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Cited by 250Neurobiology and Insect Physiology ResearchDevelopmental Biology and Gene RegulationInsect and Arachnid Ecology and Behavior

Common and Distinct Roles of Juvenile Hormone Signaling Genes in Metamorphosis of Holometabolous and Hemimetabolous Insects

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Konopova, Barbora, Smykal, Vlastimil, Jindra, Marek·2011·PLoS ONE
DOI 10.1371/journal.pone.0028728PMC PMC3234286
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Abstract

Insect larvae metamorphose to winged and reproductive adults either directly (hemimetaboly) or through an intermediary pupal stage (holometaboly). In either case juvenile hormone (JH) prevents metamorphosis until a larva has attained an appropriate phase of development. In holometabolous insects, JH acts through its putative receptor Methoprene-tolerant (Met) to regulate Krüppel-homolog 1 (Kr-h1) and Broad-Complex (BR-C) genes. While Met and Kr-h1 prevent precocious metamorphosis in pre-final larval instars, BR-C specifies the pupal stage. How JH signaling operates in hemimetabolous insects is poorly understood. Here, we compare the function of Met, Kr-h1 and BR-C genes in the two types of insects. Using systemic RNAi in the hemimetabolous true bug, Pyrrhocoris apterus, we show that Met conveys the JH signal to prevent premature metamorphosis by maintaining high expression of Kr-h1. Knockdown of either Met or Kr-h1 (but not of BR-C) in penultimate-instar Pyrrhocoris larvae causes precocious development of adult color pattern, wings and genitalia. A natural fall of Kr-h1 expression in the last larval instar normally permits adult development, and treatment with an exogenous JH mimic methoprene at this time requires both Met and Kr-h1 to block the adult program and induce an extra larval instar. Met and Kr-h1 therefore serve as JH-dependent repressors of deleterious precocious metamorphic changes in both hemimetabolous and holometabolous juveniles, whereas BR-C has been recruited for a new role in specifying the holometabolous pupa. These results show that despite considerable evolutionary distance, insects with diverse developmental strategies employ a common-core JH signaling pathway to commit to adult morphogenesis.

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  • In cockroaches and bugs, broad is expressed through the nymphal series in a temporal fashion very similar to chinmo.

    “Studies in both cockroaches [21] and bugs [33,16,43] showed that broad is expressed through the nymphal series in a temporal fashion very similar to chinmo (Figure 4a)”

    From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [33]

    The Results (Developmental Regulation of the JH-Response Genes in Pyrrhocoris; page unavailable) report that BR-C, or broad, oscillates throughout larval development in a bug. The Discussion (page unavailable) also reports BR-C expression in the final larval instar of a cockroach. Our copy does not establish its pattern across the cockroach nymphal series or compare that pattern with chinmo. (LLM, conf=0.85)

    Experimental — accuracy not yet measured

  • Broad knockdown does not cause precocious metamorphosis in hemimetabolous insects.

    “Broad knockdown, however, does not cause precocious meta­ morphosis [21,33,16,43].”

    From Regulation of metamorphosis in holometabolous insects (2026) · cites this paper as [33]

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Authors
Konopova, B., Smykal, V., & Jindra, M.
Affiliations
Czech Academy of Sciences, Biology Centre (CZ)
Corresponding author
Jindra, Marek
ORCID
Jindra, Marek
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2011-12-08
Volume
6
Issue
12
Pages
e28728
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0028728
PMC
PMC3234286
OpenAlex
W2122924619
Cited by
250
References
2
Citations by year
2026: 15 · 2025: 21 · 2024: 15 · 2023: 11 · 2022: 22 · 2021: 19 · 2020: 22 · 2019: 26 · 2018: 15 · 2017: 13 · 2016: 10 · 2015: 18 · 2014: 21 · 2013: 14 · 2012: 7
FWCI
5.70
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • ASEP (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
Grantová Agentura České Republiky (GD204/09/H058, GA204/07/1032)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Insect and Arachnid Ecology and Behavior
Keywords
juvenile hormone signaling, metamorphosis, hemimetabolism, holometabolism, methoprene-tolerant, Krüppel homolog 1, Broad-Complex, Pyrrhocoris apterus, Heteroptera, precocious metamorphosis, methoprene, larval instars, gene regulatory evolution
MeSH terms
Aging, Animals, Insecta, Juvenile Hormones, Larva, Life Cycle Stages, Models, Biological, Repressor Proteins, Signal Transduction, Conserved Sequence, Genes, Insect, Gene Expression Regulation, Developmental

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