bud sizes depending on adult wing morph fate.…”

Section: Resultsmentioning

confidence: 99%

The Fat/Hippo pathway drives photoperiod-induced wing length polyphenism

Gudmunds,

Palahí,

Armisén

et al. 2024

Preprint

View full text Add to dashboard Cite

Identifying the genetic mechanisms that translate information from the environment into developmental programs to control size, shape and color are important for gaining insights into adaptation to changing environments. Insect polyphenisms provide good models to study such mechanisms because environmental factors are the main source of trait variation. Here we studied the genetic mechanism that controls photoperiod-induced wing length polyphenism in the water striderGerris buenoi. By sequencing RNA sampled from wing buds across developmental stages under different photoperiodic conditions known to trigger alternative wing developmental trajectories, we found that differences in transcriptional activity arose primarily in the late 5thinstar stage. Among the differentially expressed genes, the Fat/Hippo and ecdysone signaling pathways, both putative growth regulatory mechanisms showed significant enrichment. We used RNA interference against the differentially expressed genes Fat, Dachsous and Yorkie to assess whether they play a causative role in photoperiod induced wing length variation inGerris buenoi. Our results show that the conserved Fat/Hippo pathway is a key regulatory network involved in the control of wing polyphenism in this species. This study provides an important basis for future comparative studies on the evolution of wing polyphenism and significantly deepens our understanding of the genetic regulation of insect polyphenisms.

show abstract

“…Since hemimetabolous insects do not undergo the intermediate pupal stage, the transition from juvenile to adult, therefore, relies mainly on the shift from Chinmo to E93 during the last nymphal stage, with Kr-h1 also involved in preventing metamorphosis through the repression of E93 ( Ureña et al, 2016 ). However, although in hemimetabolans insects depletion of Br-C does not impair metamorphosis, Br-C does regulate the progressive growth of the metamorphic tissues, such as the wing pads and the dorsal thorax ( Erezyilmaz et al, 2006 ; Fernandez-Nicolas et al, 2022 ; Huang et al, 2013 ; Konopova et al, 2011 ). This observation suggests that a premetamorphic role of Br-C was already present in hemimetabolous insects, acquiring an additional metamorphic role as pupal specifier during the evolution of holometabolous insects.…”

Section: Resultsmentioning

confidence: 99%

Antagonistic role of the BTB-zinc finger transcription factors Chinmo and Broad-Complex in the juvenile/pupal transition and in growth control

Chafino

Giannios

Casanova

et al. 2023

eLife

View full text Add to dashboard Cite

During development, the growing organism transits through a series of temporally regulated morphological stages to generate the adult form. In humans, for example, development progresses from childhood through to puberty and then to adulthood, when sexual maturity is attained. Similarly, in holometabolous insects, immature juveniles transit to the adult form through an intermediate pupal stage when larval tissues are eliminated and the imaginal progenitor cells form the adult structures. The identity of the larval, pupal and adult stages depends on the sequential expression of the transcription factors chinmo, Br-C and E93. However, how these transcription factors determine temporal identity in developing tissues is poorly understood. Here we report on the role of the larval specifier chinmo in larval and adult progenitor cells during fly development. Interestingly, chinmo promotes growth in larval and imaginal tissues in a Br-C-independent and -dependent manner, respectively. In addition, we found that the absence of chinmo during metamorphosis is critical for proper adult differentiation. Importantly, we also provide evidence that, in contrast to the well-known role of chinmo as a pro-oncogene, Br-C and E93 act as tumour suppressors. Finally, we reveal that the function of chinmo as a juvenile specifier is conserved in hemimetabolous insects as its homolog has a similar role in Blatella germanica. Taken together, our results suggest that the sequential expression of the transcription factors Chinmo, Br-C and E93 during larva, pupa an adult respectively, coordinate the formation of the different organs that constitute the adut organism.

show abstract

Broad complex and wing development in cockroaches

Cited by 8 publications

References 38 publications

Reduction of embryonic E93 expression as a hypothetical driver of the evolution of insect metamorphosis

Reduction of embryonic E93 expression as a hypothetical driver of the evolution of insect metamorphosis

The Fat/Hippo pathway drives photoperiod-induced wing length polyphenism

Antagonistic role of the BTB-zinc finger transcription factors Chinmo and Broad-Complex in the juvenile/pupal transition and in growth control

Contact Info

Product

Resources

About