Myoglianin triggers the premetamorphosis stage in hemimetabolan insects

Abstract

Insect metamorphosis is triggered by a decrease in juvenile hormone (JH) in the final juvenile instar. What induces this decrease is therefore a relevant question. Working with the cockroach Blattella germanica, we found that myoglianin (Myo), a ligand in the TGF‐β signaling pathway, is highly expressed in the corpora allata (CA, the JH‐producing glands) and the prothoracic gland [(PG), which produce ecdysone] during the penultimate (fifth) nymphal instar (N5). In the CA, high Myo levels during N5 repress the expression of juvenile hormone acid methyl transferase, a JH biosynthesis gene. In the PG, decreasing JH levels trigger gland degeneration, regulated by the factors Krüppel homolog 1, FTZ‐F1, E93, and inhibitor of apoptosis‐1. Also in the PG, a peak of myo expression in N5 indirectly stimulates the expression of ecdysone biosynthesis genes, such as neverland, enhancing the production of the metamorphic ecdysone pulse in N6. The Myo expression peak in N5 also represses cell proliferation, which can enhance ecdysone production. The data indicate that Myo triggers the premetamorphic nymphal instar in B. germanica and possibly in other hemimetabolan insects.—Kamsoi, O., Belles, X. Myoglianin triggers the premetamorphosis stage in hemimetabolan insects. FASEB J. 33, 3659–3669 (2019). http://www.fasebj.org

TGF-beta/Activin ligand Myoglianin couples muscle growth to the initiation of metamorphosis

“…While the clearance of JH is necessary to initiate metamorphosis, 417 the threshold size assessment must occur earlier. Myo has been shown to act upstream of JH 418 signaling in hemimetabolous insects: myo knockdown leads to an increase in jhamt expression in 419 the corpora cardiaca/corpora allata (Kamsoi and Belles, 2019). Thus, Myo is likely the threshold 420 size determinant that ultimately causes a drop in JH titer.…”

“…Knockdown of Kr-h1 in the penultimate nymphal instar of the 111 firebug, Pyrrhocoris apterus, the German cockroach, Blattella germanica, and the brown 112 planthopper, Nilaparvata lugens, leads to precocious adult development (Konopova et al, 2011;113 Li et al, 2018;Lozano and Belles, 2011). In addition, silencing myoglianin (myo), a gene coding 114 for one of the ligands of the TGF-beta/Activin signaling pathway, has been shown to cause extra 115 nymphal molts (Ishimaru et al, 2016;Kamsoi and Belles, 2019): Increased expression of myo 116 has been shown to trigger the final nymphal instar in Blattella germanica (Kamsoi and Belles, 117 2019). Myo expression in the corpora allata/corpora cardiaca in the fifth (penultimate nymphal) 118 instar nymphs leads to the repression of the JH biosynthesis gene, jhamt, in the sixth (last) instar 119 nymphs (Kamsoi and Belles, 2019).…”

“…In addition, silencing myoglianin (myo), a gene coding 114 for one of the ligands of the TGF-beta/Activin signaling pathway, has been shown to cause extra 115 nymphal molts (Ishimaru et al, 2016;Kamsoi and Belles, 2019): Increased expression of myo 116 has been shown to trigger the final nymphal instar in Blattella germanica (Kamsoi and Belles, 117 2019). Myo expression in the corpora allata/corpora cardiaca in the fifth (penultimate nymphal) 118 instar nymphs leads to the repression of the JH biosynthesis gene, jhamt, in the sixth (last) instar 119 nymphs (Kamsoi and Belles, 2019). Likewise, in the field cricket, Gryllus bimaculatus, RNA 120 interference (RNAi)-mediated knockdown of myo leads to supernumerary molts accompanied by 121 an increase in jhamt expression (Ishimaru et al, 2016).…”

“…These studies demonstrate that Myo 122 regulates JH production in hemimetabolous insects. In addition, Myo has been implicated in 123 ecdysteroid production as the expression of the ecdysone biosynthesis gene neverland decreases 124 in response to myo RNAi (Kamsoi and Belles, 2019). 125…”

“…Finally, we 240 reasoned that this factor would need to be expressed in the muscle. Given that Myo is expressed 241 in the muscles (Augustin et al, 2017;Lo and Frasch, 1999) and its removal leads to 242 supernumerary molts in hemimetabolous insects (Kamsoi and Belles, 2019), we suspected that 243…”