Analysis of the differentiation of Kenyon cell subtypes using three mushroom body-preferential genes during metamorphosis in the honeybee (Apis mellifera L.)

Shota Suenami, Rajib Kumar Paul, Hideaki Takeuchi, Genta Okude, Tomoko Fujiyuki, Kenichi Shirai, Takeo Kubo

Research output: Contribution to journalArticle

6 Citations (Scopus)

Abstract

The adult honeybee (Apis mellifera L.) mushroom bodies (MBs, a higher center in the insect brain) comprise four subtypes of intrinsic neurons: the class-I large-, middle-, and small-type Kenyon cells (lKCs, mKCs, and sKCs, respectively), and class-II KCs. Analysis of the differentiation of KC subtypes during metamorphosis is important for the better understanding of the roles of KC subtypes related to the honeybee behaviors. In the present study, aiming at identifying marker genes for KC subtypes, we used a cDNA microarray to comprehensively search for genes expressed in an MB-preferential manner in the honeybee brain. Among the 18 genes identified, we further analyzed three genes whose expression was enriched in the MBs: phospholipase C epsilon (PLCe), synaptotagmin 14 (Syt14), and discs large homolog 5 (dlg5). Quantitative reverse transcription-polymerase chain reaction analysis revealed that expression of PLCe, Syt14, and dlg5 was more enriched in the MBs than in the other brain regions by approximately 31-, 6.8-, and 5.6-fold, respectively. In situ hybridization revealed that expression of both Syt14 and dlg5 was enriched in the lKCs but not in the mKCs and sKCs, whereas expression of PLCe was similar in all KC subtypes (the entire MBs) in the honeybee brain, suggesting that Syt14 and dlg5, and PLCe are available as marker genes for the lKCs, and all KC subtypes, respectively. In situ hybridization revealed that expression of PLCe is already detectable in the class-II KCs at the larval fifth instar feeding stage, indicating that PLCe expression is a characteristic common to the larval and adult MBs. In contrast, expression of both Syt14 and dlg5 became detectable at the day three pupa, indicating that Syt14 and dlg5 expressions are characteristic to the late pupal and adult MBs and the lKC specific molecular characteristics are established during the late pupal stages.

Original languageEnglish
Article numbere0157841
JournalPLoS One
Volume11
Issue number6
DOIs
Publication statusPublished - Jun 1 2016
Externally publishedYes

Fingerprint

Synaptotagmins
Mushroom Bodies
mushroom bodies
phospholipase C
Bees
Apis mellifera
cell differentiation
metamorphosis
honey bees
Cell Differentiation
Genes
Brain
brain
genes
in situ hybridization
In Situ Hybridization
Pupa
genetic markers
Polymerase chain reaction
Transcription

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Analysis of the differentiation of Kenyon cell subtypes using three mushroom body-preferential genes during metamorphosis in the honeybee (Apis mellifera L.). / Suenami, Shota; Paul, Rajib Kumar; Takeuchi, Hideaki; Okude, Genta; Fujiyuki, Tomoko; Shirai, Kenichi; Kubo, Takeo.

In: PLoS One, Vol. 11, No. 6, e0157841, 01.06.2016.

Research output: Contribution to journalArticle

Suenami, Shota ; Paul, Rajib Kumar ; Takeuchi, Hideaki ; Okude, Genta ; Fujiyuki, Tomoko ; Shirai, Kenichi ; Kubo, Takeo. / Analysis of the differentiation of Kenyon cell subtypes using three mushroom body-preferential genes during metamorphosis in the honeybee (Apis mellifera L.). In: PLoS One. 2016 ; Vol. 11, No. 6.
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