Juvenile hormone prevents ecdysteroid-induced expression of broad complex rNAs in the epidermis of the tobacco hornworm, Manduca sexta

Baohua Zhou, Kiyoshi Hiruma, Tetsuro Shinoda, Lynn M. Riddiford

Research output: Contribution to journalArticle

137 Citations (Scopus)

Abstract

A cDNA homolog of the Drosophila melanogaster Broad Complex (BRC) gene was isolated from the tobacco hornworm, Manduca sexta, which shows a predicted 88% amino acid identity with Drosophila BRC in the N-terminal BTB domain. Three zinc finger domains encoding homologs of the Drosophila Z2, Z3, and Z4 domains (93, 100, and 85% identity, respectively) were obtained by RT- PCR. In Manduca dorsal abdominal epidermis, BRC RNAs were not observed during the larval molt. Three BRC transcripts - 6.0, 7.0, and 9.0 kb - first appeared at the end of the feeding stage of the fifth (final) instar when the epidermis is exposed to ecdysteroids in the absence of juvenile hormone (JH) and becomes committed to pupal differentiation. These RNAs were induced in day 2 fifth larval epidermis in vitro by 20-hydroxyecdysone (20E) in the absence of JH with dose-response and time courses similar to the induction of pupal commitment. This induction by 20E/n vitro was prevented by the presence of JH I at levels seen in vivo during the larval molt. In the wing discs, the BRC RNAs appeared shortly after ecdysis to the fifth instar and coincided with the onset of metamorphic competence of these discs. Application of a JH analogue pyriproxifen during the fourth instar molt delayed and reduced the levels of BRC mRNAs seen in the wing discs in the early fifth instar, but did not completely prevent their appearance in this tissue that first differentiates at metamorphosis. The expression of the BRC transcription factors thus appears to be one of the first molecular indications of the genetic reprogramming of the epidermis necessary for insect metamorphosis. How JH prevents BRC expression in this epidermis may provide the key to understanding how this hormone controls metamorphosis.

Original languageEnglish (US)
Pages (from-to)233-244
Number of pages12
JournalDevelopmental Biology
Volume203
Issue number2
DOIs
StatePublished - Nov 15 1998
Externally publishedYes

Fingerprint

Ecdysteroids
Manduca
Juvenile Hormones
Epidermis
RNA
Drosophila
Ecdysterone
Molting
Zinc Fingers
Drosophila melanogaster
Mental Competency
Reaction Time
Insects
Molecular Biology
Transcription Factors
Complementary DNA
Hormones
Amino Acids
Polymerase Chain Reaction
Messenger RNA

Keywords

  • 20-hydroxyecdysone
  • Broad Complex
  • Epidermal reprogramming
  • Insect metamorphosis
  • Juvenile hormone
  • Manduca sexta

ASJC Scopus subject areas

  • Developmental Biology

Cite this

Juvenile hormone prevents ecdysteroid-induced expression of broad complex rNAs in the epidermis of the tobacco hornworm, Manduca sexta. / Zhou, Baohua; Hiruma, Kiyoshi; Shinoda, Tetsuro; Riddiford, Lynn M.

In: Developmental Biology, Vol. 203, No. 2, 15.11.1998, p. 233-244.

Research output: Contribution to journalArticle

@article{f12e49ba6c704f1687b92984f3d2b65c,
title = "Juvenile hormone prevents ecdysteroid-induced expression of broad complex rNAs in the epidermis of the tobacco hornworm, Manduca sexta",
abstract = "A cDNA homolog of the Drosophila melanogaster Broad Complex (BRC) gene was isolated from the tobacco hornworm, Manduca sexta, which shows a predicted 88{\%} amino acid identity with Drosophila BRC in the N-terminal BTB domain. Three zinc finger domains encoding homologs of the Drosophila Z2, Z3, and Z4 domains (93, 100, and 85{\%} identity, respectively) were obtained by RT- PCR. In Manduca dorsal abdominal epidermis, BRC RNAs were not observed during the larval molt. Three BRC transcripts - 6.0, 7.0, and 9.0 kb - first appeared at the end of the feeding stage of the fifth (final) instar when the epidermis is exposed to ecdysteroids in the absence of juvenile hormone (JH) and becomes committed to pupal differentiation. These RNAs were induced in day 2 fifth larval epidermis in vitro by 20-hydroxyecdysone (20E) in the absence of JH with dose-response and time courses similar to the induction of pupal commitment. This induction by 20E/n vitro was prevented by the presence of JH I at levels seen in vivo during the larval molt. In the wing discs, the BRC RNAs appeared shortly after ecdysis to the fifth instar and coincided with the onset of metamorphic competence of these discs. Application of a JH analogue pyriproxifen during the fourth instar molt delayed and reduced the levels of BRC mRNAs seen in the wing discs in the early fifth instar, but did not completely prevent their appearance in this tissue that first differentiates at metamorphosis. The expression of the BRC transcription factors thus appears to be one of the first molecular indications of the genetic reprogramming of the epidermis necessary for insect metamorphosis. How JH prevents BRC expression in this epidermis may provide the key to understanding how this hormone controls metamorphosis.",
keywords = "20-hydroxyecdysone, Broad Complex, Epidermal reprogramming, Insect metamorphosis, Juvenile hormone, Manduca sexta",
author = "Baohua Zhou and Kiyoshi Hiruma and Tetsuro Shinoda and Riddiford, {Lynn M.}",
year = "1998",
month = "11",
day = "15",
doi = "10.1006/dbio.1998.9059",
language = "English (US)",
volume = "203",
pages = "233--244",
journal = "Developmental Biology",
issn = "0012-1606",
publisher = "Academic Press Inc.",
number = "2",

}

TY - JOUR

T1 - Juvenile hormone prevents ecdysteroid-induced expression of broad complex rNAs in the epidermis of the tobacco hornworm, Manduca sexta

AU - Zhou, Baohua

AU - Hiruma, Kiyoshi

AU - Shinoda, Tetsuro

AU - Riddiford, Lynn M.

PY - 1998/11/15

Y1 - 1998/11/15

N2 - A cDNA homolog of the Drosophila melanogaster Broad Complex (BRC) gene was isolated from the tobacco hornworm, Manduca sexta, which shows a predicted 88% amino acid identity with Drosophila BRC in the N-terminal BTB domain. Three zinc finger domains encoding homologs of the Drosophila Z2, Z3, and Z4 domains (93, 100, and 85% identity, respectively) were obtained by RT- PCR. In Manduca dorsal abdominal epidermis, BRC RNAs were not observed during the larval molt. Three BRC transcripts - 6.0, 7.0, and 9.0 kb - first appeared at the end of the feeding stage of the fifth (final) instar when the epidermis is exposed to ecdysteroids in the absence of juvenile hormone (JH) and becomes committed to pupal differentiation. These RNAs were induced in day 2 fifth larval epidermis in vitro by 20-hydroxyecdysone (20E) in the absence of JH with dose-response and time courses similar to the induction of pupal commitment. This induction by 20E/n vitro was prevented by the presence of JH I at levels seen in vivo during the larval molt. In the wing discs, the BRC RNAs appeared shortly after ecdysis to the fifth instar and coincided with the onset of metamorphic competence of these discs. Application of a JH analogue pyriproxifen during the fourth instar molt delayed and reduced the levels of BRC mRNAs seen in the wing discs in the early fifth instar, but did not completely prevent their appearance in this tissue that first differentiates at metamorphosis. The expression of the BRC transcription factors thus appears to be one of the first molecular indications of the genetic reprogramming of the epidermis necessary for insect metamorphosis. How JH prevents BRC expression in this epidermis may provide the key to understanding how this hormone controls metamorphosis.

AB - A cDNA homolog of the Drosophila melanogaster Broad Complex (BRC) gene was isolated from the tobacco hornworm, Manduca sexta, which shows a predicted 88% amino acid identity with Drosophila BRC in the N-terminal BTB domain. Three zinc finger domains encoding homologs of the Drosophila Z2, Z3, and Z4 domains (93, 100, and 85% identity, respectively) were obtained by RT- PCR. In Manduca dorsal abdominal epidermis, BRC RNAs were not observed during the larval molt. Three BRC transcripts - 6.0, 7.0, and 9.0 kb - first appeared at the end of the feeding stage of the fifth (final) instar when the epidermis is exposed to ecdysteroids in the absence of juvenile hormone (JH) and becomes committed to pupal differentiation. These RNAs were induced in day 2 fifth larval epidermis in vitro by 20-hydroxyecdysone (20E) in the absence of JH with dose-response and time courses similar to the induction of pupal commitment. This induction by 20E/n vitro was prevented by the presence of JH I at levels seen in vivo during the larval molt. In the wing discs, the BRC RNAs appeared shortly after ecdysis to the fifth instar and coincided with the onset of metamorphic competence of these discs. Application of a JH analogue pyriproxifen during the fourth instar molt delayed and reduced the levels of BRC mRNAs seen in the wing discs in the early fifth instar, but did not completely prevent their appearance in this tissue that first differentiates at metamorphosis. The expression of the BRC transcription factors thus appears to be one of the first molecular indications of the genetic reprogramming of the epidermis necessary for insect metamorphosis. How JH prevents BRC expression in this epidermis may provide the key to understanding how this hormone controls metamorphosis.

KW - 20-hydroxyecdysone

KW - Broad Complex

KW - Epidermal reprogramming

KW - Insect metamorphosis

KW - Juvenile hormone

KW - Manduca sexta

UR - http://www.scopus.com/inward/record.url?scp=0032533298&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0032533298&partnerID=8YFLogxK

U2 - 10.1006/dbio.1998.9059

DO - 10.1006/dbio.1998.9059

M3 - Article

VL - 203

SP - 233

EP - 244

JO - Developmental Biology

JF - Developmental Biology

SN - 0012-1606

IS - 2

ER -