Holometabolic insects such as flies or moths have a very special life cycle. They change shape during development as they progress from larval to pupal and adult stages. The critical processes through these transitions are moulting and metamorphosis. How these processes are controlled is an outstanding question among insect physiologists. It is well known that three hormones control moulting and metamorphosis, i.e. prothoracicotropic hormone,ecdysteroids and juvenile hormone (JH). The juvenile hormone's function is to modulate the action of ecdysteroids and to determine the nature of the moult;whether the insects will pass through a larval to larval, larval to pupal or pupal to adult moult. But juvenile hormone does even more as new research shows. The husband-and-wife team, James Truman and Lynn Riddiford, together with co-workers, has recently demonstrated in Science that juvenile hormone suppresses imaginal disc formation and differentiation independently of the action of ecdysteroids.

Imaginal discs are primordial tissues in the larvae, which store small groups of premature embryonic cells that are ready to develop into adult organs, such as wings, legs or antennae, as soon as metamorphosis is initiated. To investigate the control of imaginal disc morphogenesis, the scientists analysed the influence of the nutritional-state and juvenile hormone levels on this process in the tobacco hornworm, Manduca sexta.

In the final larval stage of development, juvenile hormone levels typically decline in the insect's blood, triggering the onset of imaginal disc morphogenesis. When the scientists starved larvae, the formation and growth of imaginal discs ceased; the team concluded that juvenile hormone functions to suppress imaginal disc morphogenesis, as starvation is known to raise juvenile hormone levels. Testing the effects of juvenile hormone on imaginal disc development further, the scientists removed the corpora allata (the organ that secretes juvenile hormone) to reduce the hormone levels, and found that the imaginal disc developed, regardless of whether the larvae had been starved. Interestingly, control of disc morphogenesis is independent from ecdysteroids, since the placement of ligatures to generate ecdysteroid-free portions did not interfere with the development of affected discs.

The action of juvenile hormone also appears to be independent of the insect's nutrition state, as starved larvae that had lost the corpora allata, but received a dose of a juvenile hormone mimic, showed inhibited disc morphogenesis. Thus, juvenile hormone can function as an intrinsic signal to inhibit imaginal disc morphogenesis. However, extrinsic signals that are nutrient-dependent also seem to be involved in this process, as the imaginal disc of well-fed larvae began developing during morphogenesis, overriding the inhibitory action of juvenile hormone. To date, the precise nature of the involved factors is unknown.

Even though feeding overrides juvenile hormone suppression of imaginal disc development in the last larval stage, subsequent steps in disc differentiation are still affected by juvenile hormone. For example, insects that received juvenile hormone early in the last instar showed normal early disc differentiation, which became aberrant after the second day; growth and the number of cell divisions in the imaginal disc declined compared with control animals. Thus, juvenile hormone appears to affect two different phases of disc growth: the initial formation and growth of the disc and the subsequent differentiation of the disc into more complex structures. Most importantly,nutrition-dependent factors appear only to block the initial phase of disc formation but not subsequent differentiation steps.

In summary, the team demonstrated that imaginal disc morphogenesis is controlled by both, nutrient-dependent factors and juvenile hormone,independently of ecdysteroids. Without juvenile hormone the growth of the discs resembles that of tumors, but when juvenile hormone is present disc growth is coordinated with that of the other larval tissues. Molecules with similar properties to juvenile hormone may therefore turn out to be potent anti-tumor agents.

References

Truman, J. W., Hiruma, K., Allee, J. P., MacWhinnie, S. G. B.,Champlin, D. T. and Riddiford, L. M. (
2006
). Juvenile hormone is required to couple imaginal disc formation with nutrition in insects.
Science
312
,
1385
-1389.