Brochosomins and other novel proteins from brochosomes of leafhoppers (Insecta, Hemiptera, Cicadellidae)

Roman Rakitov, Alexander A. Moysa, Arthur T. Kopylov, Sergei A. Moshkovskii, Ralph S. Peters, Karen Meusemann, Bernhard Misof, Christopher H Dietrich, Kevin Paul Johnson, Lars Podsiadlowski, Kimberly K.O. Walden

Research output: Contribution to journalArticle

Abstract

Brochosomes (BS) are secretory granules resembling buckyballs, produced intracellularly in specialized glandular segments of the Malpighian tubules and forming superhydrophobic coatings on the integuments of leafhoppers (Hemiptera, Cicadellidae). Their composition is poorly known. Using a combination of SDS-PAGE, LC-MS/MS, next-generation sequencing (RNAseq) and bioinformatics we demonstrate that the major structural component of BS of the leafhopper Graphocephala fennahi Young is a novel family of 21–40-kDa secretory proteins, referred to herein as brochosomins (BSM), apparently cross-linked by disulfide bonds. At least 28 paralogous BSM were identified in a transcriptome assembly of this species, most of which were detected in BS. Multiple additional BS-associated proteins (BSAP), possibly loosely attached to the outer and inner surfaces of BS, were also identified; some of these were glycine-, tyrosine- and proline-rich. BSM and BSAP together accounted for half of the 100 most expressed transcripts in the Malpighian tubules of G. fennahi. Except for several minor BSAP possibly related to cyclases, BSM and BSAP had no homologs among known proteins, thus representing taxonomically restricted gene families (orphans). Searching in 50 whole-body transcriptome assemblies of Hemiptera found homologs of BSM in representatives of all five families of the superfamily Membracoidea (Cicadellidae, Myerslopiidae, Aetalionidae, Membracidae, and Melizoderidae), but not in other lineages. Among the identified proteins only BSM were shared in common between all 17 surveyed leafhoppers known to produce BS. Combined CHN elemental and aminoacid analyses estimated the total protein content of BS from the integument of G. fennahi to be 60–70%.

Original languageEnglish (US)
Pages (from-to)10-17
Number of pages8
JournalInsect Biochemistry and Molecular Biology
Volume94
DOIs
StatePublished - Mar 1 2018

Fingerprint

Hemiptera
Cicadellidae
Insecta
Graphocephala fennahi
Insects
Proteins
proteins
Malpighian Tubules
Malpighian tubules
integument
transcriptome
Membracoidea
Transcriptome
fullerene
Membracidae
Fullerenes
secretory granules
disulfide bonds
glycine (amino acid)
bioinformatics

Keywords

  • Expression analysis
  • Insect
  • Malpighian tubules
  • Novel protein families
  • Orphan genes
  • Proteomics
  • RNA-Seq
  • Secretory granules
  • Taxonomically restricted genes
  • Transcriptomes

ASJC Scopus subject areas

  • Biochemistry
  • Molecular Biology
  • Insect Science

Cite this

Rakitov, R., Moysa, A. A., Kopylov, A. T., Moshkovskii, S. A., Peters, R. S., Meusemann, K., ... Walden, K. K. O. (2018). Brochosomins and other novel proteins from brochosomes of leafhoppers (Insecta, Hemiptera, Cicadellidae). Insect Biochemistry and Molecular Biology, 94, 10-17. https://doi.org/10.1016/j.ibmb.2018.01.001

Brochosomins and other novel proteins from brochosomes of leafhoppers (Insecta, Hemiptera, Cicadellidae). / Rakitov, Roman; Moysa, Alexander A.; Kopylov, Arthur T.; Moshkovskii, Sergei A.; Peters, Ralph S.; Meusemann, Karen; Misof, Bernhard; Dietrich, Christopher H; Johnson, Kevin Paul; Podsiadlowski, Lars; Walden, Kimberly K.O.

In: Insect Biochemistry and Molecular Biology, Vol. 94, 01.03.2018, p. 10-17.

Research output: Contribution to journalArticle

Rakitov, R, Moysa, AA, Kopylov, AT, Moshkovskii, SA, Peters, RS, Meusemann, K, Misof, B, Dietrich, CH, Johnson, KP, Podsiadlowski, L & Walden, KKO 2018, 'Brochosomins and other novel proteins from brochosomes of leafhoppers (Insecta, Hemiptera, Cicadellidae)', Insect Biochemistry and Molecular Biology, vol. 94, pp. 10-17. https://doi.org/10.1016/j.ibmb.2018.01.001
Rakitov, Roman ; Moysa, Alexander A. ; Kopylov, Arthur T. ; Moshkovskii, Sergei A. ; Peters, Ralph S. ; Meusemann, Karen ; Misof, Bernhard ; Dietrich, Christopher H ; Johnson, Kevin Paul ; Podsiadlowski, Lars ; Walden, Kimberly K.O. / Brochosomins and other novel proteins from brochosomes of leafhoppers (Insecta, Hemiptera, Cicadellidae). In: Insect Biochemistry and Molecular Biology. 2018 ; Vol. 94. pp. 10-17.
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abstract = "Brochosomes (BS) are secretory granules resembling buckyballs, produced intracellularly in specialized glandular segments of the Malpighian tubules and forming superhydrophobic coatings on the integuments of leafhoppers (Hemiptera, Cicadellidae). Their composition is poorly known. Using a combination of SDS-PAGE, LC-MS/MS, next-generation sequencing (RNAseq) and bioinformatics we demonstrate that the major structural component of BS of the leafhopper Graphocephala fennahi Young is a novel family of 21–40-kDa secretory proteins, referred to herein as brochosomins (BSM), apparently cross-linked by disulfide bonds. At least 28 paralogous BSM were identified in a transcriptome assembly of this species, most of which were detected in BS. Multiple additional BS-associated proteins (BSAP), possibly loosely attached to the outer and inner surfaces of BS, were also identified; some of these were glycine-, tyrosine- and proline-rich. BSM and BSAP together accounted for half of the 100 most expressed transcripts in the Malpighian tubules of G. fennahi. Except for several minor BSAP possibly related to cyclases, BSM and BSAP had no homologs among known proteins, thus representing taxonomically restricted gene families (orphans). Searching in 50 whole-body transcriptome assemblies of Hemiptera found homologs of BSM in representatives of all five families of the superfamily Membracoidea (Cicadellidae, Myerslopiidae, Aetalionidae, Membracidae, and Melizoderidae), but not in other lineages. Among the identified proteins only BSM were shared in common between all 17 surveyed leafhoppers known to produce BS. Combined CHN elemental and aminoacid analyses estimated the total protein content of BS from the integument of G. fennahi to be 60–70{\%}.",
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AU - Moysa, Alexander A.

AU - Kopylov, Arthur T.

AU - Moshkovskii, Sergei A.

AU - Peters, Ralph S.

AU - Meusemann, Karen

AU - Misof, Bernhard

AU - Dietrich, Christopher H

AU - Johnson, Kevin Paul

AU - Podsiadlowski, Lars

AU - Walden, Kimberly K.O.

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KW - Novel protein families

KW - Orphan genes

KW - Proteomics

KW - RNA-Seq

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KW - Taxonomically restricted genes

KW - Transcriptomes

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