Skip to main content
Advertisement

Main menu

  • Home
  • Articles
    • Accepted manuscripts
    • Issue in progress
    • Latest complete issue
    • Issue archive
    • Archive by article type
    • Special issues
    • Subject collections
    • Sign up for alerts
  • About us
    • About Development
    • About the Node
    • Editors and Board
    • Editor biographies
    • Travelling Fellowships
    • Grants and funding
    • Journal Meetings
    • Workshops
    • The Company of Biologists
    • Journal news
  • For authors
    • Submit a manuscript
    • Aims and scope
    • Presubmission enquiries
    • Article types
    • Manuscript preparation
    • Cover suggestions
    • Editorial process
    • Promoting your paper
    • Open Access
    • Biology Open transfer
  • Journal info
    • Journal policies
    • Rights and permissions
    • Media policies
    • Reviewer guide
    • Sign up for alerts
  • Contacts
    • Contacts
    • Subscriptions
    • Feedback
  • COB
    • About The Company of Biologists
    • Development
    • Journal of Cell Science
    • Journal of Experimental Biology
    • Disease Models & Mechanisms
    • Biology Open

User menu

  • Log in

Search

  • Advanced search
Development
  • COB
    • About The Company of Biologists
    • Development
    • Journal of Cell Science
    • Journal of Experimental Biology
    • Disease Models & Mechanisms
    • Biology Open

supporting biologistsinspiring biology

Development

  • Log in
Advanced search

RSS  Twitter  Facebook  YouTube 

  • Home
  • Articles
    • Accepted manuscripts
    • Issue in progress
    • Latest complete issue
    • Issue archive
    • Archive by article type
    • Special issues
    • Subject collections
    • Sign up for alerts
  • About us
    • About Development
    • About the Node
    • Editors and Board
    • Editor biographies
    • Travelling Fellowships
    • Grants and funding
    • Journal Meetings
    • Workshops
    • The Company of Biologists
    • Journal news
  • For authors
    • Submit a manuscript
    • Aims and scope
    • Presubmission enquiries
    • Article types
    • Manuscript preparation
    • Cover suggestions
    • Editorial process
    • Promoting your paper
    • Open Access
    • Biology Open transfer
  • Journal info
    • Journal policies
    • Rights and permissions
    • Media policies
    • Reviewer guide
    • Sign up for alerts
  • Contacts
    • Contacts
    • Subscriptions
    • Feedback
Research Article
Integration of complex larval chemosensory organs into the adult nervous system of Drosophila
Nanaë Gendre, Karin Lüer, Sandrine Friche, Nicola Grillenzoni, Ariane Ramaekers, Gerhard M. Technau, Reinhard F. Stocker
Development 2004 131: 83-92; doi: 10.1242/dev.00879
Nanaë Gendre
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Karin Lüer
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Sandrine Friche
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Nicola Grillenzoni
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Ariane Ramaekers
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Gerhard M. Technau
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Reinhard F. Stocker
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • Article
  • Figures & tables
  • Info & metrics
  • PDF
Loading

Article Figures & Tables

Figures

  • Tables
  •     Fig. 5.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Fig. 5.

    Fate of pharyngeal sensory neurons through metamorphosis. Persisting neurons are shown in color, neurons undergoing apoptosis in black, and newly born neurons with a dot. Individual sensilla are shown as arrowhead symbols. (A) Third larval instar: the dorsal pharyngeal sense organ (dps) consists of two groups of neurons, a and p1. Precise numbers of sensilla in the dps, dpo (dorsal pharyngeal organ) and vps (ventral pharyngeal sense organ) are unclear. lbn, labial nerve; lrn, labral nerve; pps, posterior pharyngeal sense organ. (B) Adult: the dorsal cibarial sense organ (dcso) corresponds to the conserved pps. The labral sense organ (lso) and the ventral cibarial sense organ (vcso) derive essentially from the dps. However, the vcso also includes two neurons of the dpo. Seven small sensilla of the lso as well as the fishtrap bristles (ftb; numbers in the diagram reduced) are born during metamorphosis. Remaining neurons of the dps and dpo are located along the accessory pharyngeal nerve (apn). pn, pharyngeal nerve.

  •     Fig. 1.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Fig. 1.

    Pharyngeal sense organs in third instar larvae (A,B,G-J) and adults (C-F,K-N) of D. melanogaster, as shown by the P[GAL4] driver line MJ94, expressed in all pharyngeal neurons (all panels except H,L) and the prosV1 line, which labels subsets of accessory cells (H,L). Expression patterns are shown by the reporters lacZ (A-F: blue) or mCD8-GFP (G-N: green). Neuronal nuclei in G-N are labeled with anti-Elav antibody (red). (A) The larval pharynx is equipped with a dorsal and a ventral pharyngeal sense organ located behind the mouth-hooks (dps, vps), and a smaller sense organ far more posterior (pps), in a region characterized by cuticular ridges (ri). Additional expression is seen in Bolwig's organ (bo), in the presumed dorsal pharyngeal organ (dpo) and in the dorsal and terminal organs (do, to). (B) The pps is composed of an anterior and a posterior sensillum (a, p). (C) The adult pharynx comprises the dorsal and ventral cibarial sense organs (dcso, vcso) and the labral sense organ (lso). MJ94 drives expression also in maxillary palp sensilla (ms) and in labial palp taste bristles (tb). Higher magnifications reveal an anterior and a posterior sensillum in the dcso (D: a, p), three sensilla in the vcso (E: 1-3) and nine sensilla in the lso (F: 1-9; opposite lso shown on top). Label occurs also in the neurons of the fishtrap bristles (E: ftb). Both the larval pps (G,H) and the adult dcso (K,L) are composed of two sensilla (G,K: arrows) of three neurons each. In both sense organs, prosV1 labels two accessory cells (H,L: arrowheads). The larval dps (I) and vps (J) contain 17-18 and 16 neurons, respectively. The dps is accompanied further back by the dorsal pharyngeal organ (I: dpo). (M) In the adult, the vcso includes three sensilla (1-3) comprising eight neurons (between arrowheads). The vcso is accompanied by two rows of mononeuronal fishtrap bristles (ftb) and by a few extra neurons (arrows). (N) The nine sensilla of the lso contain a total of 18 neurons. (A,B,F,G) Lateral view, distal to the left. (C-E,H-N) Frontal view, distal to the bottom. Scale bars, 100 μm (A,C), 50 μm (N), 40 μm (D-F), 20 μm (B,G-M)

  •     Fig. 2.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Fig. 2.

    Embryonic origin of subsets of neurons and nonneuronal cells in the pharyngeal sense organs, as shown by HRP injection at the syncytial blastoderm stage (A D) and by FLPout (Wong et al., 2002) induced in F1 embryos of the cross MJ94 × y w hs-flp; Sp/CyO; UAS>CD2 y+>mCD8-GFP (E-L). (E-L) Neuronal nuclei are labeled with anti-Elav antibody (red). (A-C′) HRP product is present in dendritic tips of the lso sensillum 7 (A: arrow) and of the vcso (B: arrow), as well as in dendrites, cell bodies and axons of dcso neurons (consecutive sections C,C′: arrows). (D) Fishtrap bristles labeled by MJ94/UAS-lacZ (arrows) lack HRP staining, in contrast to the vcso (arrowhead). (E-I) When FLPouts are induced in the MJ94 line at 12-24 hours after egg laying (AEL), single neurons are labeled in the lso, in both sensillum 7 (composed of eight neurons) (E-G: 7) and the mononeuronal sensilla 1-6 (G: 3). By contrast, the bineuronal sensilla 8 and 9 always exhibit paired labeled neurons (H,I: arrows). Simultaneous labeling of two sensilla suggests the occurrence of two independent FLPout events (F,G). (J) FLPouts induced earlier (6-18 hours AEL) lead to simultaneous label in many neurons (e.g. three in sensillum 7). (K,L) FLPout induced at 12-24 hours AEL invariably leads to single labeled neurons in the multineuronal sensilla of the vcso (K) and dcso (L). The two large neurons in K (arrows) are outside the vcso. ftb, fishtrap bristles. Distal is to the bottom except in (A) in which distal is to the left. F shows both left and right lso. Scale bars, 20 μm (A shows scale for A-D; E shows scale for E-L).

  •     Fig. 3.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Fig. 3.

    Early pupal origin of subsets of neuronal and non-neuronal cells in the adult pharyngeal sense organs, as shown by BrdU incorporation at 3 hours APF in MJ94 (G: 18 hours APF). The patterns were visualized by lacZ expression (blue) in the light microscope (A,B,F,G) or by mCD8-GFP expression (green) in the confocal microscope (C-E,H,I). The anti-BrdU product is shown in brown (A,B,F,G) or red (C-E,H,I). (A-E) In the lso, BrdU label is particularly obvious in the neurons of the distal sensilla 8 and 9. Additional BrdU take-up is visible in the neuron of the mononeuronal sensillum 6 (D) and in subsets of accessory cells (C-E: arrows). (F-I) In both vcso (F,H) and dcso (G,I), two accessory cells (arrowheads) but none of the neurons (large arrows) are BrdU positive. However, BrdU label is present in the neurons of the fishtrap bristles (H: small arrows). Asterisks in G,H indicate BrdU uptake in cells of the pharyngeal wall. (A,C,D,E) Sagittal sections; all others panels represent frontal views. Dots indicate midline. Distal is to the left (A-E) or to the bottom (F-I). Scale bars, 10 μm (F,G), 20 μm (A,B,H), 40 μm (C-E,I).

  •     Fig. 4.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Fig. 4.

    Metamorphic transformation of pharyngeal sense organs, as shown by MJ94/UAS-mCD8-GFP (green). Red indicates the Elav marker except in E,F, in which it indicates α-caspase antibody. Stages are indicated in hours APF. (A-C) The pps maintains two sensilla throughout metamorphosis (arrows) each comprising three differentiated neurons, and becomes the dcso. (D-F) By contrast, the vps disintegrates in the early pupa and its neurons lose Elav immunoreactivity (D: arrows) or give rise to Elav-positive debris (D: arrowheads). Evidence for apoptosis is shown by staining with anti-caspase antibody (E). Neuronal identity of the apoptotic cells is indicated by mCD8 expression in the same optical section (E′). By contrast, anti-caspase antibody does not bind to the neurons of the dps (F,F′). (G-I) The dps with its clusters a and p1 is joined by two additional neurons (p2) from the dpo, forming a dps complex (dps c.). (J-O) Later on, the dps c. splits into two distinct sense organs, vcso and lso. The vcso includes p1 and p2, with six and two neurons, respectively (J-L). The p1 cluster comprises the distal and middle sensilla of the vcso, and the p2 cluster comprises the proximal sensillum. Five to six additional neurons deriving from dps and dpo remain outside the vcso (J-L: asterisks). At 24 hours APF, the neurons of the fishtrap bristles appear (L: arrowheads). In the lso, the a cluster (consisting of nine neurons) will form sensillum 7 (eight neurons; M: arrowheads) and an extra mononeuronal sensillum (M: small arrow). An additional nine neurons appear in the distal part of the lso (M,N: large arrows), four of which are associated with bineuronal sensilla 8 and 9 (M-O: asterisks). White dots indicate midline; distal is to the bottom except in F,F′, in which distal is to the left. Scale bar, 20 μm.

Tables

  • Figures
  • Table 1.

    Adult pharyngeal sense organs: neuronal composition, function and expression pattern of P[GAL4] lines used

    Total number of Elav-positive cells Number of GAL4-expressing cells
    Sense organSensillum typeNumber of neuronsFunctionCSMJ94MJ94prosV1
    dcsoPosterior3Gustatory6 (n=4)6 (n=15)60
    Anterior3Gustatory
    Accessory cells02
    Proximal*2*Gustatory*?
    vcsoMiddle2Gustatory8 (n=11)8 (n=9)80
    Distal4Gustatory
    Accessory cells03
    lso1-66×1Mechanosensory
    78Gustatory18 (n=11)18 (n=7)180
    82Gustatory and mechanosensoryor 19 (n=2)
    92Gustatory and mechanosensory
    Large/small accessory cells03/8
    Fishtrap bristles (two rows)Eighteen to 23 sensillaOne eachMechanosensoryOne eachOne eachOne each0
    Accessory cells0One each
    • Data in columns 2-4 are from Nayak and Singh (1985), except * (this paper).

  • Table 2.

    Clones induced in pharyngeal sensilla by hs flip-out in the MJ94 line

    Flip-out induced 12-24 hours AEL Number of labeled neurons observed
    Sense organSensillum type (neuron number)12Flip-out induced early (6-18 hours AEL)
    dcsoPosterior (3)5×0×
    Anterior (3)4×0×
    vcsoProximal (2)
    Middle (2)9×0×1×: 2 neurons
    Distal (4)
    lso1 (1)1×0×
    2 (1)1×0×
    3 (1)5×0×
    4 (1)3×0×
    5 (1)3×0×
    6 (1)6×0×
    7 (8)14×1×1×: 3 neurons
    8 (2)0×3×*
    9 (2)1׆,‡2׆
    Fishtrap bristlesProximal (1)0×0×
    Distal (1)0×0×
    • The three sensilla of the VCSO were not identified in the flip-outs.

      Total number of left/right sides observed is 86.

    • ↵* Two of the cases were induced at 12-18 hours after egg laying (AEL), one case at 18-24 hours AEL

    • ↵† Induced at 12-18 hours AEL

    • ↵‡ Perhaps caused by abnormal loss of second neuron

Previous ArticleNext Article
Back to top
Previous ArticleNext Article

This Issue

 Download PDF

Email

Thank you for your interest in spreading the word on Development.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
Integration of complex larval chemosensory organs into the adult nervous system of Drosophila
(Your Name) has sent you a message from Development
(Your Name) thought you would like to see the Development web site.
Share
Research Article
Integration of complex larval chemosensory organs into the adult nervous system of Drosophila
Nanaë Gendre, Karin Lüer, Sandrine Friche, Nicola Grillenzoni, Ariane Ramaekers, Gerhard M. Technau, Reinhard F. Stocker
Development 2004 131: 83-92; doi: 10.1242/dev.00879
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Research Article
Integration of complex larval chemosensory organs into the adult nervous system of Drosophila
Nanaë Gendre, Karin Lüer, Sandrine Friche, Nicola Grillenzoni, Ariane Ramaekers, Gerhard M. Technau, Reinhard F. Stocker
Development 2004 131: 83-92; doi: 10.1242/dev.00879

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Alerts

Please log in to add an alert for this article.

Sign in to email alerts with your email address

Article navigation

  • Top
  • Article
    • Summary
    • Introduction
    • Materials and methods
    • Results
    • Discussion
    • Acknowledgments
    • Footnotes
    • References
  • Figures & tables
  • Info & metrics
  • PDF

Related articles

Cited by...

More in this TOC section

  • The plakin domain of C. elegans VAB-10/plectin acts as a hub in a mechanotransduction pathway to promote morphogenesis
  • A biphasic role of non-canonical Wnt16 signaling during early anterior-posterior patterning and morphogenesis of the sea urchin embryo
  • Minimal in vivo requirements for developmentally regulated cardiac long intergenic non-coding RNAs
Show more RESEARCH ARTICLES

Similar articles

Other journals from The Company of Biologists

Journal of Cell Science

Journal of Experimental Biology

Disease Models & Mechanisms

Biology Open

Advertisement

Interviews — Bénédicte Sanson and Kate Storey

Bénédicte Sanson and Kate Storey

Hear from Bénédicte Sanson, winner of the BSDB’s Cheryll Tickle medal, and Kate Storey, winner of the BSDB’s Waddington Medal, as they discuss their research, the future of the field and the importance of collaboration.


Review Commons launches

We're excited to be an affiliate journal for Review Commons, the ASAPbio/EMBO platform for high-quality journal-independent peer-review in the life sciences, which went live on 09 December.


Have you heard about our Travelling Fellowships?

Peter Baillie-Johnson in Switzerland

Early-career researchers can apply for up to £2,500 to offset the cost of travel and expenses to make collaborative visits to other labs around the world. Read about Peter’s experience in Switzerland, where he joined forces with the Lutolf lab to refine a protocol for producing gastruloids.


Publishing peer review reports

To continue working towards transparency around the editorial process, Development now publishes a ‘Peer review history file’ alongside published papers. Read more about the policy and see the reports for yourself in one the first papers to publish the reports (under the ‘Info & metrics’ tab).


Development at a glance — Cell interactions in collective cell migration

Extract from the poster showing specific cell-cell interactions in metastasis.

Take a look at the latest poster and accompanying article by Denise Montell and her colleagues from the University of California, where they describe a sampling of both known and new cells that migrate collectively in vivo.

Articles

  • Accepted manuscripts
  • Issue in progress
  • Latest complete issue
  • Issue archive
  • Archive by article type
  • Special issues
  • Subject collections
  • Sign up for alerts

About us

  • About Development
  • About the Node
  • Editors and board
  • Editor biographies
  • Travelling Fellowships
  • Grants and funding
  • Journal Meetings
  • Workshops
  • The Company of Biologists

For authors

  • Submit a manuscript
  • Aims and scope
  • Presubmission enquiries
  • Article types
  • Manuscript preparation
  • Cover suggestions
  • Editorial process
  • Promoting your paper
  • Open Access
  • Biology Open transfer

Journal info

  • Journal policies
  • Rights and permissions
  • Media policies
  • Reviewer guide
  • Sign up for alerts

Contact

  • Contact Development
  • Subscriptions
  • Advertising
  • Feedback

 Twitter   YouTube   LinkedIn

© 2019   The Company of Biologists Ltd   Registered Charity 277992