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First published online 16 September 2003
doi: 10.1242/dev.00727

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Extracellular cues and pioneers act together to guide axons in the ventral cord of C. elegans

Max Planck Institute for Medical Research, Jahnstrasse 29, 69120 Heidelberg, Germany

View larger version (37K): [in a new window]   Fig. 1. Ventral cord development. (A-C) Trajectories of various axons in the ventral cord. Ventral aspect, anterior towards the left. (A) RIF axons pioneer the pathway from the anterior end of the ventral cord towards the nerve ring. RIF axons cross the ventral midline (a) and enter the nerve ring on the contralateral side (not shown). The AVG cell body is next to the RIF cell bodies in the retrovesicular ganglion (rvg). The AVG axon pioneers the right ventral cord axon tract. PVP cell bodies lie at the posterior end of the ventral cord. Their axons also cross the ventral midline (b) to grow anteriorly in the contralateral ventral cord tract, i.e. the PVPL axon grow in the right axon tract, and the PVPR axon in the left tract. The PVPR axon pioneers the left ventral cord axon tract. (B) Almost all interneuron axons growing out of the nerve ring cross over to the right side exactly where the RIF neurons crossed earlier (a). Motoneuron cell bodies lie on the ventral midline and send their axons into the right axon tract (b). DA and DB motoneuron commissure grow straight out of the cell body towards the dorsal cord (c), some on the left and others on the right side (not shown). DD motoneuron commissures branch off the ventral cord axon and always grow on the right side (d). (C) Overlay of A and B. (D) Ventral cord cross-section illustrating the position of axons within the ventral cord as well as the order of outgrowth (numbers in circles). Early outgrowing axons (AVG, DD) tend to be dorsally close to the basement membrane, whereas later outgrowing axons (DA/DB, interneurons) occupy central and ventral positions. Modified, with permission, from White et al. (White et al., 1986).

View larger version (81K): [in a new window]   Fig. 2. Left-right asymmetry of the ventral cord. (A,B) Wild-type animal. RIF neurons and AVG are labeled with odr-2::CFP (A), interneurons with glr-1::GFP, DA/DB motoneurons with unc-129::YFP (B). RIF axons extend anteriorly into the nerve ring crossing the ventral midline (arrowhead, RIF cell bodies are marked with asterisks. Later outgrowing interneuron axons cross over into the right axon tract at the same position (arrowhead in B). (C,D) Animal in which RIFR/L, SABVR/L and RIGR/L have been ablated, labeled with odr-2::CFP (C) and glr-1::DsRed (D). (C) Absence of the RIF neurons (compare with A); only AVG is still present. (D) Interneuron axons still cross over into the right axon tract (arrowhead). (E,F) Wild-type (E) and nid-1(ur41) mutant animals (F) labeled with a pan-neuronal marker (evIs111). (E) The majority of the axons extends in the right axon tract. (F) Almost half of the axons extend in the left tract in the nid-1 mutant (arrows). All animals show a ventral aspect with anterior towards the left. Scale bars: 10 µm.

View larger version (58K): [in a new window]   Fig. 3. Ventral cord defects in lin-11(n389) mutants. (A-D) Wild type, ventral cord with interneurons and motoneurons labeled with different GFP variants: (A-C) single color marker, (D) overlay. (E-H) Ventral cord defects in lin-11(n389), same labels and arrangement as in A-D. Arrowheads indicate axons inappropriately crossing the ventral midline. (I,J) Wild type (I) and lin-11(n389) mutant (J), DA/DB motoneurons labeled. Arrowheads in J indicate commissures growing out on the wrong side. All animals are shown from a ventral aspect with anterior towards the left. Scale bars: 10 µm in A-H; 20 µm in I,J. Markers shown are unc-129::CFP (dark blue in A,D,E,H, gray in I,J), glr-1::GFP (green in B,D,F,H), unc-47::DsRed (red in C,D,G,H).

View larger version (63K): [in a new window]   Fig. 4. AVG and PVP cell type marker expression in lin-11 and unc-30 mutants. (A-D) AVG marker. Ventral aspect of the anterior end of the ventral cord with the retrovesicular ganglion. (A,B) odr-2::GFP, (C,D) glr-1::GFP in wild type (A,C) or lin-11(n389) (B,D). Marker expression is absent in AVG in lin-11(n389) (asterisks in B and D indicate where the AVG cell body should be). (E-H) Expression of odr-2::GFP in the preanal ganglion. (E) wild type; expression is strong in PVPR and PVPL and weakly seen in PVT. (F) unc-30(e191) mutant; expression in PVPR (asterisk) is missing. (G,H) expression in lin-11(n389). Expression levels in PVP neurons are either reduced (G) or expression is completely absent (H, asterisks). Scale bars: 5 µm in A,B,E-H; 10 µm in C,D.

View larger version (60K): [in a new window]   Fig. 5. Correlation of ventral cord defects in various mutants. (A-C) Wild type with PVP and PVQ axon labeled in different colors. (A,B) Single channel, (C) overlay. (D-F) sax-3(ky123) mutant with PVP and PVQ axon labeled in different colors. (D,E) Single channel, (F) overlay. The PVPR axon (D) and the PVQL axon (E) cross the midline repeatedly at the same positions (arrowheads). (G-I) lin-11(n389) mutant with PVQ and interneuron axons labeled differentially. (G,H) Single channels, (I) overlay. PVQL and interneurons cross into the contralateral axon tract at different positions (arrowheads in G and H). (J-L) nid-1(ur41) mutant with PVP and PVQ axon labeled in different colors. (J,K) Single channels, (L) overlay. The AVG and PVPL axons (J) and the PVQR axon (K) cross the midline at the same position (arrowheads) to run together in the left axon tract. (M-O) unc-6(ev400) mutant with PVP/AVG and D-type motoneuron axons labeled differentially, (M,N) Single channels, (O) overlay. The AVG axon crosses the ventral midline to grow in the left axon tract (arrowhead in M), whereas the D-type motoneuron axons all grow out correctly on the right side. All animals are shown from a ventral aspect with anterior towards the left. Scale bars: 10 µm in A-I,M-O; 20 µm in J-L. Markers shown are glr-1::GFP (green in H,I), unc-47::DsRed (red in N,O), odr-2::CFP (light blue in B,C,E,F,J,L,M,O), sra-6::DsRed2 (yellow in A,C,D,F,G,I,K,L).

View larger version (30K): [in a new window]   Fig. 6. The logic of axon outgrowth. The dependencies between early and late outgrowing axons (A), and the importance of extracellular cues for particular classes of axons (B). Arrows indicate the class of axons that is influenced by the extracellular cues or an earlier outgrowing axon. The thickness of the arrow corresponds to the strength of the interaction.