Formation of rigid, non-flight forewings (Elytra) of a beetle requires two major cuticular proteins

Yasuyuki Arakane, Joseph Lomakin, Stevin H. Gehrke, Yasuaki Hiromasa, John M. Tomich, Subbaratnam Muthukrishnan, Richard W. Beeman, Karl J. Kramer, Michael R. Kanost

Research output: Contribution to journalArticle

39 Citations (Scopus)

Abstract

Insect cuticle is composed primarily of chitin and structural proteins. To study the function of structural cuticular proteins, we focused on the proteins present in elytra (modified forewings that become highly sclerotized and pigmented covers for the hindwings) of the red flour beetle, Tribolium castaneum. We identified two highly abundant proteins, TcCPR27 (10 kDa) and TcCPR18 (20 kDa), which are also present in pronotum and ventral abdominal cuticles. Both are members of the Rebers and Riddiford family of cuticular proteins and contain RR2 motifs. Transcripts for both genes dramatically increase in abundance at the pharate adult stage and then decline quickly thereafter. Injection of specific double-stranded RNAs for each gene into penultimate or last instar larvae had no effect on larval-larval, larval-pupal, or pupal-adult molting. The elytra of the resulting adults, however, were shorter, wrinkled, warped, fenestrated, and less rigid than those from control insects. TcCPR27-deficient insects could not fold their hindwings properly and died prematurely approximately one week after eclosion, probably because of dehydration. TcCPR18-deficient insects exhibited a similar but less dramatic phenotype. Immunolocalization studies confirmed the presence of TcCPR27 in the elytral cuticle. These results demonstrate that TcCPR27 and TcCPR18 are major structural proteins in the rigid elytral, dorsal thoracic, and ventral abdominal cuticles of the red flour beetle, and that both proteins are required for morphogenesis of the beetle's elytra.

Original languageEnglish
Article numbere1002682
JournalPLoS genetics
Volume8
Issue number4
DOIs
Publication statusPublished - Apr 1 2012

Fingerprint

Beetles
beetle
Coleoptera
Tribolium castaneum
cuticle
protein
structural proteins
Proteins
insect
proteins
Insects
Flour
insect cuticle
insects
dehydration (animal physiology)
insect control
double-stranded RNA
chest
chitin
Tribolium

All Science Journal Classification (ASJC) codes

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics
  • Genetics(clinical)
  • Cancer Research

Cite this

Arakane, Y., Lomakin, J., Gehrke, S. H., Hiromasa, Y., Tomich, J. M., Muthukrishnan, S., ... Kanost, M. R. (2012). Formation of rigid, non-flight forewings (Elytra) of a beetle requires two major cuticular proteins. PLoS genetics, 8(4), [e1002682]. https://doi.org/10.1371/journal.pgen.1002682

Formation of rigid, non-flight forewings (Elytra) of a beetle requires two major cuticular proteins. / Arakane, Yasuyuki; Lomakin, Joseph; Gehrke, Stevin H.; Hiromasa, Yasuaki; Tomich, John M.; Muthukrishnan, Subbaratnam; Beeman, Richard W.; Kramer, Karl J.; Kanost, Michael R.

In: PLoS genetics, Vol. 8, No. 4, e1002682, 01.04.2012.

Research output: Contribution to journalArticle

Arakane, Y, Lomakin, J, Gehrke, SH, Hiromasa, Y, Tomich, JM, Muthukrishnan, S, Beeman, RW, Kramer, KJ & Kanost, MR 2012, 'Formation of rigid, non-flight forewings (Elytra) of a beetle requires two major cuticular proteins', PLoS genetics, vol. 8, no. 4, e1002682. https://doi.org/10.1371/journal.pgen.1002682
Arakane, Yasuyuki ; Lomakin, Joseph ; Gehrke, Stevin H. ; Hiromasa, Yasuaki ; Tomich, John M. ; Muthukrishnan, Subbaratnam ; Beeman, Richard W. ; Kramer, Karl J. ; Kanost, Michael R. / Formation of rigid, non-flight forewings (Elytra) of a beetle requires two major cuticular proteins. In: PLoS genetics. 2012 ; Vol. 8, No. 4.
@article{25dc58c198454d48a6d0b73f3cd08ea8,
title = "Formation of rigid, non-flight forewings (Elytra) of a beetle requires two major cuticular proteins",
abstract = "Insect cuticle is composed primarily of chitin and structural proteins. To study the function of structural cuticular proteins, we focused on the proteins present in elytra (modified forewings that become highly sclerotized and pigmented covers for the hindwings) of the red flour beetle, Tribolium castaneum. We identified two highly abundant proteins, TcCPR27 (10 kDa) and TcCPR18 (20 kDa), which are also present in pronotum and ventral abdominal cuticles. Both are members of the Rebers and Riddiford family of cuticular proteins and contain RR2 motifs. Transcripts for both genes dramatically increase in abundance at the pharate adult stage and then decline quickly thereafter. Injection of specific double-stranded RNAs for each gene into penultimate or last instar larvae had no effect on larval-larval, larval-pupal, or pupal-adult molting. The elytra of the resulting adults, however, were shorter, wrinkled, warped, fenestrated, and less rigid than those from control insects. TcCPR27-deficient insects could not fold their hindwings properly and died prematurely approximately one week after eclosion, probably because of dehydration. TcCPR18-deficient insects exhibited a similar but less dramatic phenotype. Immunolocalization studies confirmed the presence of TcCPR27 in the elytral cuticle. These results demonstrate that TcCPR27 and TcCPR18 are major structural proteins in the rigid elytral, dorsal thoracic, and ventral abdominal cuticles of the red flour beetle, and that both proteins are required for morphogenesis of the beetle's elytra.",
author = "Yasuyuki Arakane and Joseph Lomakin and Gehrke, {Stevin H.} and Yasuaki Hiromasa and Tomich, {John M.} and Subbaratnam Muthukrishnan and Beeman, {Richard W.} and Kramer, {Karl J.} and Kanost, {Michael R.}",
year = "2012",
month = "4",
day = "1",
doi = "10.1371/journal.pgen.1002682",
language = "English",
volume = "8",
journal = "PLoS Genetics",
issn = "1553-7390",
publisher = "Public Library of Science",
number = "4",

}

TY - JOUR

T1 - Formation of rigid, non-flight forewings (Elytra) of a beetle requires two major cuticular proteins

AU - Arakane, Yasuyuki

AU - Lomakin, Joseph

AU - Gehrke, Stevin H.

AU - Hiromasa, Yasuaki

AU - Tomich, John M.

AU - Muthukrishnan, Subbaratnam

AU - Beeman, Richard W.

AU - Kramer, Karl J.

AU - Kanost, Michael R.

PY - 2012/4/1

Y1 - 2012/4/1

N2 - Insect cuticle is composed primarily of chitin and structural proteins. To study the function of structural cuticular proteins, we focused on the proteins present in elytra (modified forewings that become highly sclerotized and pigmented covers for the hindwings) of the red flour beetle, Tribolium castaneum. We identified two highly abundant proteins, TcCPR27 (10 kDa) and TcCPR18 (20 kDa), which are also present in pronotum and ventral abdominal cuticles. Both are members of the Rebers and Riddiford family of cuticular proteins and contain RR2 motifs. Transcripts for both genes dramatically increase in abundance at the pharate adult stage and then decline quickly thereafter. Injection of specific double-stranded RNAs for each gene into penultimate or last instar larvae had no effect on larval-larval, larval-pupal, or pupal-adult molting. The elytra of the resulting adults, however, were shorter, wrinkled, warped, fenestrated, and less rigid than those from control insects. TcCPR27-deficient insects could not fold their hindwings properly and died prematurely approximately one week after eclosion, probably because of dehydration. TcCPR18-deficient insects exhibited a similar but less dramatic phenotype. Immunolocalization studies confirmed the presence of TcCPR27 in the elytral cuticle. These results demonstrate that TcCPR27 and TcCPR18 are major structural proteins in the rigid elytral, dorsal thoracic, and ventral abdominal cuticles of the red flour beetle, and that both proteins are required for morphogenesis of the beetle's elytra.

AB - Insect cuticle is composed primarily of chitin and structural proteins. To study the function of structural cuticular proteins, we focused on the proteins present in elytra (modified forewings that become highly sclerotized and pigmented covers for the hindwings) of the red flour beetle, Tribolium castaneum. We identified two highly abundant proteins, TcCPR27 (10 kDa) and TcCPR18 (20 kDa), which are also present in pronotum and ventral abdominal cuticles. Both are members of the Rebers and Riddiford family of cuticular proteins and contain RR2 motifs. Transcripts for both genes dramatically increase in abundance at the pharate adult stage and then decline quickly thereafter. Injection of specific double-stranded RNAs for each gene into penultimate or last instar larvae had no effect on larval-larval, larval-pupal, or pupal-adult molting. The elytra of the resulting adults, however, were shorter, wrinkled, warped, fenestrated, and less rigid than those from control insects. TcCPR27-deficient insects could not fold their hindwings properly and died prematurely approximately one week after eclosion, probably because of dehydration. TcCPR18-deficient insects exhibited a similar but less dramatic phenotype. Immunolocalization studies confirmed the presence of TcCPR27 in the elytral cuticle. These results demonstrate that TcCPR27 and TcCPR18 are major structural proteins in the rigid elytral, dorsal thoracic, and ventral abdominal cuticles of the red flour beetle, and that both proteins are required for morphogenesis of the beetle's elytra.

UR - http://www.scopus.com/inward/record.url?scp=84860583822&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84860583822&partnerID=8YFLogxK

U2 - 10.1371/journal.pgen.1002682

DO - 10.1371/journal.pgen.1002682

M3 - Article

VL - 8

JO - PLoS Genetics

JF - PLoS Genetics

SN - 1553-7390

IS - 4

M1 - e1002682

ER -