Juvenile hormone–dependent Kazal‐type serine protease inhibitor Greglin safeguards insect vitellogenesis and egg production

Abstract

In addition to preventing insect metamorphosis, juvenile hormone (JH) is known to stimulate aspects of insect reproduction. However, the molecular mechanisms of JH action in insect reproduction remain largely unknown. By reanalyzing the transcriptomic data from adults and other developmental stages of the migratory locust Locusta migratoria, we identified a gene coding for Kazal-type protease inhibitor, previously named Greglin. Greglin is specifically expressed in adult females and most abundant in the fat body and ovaries. Interestingly, Greglin is among the top 3 of highly expressed genes in adult female locusts, after 2 vitellogenin ( Vg) genes. Greglin is induced by JH and expressed at remarkably high levels in the vitellogenic stage. Knockdown of Greglin in adult female locusts results in accelerated degradation of serine protease substrate and significantly reduced levels of Greglin protein in hemolymph and ovaries. The consequent phenotypes include blocked oocyte maturation, arrested ovarian growth and shrunken follicular epithelium, as well as declines in egg number and hatchability. The data provide the first evidence, to our knowledge, that JH-dependent Greglin is involved in locust vitellogenesis and oocyte maturation likely by protecting vitellogenesis and other forms of yolk precursors from proteolysis. The result offers new insights into the regulation of JH and function of protease inhibitors in insect vitellogenesis, oocyte maturation and fecundity.-Guo, W., Wu, Z., Yang, L., Cai, Z., Zhao, L., Zhou, S. Juvenile hormone-dependent Kazal-type serine protease inhibitor Greglin safeguards insect vitellogenesis and egg production.

Juvenile hormone acts through FoxO to promote Cdc2 and Orc5 transcription for polyploidy-dependent vitellogenesis

“…We previously reported that hemolymph JH titers were undetectable at adult female eclosion, progressively elevated in previtellogenic phase, sharply increased in early vitellogenic stage, and rose to a peak in late vitellogenic stage (Fig. 1C) (Guo et al, 2019). Because adult female locusts started feeding 12 h post eclosion, the extremely low p-FoxO levels within 12 h after adult emergence might be primarily due to the absence of food intake.…”

Parent of origin gene expression in the bumblebee, Bombus terrestris, supports Haig’s kinship theory for the evolution of genomic imprinting

“…Most recently a kazal-type serine protease inhibitor has been directly linked to oocyte development in the desert locust Schistocerca gregaria (Guo et al, 2019). A knock-down of the protein producing gene Greglin by RNAi caused extreme effects on reproduction, including; diminished oocyte production and maturation, a decline in the number of eggs produced and hatching success (Guo et al, 2019). Future work identifying the function of serine protease inhibitors in social insects is needed to better understand the function of parent-of-origin expression of these genes in both B. terrestris and A. mellifera .…”

Protein kinase C mediates juvenile hormone–dependent phosphorylation of Na+/K+-ATPase to induce ovarian follicular patency for yolk protein uptake

“…2 (C and D), the levels of phosphorylated Na ϩ /K ϩ -ATPase ␣-subunit were significantly increased on day 2, reached peaks at 4 -7 days PAE, and then declined on day 8. As locust hemolymph JH titer is undetectable at eclosion but elevates significantly in the previtellogenic stage and rises to a peak during vitellogenesis (46,47), the elevation of Na ϩ /K ϩ -ATPase ␣-subunit phosphorylation appeared to correlate with its enhanced activity and the phase of increased JH titers.…”

“…The gregarious phase of migratory locusts was maintained under a light/dark photoperiod of 14 h/10 h and at 30 Ϯ 2°C as described previously (46). The diet included a continuous supply of wheat bran and fresh wheat seedlings provided once daily.…”