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Dev Biol. 2014 Jun 15;390(2):221-30. doi: 10.1016/j.ydbio.2014.03.006. Epub 2014 Mar 22.

Importance of juvenile hormone signaling arises with competence of insect larvae to metamorphose.

Author information

1
Biology Center, Academy of Sciences of the Czech Republic, 37005 Ceske Budejovice, Czech Republic; Department of Molecular Biology, Faculty of Sciences, University of South Bohemia, 37005 Ceske Budejovice, Czech Republic.
2
National Institute of Agrobiological Sciences, Tsukuba, Ibaraki 305-8634, Japan.
3
Biology Center, Academy of Sciences of the Czech Republic, 37005 Ceske Budejovice, Czech Republic.
4
Biology Center, Academy of Sciences of the Czech Republic, 37005 Ceske Budejovice, Czech Republic; Animal, Food and Health Sciences Division, Commonwealth Scientific and Industrial Research Organization, North Ryde, NSW 2113, Australia. Electronic address: jindra@entu.cas.cz.

Abstract

Juvenile hormone (JH) postpones metamorphosis of insect larvae until they have attained an appropriate stage and size. Then, during the final larval instar, a drop in JH secretion permits a metamorphic molt that transforms larvae to adults either directly (hemimetaboly) or via a pupal stage (holometaboly). In both scenarios, JH precludes metamorphosis by activating the Kr-h1 gene through a JH receptor, Methoprene-tolerant (Met). Removal of Met, Kr-h1, or JH itself triggers deleterious precocious metamorphosis. Although JH is thought to maintain the juvenile status throughout larval life, various methods of depleting JH failed to induce metamorphosis in early-instar larvae. To determine when does JH signaling become important for the prevention of precocious metamorphosis, we chose the hemimetabolous bug, Pyrrhocoris apterus, and the holometabolous silkworm, Bombyx mori. Both species undergo a fixed number of five larval instars. Pyrrhocoris larvae subjected to RNAi-mediated knockdown of Met or Kr-h1 underwent precocious adult development when treated during the fourth (penultimate) instar, but younger larvae proved increasingly resistant to loss of either gene. The earliest instar developing minor signs of precocious metamorphosis was the third. Therefore, the JH-response genes may not be required to maintain the larval program during the first two larval instars. Next, we examined Bombyx mod mutants that cannot synthesize authentic, epoxidized forms of JH. Although mod larvae expressed Kr-h1 mRNA at severely reduced levels since hatching, they only entered metamorphosis by pupating after four, rarely three instars. Based on findings in Pyrrhocoris and Bombyx, we propose that insect postembryonic development is initially independent of JH. Only later, when larvae gain competence to enter metamorphosis, JH signaling becomes necessary to prevent precocious metamorphosis and to optimize growth.

KEYWORDS:

Heterochronic development; Hormonal signaling; Insect metamorphosis; Juvenile hormone; Krüppel homolog 1; Methoprene-tolerant

PMID:
24662045
DOI:
10.1016/j.ydbio.2014.03.006
[Indexed for MEDLINE]
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